Applying evolutionary biology to address global challenges

DOI 101126science1245993 (2014)346 Science

et alScott P CarrollApplying evolutionary biology to address global challenges

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RESEARCH

17 OCTOBER 2014 bull VOL 346 ISSUE 6207 313SCIENCE sciencemagorg

BACKGROUND Differences among species

in their ability to adapt to environmental

change threaten biodiversity human health

food security and natural resource avail-

ability Pathogens pests and cancers often

quickly evolve resistance to control measures

whereas crops livestock wild species and

human beings often do not adapt

fast enough to cope with

climate change habi-

tat loss toxicants

and lifestyle

change To

addre s s

Applying evolutionary biology to address global challenges

APPLIED EVOLUTION

Scott P Carroll Peter Soslashgaard Joslashrgensen Michael T Kinnison Carl T Bergstrom

R Ford Denison Peter Gluckman Thomas B Smith Sharon Y Strauss Bruce E Tabashnik

Tactics and tools of applied evolutionary biology (Top) Evolutionary tactics to address the

major societal challenges treated in the present study are shown as a wheel Challenges in the

food health and environment sectors are caused by rapid contemporary evolution or in more

slowly reproducing or threatened species phenotype-environment mismatch Gene f ow and

selection agents make challenges in one sector dependent on actions in others Current prog-

ress in implementing tactics of applied evolutionary biology to address challenges varies widely

(Bottom) Many of these tactics use a common toolbox of strategies to prevent unwanted evo-

lution or to reduce f tness in harmful organisms as well as to reduce mismatch between organ-

isms and human-altered environments or to increase group performance in desired organisms

Each of these strategies uses a combination of manipulations of the organismal genotype phe-

notypic plasticity (development) or environmental conditions

REVIEW SUMMARY

these challenges practices based on evolu-

tionary biology can promote sustainable out-

comes via strategic manipulation of genetic

developmental and environmental factors

Successful strategies effectively slow un-

wanted evolution and reduce fitness in costly

species or improve performance of valued

organisms by reducing phenotype-

environment mismatch or

increasing group pro-

ductivity Tactics

of applied

evolution-

ary bi-

ology range broadly from common policies

that promote public health or preserve habi-

tat for threatened speciesmdashbut are easily over-

looked as having an evolutionary rationale to

the engineering of new genomes

ADVANCES The scope and development

of current tactics vary widely In particular

genetic engineering attracts much attention

(and controversy) but now is used mainly

for traits under simple

genetic control Human

gene therapy which

mainly involves more

complex controls has

yet to be applied suc-

cessfully at large scales

In contrast other methods to alter complex

traits are improving These include artificial

selection for drought- and flood-tolerant

crops through bioinformatics and applica-

tion of ldquolife courserdquo approaches in medicine

to reduce human metabolic disorders

Successful control of unwanted evolution

depends on governance initiatives that ad-

dress challenges arising from both natural

and social factors Principal among these

challenges are (i) global transfer of genes

and selection agents (ii) interlinked evo-

lution across traditional sectors of society

(environment food and health) and (iii)

conflicts between individual and group in-

centives that threaten regulation of anti-

biotic use and crop refuges Evolutionarily

informed practices are a newer prospect in

some fields and require more systematic re-

search as well as ethical considerationmdashfor

example in attempts to protect wild species

through assisted migration in the choice of

source populations for restoration or in ge-

netic engineering

OUTLOOK A more unified platform will

better convey the value of evolutionary meth-

ods to the public scientists and decision-

makers For researchers and practitioners

applications may be expanded to other dis-

ciplines such as in the transfer of refuge

strategies that slow resistance evolution in

agriculture to slow unwanted evolution

elsewhere (for example cancer resistance

or harvest-induced evolution) For policy-

makers adoption of practices that minimize

unwanted evolution and reduce phenotype-

environment mismatch in valued species is

likely essential to achieve the forthcoming

Sustainable Development Goals and the

2020 Aichi Biodiversity Targets

The list of author affiliations is available in the full article online

Corresponding author E-mail spcarrollucdavisedu (SPC) psjorgensenbiokudk (PSJ) Cite this Review as Scott P Carroll et al Science 346 1245993 (2014) DOI 101126science1245993

Read the full article at httpdxdoiorg101126science1245993

ON OUR WEB SITE

SECTORS

CHALLENGES

by manipulation ofControl harmful organisms

1) slow unwanted evolution

Protect desirable organisms

3) reduce phenotype- environment mismatch

4) increase group performance2) reduce ftness bull Development

bull Environment

bull Genotype

Implementation

Toolbox

Emergingdiseasesurvei

llance

Integrated pest management

Reduceinbreeding

Cross-sector antibioticreg

ulation

Cross-secto

r antibiotic regulationNatural en

closures

Cancerresistan

ce

Habitat protection

Choice of seed sources

Reducetoxicants

Captivebreeding

programs

Genome-guided breeding strateg

iesHealt

hfuldietampactivitylevel

Restorationsources amp

assisted migration

Drought amp food tolerant GMcrops

Genetherapy

Biodiversity loss

Climate extremes reduceyield

Chronic disease

ENVIRONM

ENT

FOOD

HEALTLLH

Newcancertreatments

Refuge strategies foff r GM crops

Fewer generations incaptivity

Antibioticresistan

ce

Pesticide resistance

EvolutionincaptivityH

EALTLLH

FOOD

ENV

IRONMENT

TACTICS

GE

NE

F

LOW

SELECTIO

N A

GE

NTS

Emerginginfeffctiousdis

ease

Antibiotic resistance

Published by AAAS

REVIEW

APPLIED EVOLUTION

Applying evolutionary biology toaddress global challengesScott P Carroll12dagger Peter Soslashgaard Joslashrgensen34dagger Michael T Kinnison5

Carl T Bergstrom6 R Ford Denison7 Peter Gluckman8 Thomas B Smith910

Sharon Y Strauss11 Bruce E Tabashnik12

Two categories of evolutionary challenges result from escalating human impacts on theplanet The first arises from cancers pathogens and pests that evolve too quickly andthe second from the inability of many valued species to adapt quickly enough Appliedevolutionary biology provides a suite of strategies to address these global challengesthat threaten human health food security and biodiversity This Review highlights bothprogress and gaps in genetic developmental and environmental manipulations acrossthe life sciences that either target the rate and direction of evolution or reduce themismatch between organisms and human-altered environments Increased developmentand application of these underused tools will be vital in meeting current and futuretargets for sustainable development

Human influence on the biosphere (1 2) hasprofound consequences for both the rateand direction of evolution (3) Among theconsequences are the challenges billionsof people face from the effects of cancers

pests and pathogens that adapt quickly to ourinterventions against them At the same timehumans and other organisms that we value foreconomic ecological or aesthetic reasons areoften not able to adapt quickly enough to keeppace with human alterations of the environ-ment These contemporary dilemmas increasinglythreaten human health food security and bi-ological diversity (4ndash12) For example the WorldHealth Organization (WHO) warns that micro-bial resistance to antimicrobial drugs threatensthe achievements of modern medicine (13) Like-wise more than 11000 documented cases of pes-

ticide resistance in nearly 1000 species of insectsweeds and plant pathogens jeopardize agricul-tural economies and food supplies worldwide(14) Failure to adapt may be equally dire andcostly as in the prevalent mismatch betweenmodern human nutritional and lifestyle behav-iors and those of our evolutionary past which isgenerally considered a major contributing factorto the high incidence of obesity and associatedillnesses such as type 2 diabetes mellitus and car-diovascular disease (15) Meanwhile the prospectof Earthrsquos sixth mass extinction of species be-comes imminent as species are unable to adaptquickly enough to environmental change (16) Agrowing application of principles from evolu-tionary biology to challenges such as these mayimprove our ability to meet many of the mostpressing problems of the 21st century (12 17ndash19)Here we review current and prospective ap-

plications of evolutionary biology that may pro-vide solutions for major societal challenges Weexamine management approaches that attempteither to improve or to undermine adaptation tomodern environments by manipulating the rela-tions between the traits of organisms and thepatterns of selection imposed by their environ-ments These manipulations include tools thatmay be widely considered evolutionary such asselective breeding and emerging technologies ingenetics as well as manipulations that are oftenoverlooked as evolutionary specifically manipu-lations of development that modify traits inde-pendent of genetic change and the altering ofenvironments in ways that can modulate selec-tion itself A conceptual framework linking all ofthese genetic developmental and environmentalmanipulations is likely to lead to greater im-plementation and cross-disciplinary integrationof applied evolutionary methods We highlighthow evolutionary strategies may be used to achieve

policy targets of sustainable development for im-proved human health food production naturalresource use and biodiversity conservation in-cluding how stakeholder conflicts may be reducedto achieve desired outcomes Throughout we un-derscore the merits of building a more unifiedand integrated field of applied evolutionary bi-ology to address global challenges

Core evolutionary concepts and theirrelevance to global challenges

Evolution defined as the change in genetic make-up of a population over successive generationsrequires genetic variation which arises from mu-tation and recombination (20) Most importantfor adaptation is genetic variation that affectsvariation in functional traits (21) such that al-ternate genotypes produce alternate phenotypesSelection increases the frequency of genes thatimprove fitnessmdashthe ability to survive and repro-duce The specific genetic basis for most traits isnot known but trait differences among individ-uals typically have a significant heritable (geno-typic) basis This basis includes heritable aspectsof development which also may evolve and giverise to adaptive phenotypic plasticity (22) A pop-ulation with low fitness may experience strongnatural selection that favors better-adapted geno-types However strong selection will not neces-sarily ldquorescuerdquo a population if there are too fewadapted individuals or suitable genes for thepopulation to persist (23) Movement of genesbetween populations (gene flow) and randomchanges in gene frequency in small populations(genetic drift) can also cause evolution and in-fluence the outcome of natural selection (20)These concepts apply not only to organisms frombacteria to humans but also to viruses and cancercells (24)The core concepts of evolutionary biology are

best known for explaining the unity diversityand adaptive characteristics of organisms (17)Phylogenetic methods that establish the related-ness of organisms are central to understandingthe patterns and processes of evolution under-lying the function and diversity of living systems(25) The practical applications of phylogeneticmethods have been thoroughly reviewed by othersand include such diverse objectives as reconstruct-ing invasion routes of harmful organisms conser-vation planning and combating crime (17 26)Here we focus on the manipulation of processesthat determine the adaptedness of individualspopulations and other biological systems in orderto meet management objectives (Fig 1)Agriculture medicine and conservation address

different challenges but nonetheless share com-mon strategies tomanage phenotype-environmentmismatch and the associated risks to populationsexperiencing strong selection (Fig 2) Those strat-egies can be classified as genotypic developmentalor those related to environmental manipulationsThe potential sustainability of such practicesmay be assessed by comparing the intensity ofselection with the adaptive capacity of a targetpopulation (27) For example the widespreaduse of antibiotics that exert strong selection on

RESEARCH

SCIENCE sciencemagorg 17 OCTOBER 2014 bull VOL 346 ISSUE 6207 1245993-1

1Department of Entomology University of California DavisOne Shields Avenue Davis CA 95616 USA 2Institute forContemporary Evolution Davis CA 95616 USA 3Center forMacroecology Evolution and Climate Department of BiologyUniversity of Copenhagen 2100 Copenhagen Denmark4Center for Macroecology Evolution and Climate NaturalHistory Museum of Denmark University of Copenhagen2100 Copenhagen Denmark 5School of Biology and EcologyUniversity of Maine Orono ME 04469 USA 6Department ofBiology University of Washington Seattle WA 98195 USA7Department of Ecology Evolution and Behavior Universityof Minnesota Minneapolis MN 55108 USA 8Centre forHuman Evolution Adaptation and Disease Liggins InstituteUniversity of Auckland Auckland New Zealand 9Departmentof Ecology and Evolutionary Biology University of CaliforniaLos Angeles CA 90095 USA 10Center for TropicalResearch Institute of the Environment and SustainabilityUniversity of California Los Angeles 619 Charles E YoungDrive East Los Angeles 90095-1496 CA 11Department ofEvolution and Ecology and Center for Population BiologyUniversity of California Davis One Shields Avenue CA95616 USA 12Department of Entomology University ofArizona Tucson AZ 85721 USAThese authors contributed equally to this work daggerCorrespondingauthor E-mail spcarrollucdavisedu (SPC) psjorgensenbiokudk (PSJ)

bacteria is typically not sustainable for con-trolling highly adaptable microbe populationsbecause they rapidly evolve resistance (28) Ac-cordingly the sustainability of antibiotic usecan be increased by either reducing selection forexample through regulated use of particularlystrong antibiotics or by attempts to surpass theadaptive capacity ofmicrobes through drug com-binations (29) Below we review successes andemerging methods in applied evolutionary bi-ology highlighting commonalities across thesectors of health food and environmental man-agement (Fig 3)

Successes and prospects in appliedevolutionary biology

Applied evolutionary biology encompasses wide-ly different manipulations that may togetherachieve a broad range of goals From protectingbiodiversity with conventional environmentalmanagement that increases fitness in wild en-vironments to medical recommendations fortraditional diets some methods of applied evo-lutionary biology have a long history of use evenif they are not often seen as evolutionary in na-ture In contrast the synthesis of wholly novelgenomes with emerging technologies representsobvious evolutionary manipulation that deliber-ately adds new organisms to the tree of life but

with little history of application it involves un-known risks and public controversy Here wereview some of the most recent successes andleading prospects for the application of evolu-tionary biology in a progression from relativelywell established methods to underexplored strat-egiesWe first considermanipulations of selectionto improve population productivity and individ-ual health and to delay the emergence of resist-ance (Fig 2) We then examine less developedmethods for the cultivation of populations in-herently preadapted to impending environmen-tal changes and for innovative applications ofgroup selection in crops and wildlife We endthis section with urgent considerations for man-aging evolutionary factors that span disciplinaryboundaries as in cases of emerging zoonoticdisease

Environmental alignment to securebiodiversity and human health

A common application of evolutionary princi-ples is to manage current environments to bemore like the historical habitats in which selec-tion shaped the genetic makeup of humans andother species Conventional habitat protectionand restoration recognize that threatened spe-cies often adapt poorly to changing environmentsin the wild (26 30) Conversely rapid adaptation

to captive rearing programs used to rebuildpopulations of rare species contributes to a 50to 90 failure rate of reintroductions (31) Re-introduction success has been improved with en-closures and rearing methods that mimic wildconditions and by limiting the number of cap-tive generations to minimize adaptation to arti-ficial conditions (32)Some of the most serious noncommunicable

diseases in humans may be prevented by bet-ter aligning current environments with those inwhich our hunter-gatherer ancestors evolved (33)Sedentary modern lifestyles and diets with highndashglycemic index processed foods are increasinglyimplicated in the rapidly rising rates of obesitydiabetes and cardiovascular disorders (34) Thesedisorders are estimated to contribute to abouttwo-thirds of all deaths in Western societies (35)and to a growing proportion of deaths in de-veloping countries (36 37) In 2012 the eco-nomic burden of type 2 diabetes alone wasestimated at $500 billion globally nearly 1of world Gross Domestic Product (38) To restoreconditions to which people are better adaptedphysiologically while retaining the desired ele-ments of a modern lifestyle (35) public healthscientists recommend greater physical activity(39) with reduced consumption of refined carbo-hydrates (36) that is diets and activity levelscloser to those of the past to which we are betteradapted More generally a number of evolution-arily based tools are available to prevent chronicnoncommunicable diseases including the 19of global cancer incidents that WHO attributesto environmental exposure (40) These tools in-clude life-course approaches which manage thetiming and duration of environmental expo-sures to minimize risks of subsequent chronicdisease (41) From a public health standpointenvironmental approaches to disease preven-tion may often be most cost-effective when ap-plied outside of health care settings and whensimultaneously targeting groups of people ratherone individual at a time such as through priceregulation on goods or public information cam-paigns (42) Further systematic population scansthat associate disease phenotypes with humangenotypes (43 44) are an important tool for de-termining the genetic basis of lifestyle diseasesand therefore in assessing heritable risk andtreatment options Such assessments howeverrun the risk of identifying false-positives andunderestimating the complexity of genetic andepigenetic regulation (45 46) For example it isestimated that 90 of chronic disease risk can-not currently be directly linked to genetic fac-tors but is more likely to be understood in thecontext of human environmental exposures suchas diet and toxicants (47) Thus future preventionand treatment of chronic diseases will combineenhanced genotype-phenotype association scanswith improved monitoring of toxic compoundsin the surrounding environment and in humantissues (47) Such genotype-phenotype associa-tion studies search simultaneously for associationsacross the hundreds of disease phenotypes in-cluded in electronic medical registers (45) This

1245993-2 17 OCTOBER 2014 bull VOL 346 ISSUE 6207 sciencemagorg SCIENCE

log (generation time)

log

(p

op

ula

tio

n s

ize

)

Conservationbiology

Annual organisms

Contemporaryevolution

Phenotype-environmentmismatch

MedicineHuman epithelia

MedicineHumanneurons

MedicineHumanfat cells

MedicineHumans

MedicineHuman

bone marrow

AllViral amp microbial

pathogensmutualists

commensals

Agriculture ampnatural resources

CropsLivestock

Trees

All

Multicellular

pestsweedsinvasive species

Pollinators

Fig 1 The two central paradigms of applied evolution are managing contemporary evolution andphenotype-environment mismatch Managing contemporary evolution is critical for rapidly reproduc-ing organisms with large population sizes such as the methicillin-resistant Staphylococcus aureus(MRSA) pictured top left Altering phenotype-environment mismatch is most relevant for organismswith relatively long generation times and low population sizes such as the large mammals shown lowerright Labels in ovals refer to example organisms viruses or cell types in specified management sectorsldquoAllrdquo indicates relevance to all management sectors (food health and environment) References areprovided in table S1

RESEARCH | REVIEW

expanded approach reduces the rate of false-positives and helps to identify genetic factorsthat contribute to multiple diseases as well asdiseases controlled by multiple genes

Altering genomes for improved foodsecurity and human health

Climate change and environmental degradationcompromise the productivity of agricultural sys-tems that must feed a rapidly growing humanpopulation (48) Genetic modification of cropsthrough enhanced artificial selection methods andperhaps genetic engineering will likely be impor-tant in meeting these challenges Genetically en-gineered (GE) crops were first grown on a largescale in 1996 and during 2013 18 million farmersin 27 countries planted GE crops on ~10 of theworldrsquos cultivated land (175 million hectares) (49)More than 99 of this area was planted withsoybean corn cotton or canola into which geneswere inserted to confer tolerance to herbicidesprotection against insects or both (50) These en-gineered varieties are extreme examples of appar-ently effective genotypic manipulations to reducemismatch to specific environments However so-cietal acceptance is an important factor and GE

crops remain controversial (51 52) They havenot been adopted widely in some regions in-cluding Europe where alternative manipulationsof evolutionary mismatch such as use of non-GElines with some degree of tolerance pesticide ap-plications and integrated pest management serveas alternative genotypic and environmental ma-nipulations (53)An alternative to genetic engineering is en-

hanced artificial selection and hybridization ofsuperior cultivated varieties with molecular ge-netic tools that identify individuals and generegions conveying preferred traits (54) A pri-ority application where genetic engineering hasuntil now been less successful (55) is to improveabiotic tolerance because of more frequentweather extremes under climate change Forexample flood-tolerant rice which is grown bytwo million farmers in Bangladesh and India(49) was developed with marker-assisted breed-ing by using molecular markers of quantita-tive traits to identify targets for hybridizationand selection (56) At the same time candidatedrought-tolerance genes for GE crops have alsorecently been identified in rice as well as corn(57 58) with corn hybrids putatively tolerant

to both drought and herbicidesbrought to market in 2013 (55 59)Regardless whether produced viaartificial selection or genetic engi-neering the potential to improvefood security by reducing mis-matchmay be greatest when tech-nology allows growers to select orcustomize crop varieties for adap-tation in their local agroecosys-tems (60)In contrast to the advances in

agriculture genetic modificationto treat human disease is in a trialphase Gene therapy is under de-velopment mainly for diseaseswith high heritability and simplegenetic control in which replac-ing or complementing parts ofa patientrsquos genome can improvetheir health (61ndash63) Therapies inadvanced trial stages include thetargeting of retinal cells to preventexpression of heritable blindness(64 65) and oral administrationof p53 gene for tumor suppression(66) However even as targetedDNA analysis and whole-genomesequencing of patients becomesincreasingly routine (67) few ef-forts have met the promise oftheir preclinical and clinical trialsto reach final approval phase ofldquopostmarketingrdquo surveillance trials(68 69)

Using environmentalheterogeneity to delaythe evolution of resistance

One of the most costly and wide-spread outcomes of efforts to con-

trol populations is the rapid evolution of resistanceto controlmeasures in insect pests (14) weeds (70)pathogens and cancers (71) For example inten-sive use of the systemic herbicide glyphosate[N-(phosphonomethyl)glycine] by farmers par-ticularly those who grow glyphosate-tolerant GEcrops has selected for resistance in 24 weedspecies in 18 countries since 1996 (72 73) Incontrast strategies that vary selection in spaceor time have delayed the evolution of resistancein some pests (Fig 3) For example scientists andfarmers have proactively developed and imple-mented strategies to slow pest adaptation to GEcrops that produce insecticidal proteins fromBacillus thuringiensis (Bt) (74 75) The primarystrategy employs ldquorefugesrdquo of host plants thatdo not produce Bt toxins to promote survival ofsusceptible pests (74) In principle the rare re-sistant pests that survive on Bt crops are morelikely to mate with the comparatively abundantsusceptible pests from the nearby refuges If re-sistance is inherited as a recessive trait the het-erozygous offspring from such matings will besusceptible and will die on the transgenic plantsThe US Environmental Protection Agency (EPA)and regulatory agencies in many other countries


Genotype manipulation

Phenotype

distribution

Genotype

distribution

Optimum

phenotype

range

A

B C D

Manipulation

of mismatch

Fre

qu

en

cy

Trait value

Mismatch

Environment manipulationDevelopmental manipulation

Fig 2 Phenotype-environment mismatch (A) Mismatch between phenotypes and an environment occurs when apopulations phenotypic trait distribution differs from the optimum greater mismatch increases selection foradaptation but also implies greater costs through reduced survival and reproduction (B) Genotypic manipulationsreduce mismatch by managing existing genetic variation or introducing new genes For example conventionalcorn is damaged by insect pests (left) that are killed by bacterial proteins produced by GE Bt corn (right) Alter-natively evolutionary mismatch can also be managed by (C) developmental manipulations of phenotypes such asvaccination to enhance immunity against pathogens or (D) environmental manipulations such as habitat restora-tion These examples demonstrate methods to reduce mismatch but these same tactics can be reversed to imposegreater mismatch where beneficial to human interests (eg pest eradication)

RESEARCH | REVIEW


Strategy Tactic Food and fiber Health Environment

A Control pests pathogens and invaders by

slowing unwanted evolution

B

Maintain genotypesvulnerable to control

Integrated control ofinvasive species

Stress invaderrsquosweak pointssequentially

Reduceinvader fitness

Target mobile forms to reducedispersal

Alter local conditions or assist migration

Selected hybridized or GE genotypes

Limit competitionprotect in reserves

Favor susceptiblepathogens cell lines

Cycle treatments of pathogens cancers

Multitargetvaccines reducetransmission

Favor survivalof benign strains

Mutate viruseseliminatevectors

Alter lifestyle for health offspring

Recombinant drugs gene therapy

Internalize public costs and benefits

Nontoxic plantings save treatable pests

Rotate cropspesticides

Integratemultiple tactics pyramiding

Mow to selectweeds to shade less

Reducepest fitness

Adopt crops suited to current environment

Wild crop relativesmolecular breeding

Favor efficiency weed suppression

increasing group performance

Protect desirable populations by

reducing phenotype environment mismatch

reducing adversary fitness

Protect somesusceptible forms

Switch treatments to slow adaptation

Apply stressorstogether

Favor benigngenotypes

Transgenicmutation

Modify environment or move

Modify genotypes

Select emergent group traits

Spatialvariationin selection

Temporal variationin selection

Diversifiedselection

Trait-basedselection

Add mutationalload

Reduce selection

Improve fit toenvironment

Group selectioncooperation

Space

Mix

Time

Now Later

hybrid

Fig 3 Two management intervention categories of applied evolutionarybiology (A) Controlling adversaries and (B) Protecting valued populationsTogether they are enabled by four strategies (headings) A core set of eightevolutionary principles guides the execution of these strategies and underliestactics (left columns) used tomeetmanagement objectives in the food and fiberproduction health and environmental sectors (right columns) Colored squares

show different treatments curves show frequency distributions of phenotypesdouble helices are genomes green arrows show change through space or timegreen wedges show point interventions using selection or genetic engineeringSemicolons separate multiple management examples Hypothetical applica-tions are given in two cases that lack empirical examples Expanded treatmentsfor each cell and references are provided in table S2

RESEARCH | REVIEW

have mandated refuges since Bt crops werefirst commercialized (76 77) Retrospective anal-ysis after more than a decade of monitoringindicates that refuges do indeed delay resistanceparticularly when resistance is a recessive trait(77 78)The success of refuge tactics in agriculture is

now drawing attention in other managementsectors including fisheries where refuges mayimpede costly life-history evolution and body-sizeevolution resulting from harvest selection (79)Likewise in cancer management portions of tu-mors with low vascularization and consequentlylow delivery of chemotoxins may serve as refugesthat sustain chemosensitive tumor genotypes(80 81) and slow the evolution of resistance tochemotherapy inmetastatic cancer (82 83) Suchresistance accounts for a large proportion ofcurrent treatment failures (84) Compared withtypical failures when oncologists try to eradicatea patientrsquos cancer with high drug doses lowerdoses could be more successful if they favor sur-vival of chemosensitive cell lines that can out-compete chemoresistant lines (85) Increasinglysophisticated models of tumor evolution mayeventually support implementation of such non-eradication therapies (86)Whereas refuges delay resistance by swamping

resistant lineages with susceptible lineages an-other strategy attempts to curb resistance throughselection that combines multiple modes of ac-tion (also known as ldquostackingrdquo or ldquopyramidingrdquo)In many human diseasesmdashincluding HIV tuber-culosis malaria and cancermdashresistance frequent-ly evolves under selection from individual drugs(87) Combination therapies are based on theevolutionary principle that if genes conferringresistance to each selection pressure are rareand inherited independently individuals withall of the genes required for full resistance willbe rare or even absent in target populations(4 14 88 89) For example resistance evolvedrapidly to potent antiretroviral drugs admin-istered singly in patients with HIV but com-binations of three such drugs have providedlong-term efficacy and have become the stan-dard of care (90 91) The potential tradeoffs as-sociated with combining two or more drugs orpesticides to delay resistance include short-termincreases in costs (92) and negative side effects(93) as well as the concern that such combi-nations will also ultimately favor the evolutionof multiple resistance (87 94 95) For exampleincorporating two or more toxins together in GEvarieties slows resistance evolution (96 97) butthis advantage may diminish when less-resistantsingle-toxin varieties are planted in the samearea as multitoxin varieties and provide steppingstones for multiple-resistance evolution (98)Combined selection pressures are most likelyto be durable when implemented as a facet ofmore broadly integrated systems such as inte-grated pest management (IPM) IPM combinesselection pressures from a diverse suite of tacticsfor pest suppression including various forms ofbiological control and optimized spatiotemporalcropping schemes (99) By increasing treatment

durability combinatorial strategies are amongthe most important instruments for the controlof highly adaptable pests pathogens and can-cers (Fig 3)

Choosing population sourcesto anticipate climate change

Although some strategies of applied evolution-ary biology are established or rapidly increasingother rarely used strategies are of interest be-cause of their underexplored potential to replaceor complement longstanding management prac-tices These include using nonlocal seeding sourcesfor replanting in environmental restoration andforestry as well as the exploitation of groupselection-based designs in crop and livestockbreedingThe mismatch of valued plants to new climates

is an overarching challenge in forestry agri-culture and conservation biology A widespreaddebate concerns whether to use local versus ex-ternal sources of genetic material for replantingto best anticipate climate change in forestry ag-riculture wildlife and environmental restorationThe massive scale of many replanting effortsmdash400000 ha of production forest is planted eachyear in Canada alone (100)mdashplus the long in-tervals between plantings for many perennialspecies and restoration projects means thatthese choices may have broad economic andecological consequences Traditionally residentstocks have been favored to capture locallyvaluable adaptations In forestry this approachis exemplified by established bioclimatic ldquoseed-transfer zonesrdquo that guide seed sourcing forplanting of some of the worldrsquos largest pro-duction systems (101 102) Evidence from wild-plant restoration programs indicates howeverthat local sources are not always best particu-larly in altered environments (103ndash108) This mayarise when nearby sources share some of thevulnerabilities responsible for the declines ofthe original populations (102) In these situa-tions climate mismatches may be better relievedby translocating genotypes that are preadaptedto expected conditions (109 110) for examplemore tolerant to heat drought or pest stresses(111) When single sources do not show the rangeof adaptations required at a given site reintro-duction may be improved with propagules pooledfrom a diversity of sources to increase overallgenetic variation and thus the odds that someindividuals will be suited for changing condi-tions (103 104 112) A recent meta-analysis inrestoration ecology underscores shortcomingsof the ldquolocal-is-bestrdquo dictum (108) and compa-rable analyses of sourcing successes and failuresin forestry and perennial agriculture are neededto find ways to sustain productivity under cli-mate change

Exploiting group versus individualperformance in crops and livestock

In most agriculture and aquaculture produc-tivity is measured at the level of groups (eg fieldor herd) rather than in individual performanceMore attention to traits that improve group per-

formance may thus offer a broader suite of tacticsto increase production while demanding fewerresources including pesticides to meet basichuman needs (113) (Fig 3) In the majority ofnatural systems group selection is consideredweak relative to selection among individuals(114) Consequently past natural selection in theancestors of domesticated species may have fa-vored traits that promote individual perform-ance but are costly to group productivity Oneimportant consequence may be greater currentopportunities for artificial selection of individ-ual traits that improve group performance whileavoiding inadvertent evolution of ldquouncoopera-tiverdquo individuals (8) such as those with com-petitive root structures in dryland field crops(115) Artificial selection for group yield in maizehas produced lines with reduced male functionand that bear more-vertical leaves which re-duce the shading of neighbors Both of thesetraits decrease individual plant performancewhile enhancing group productivity (116 117)but in the absence of strategic breeding to favorthese changes directly they have evolved onlyslowly requiring 60 years to appear as unplannedresponses to selection on group yield alone (118)Weiner and colleagues (119) have proposed aproactive design for wheat production that se-lects for traits that increase collective shadingof weeds within specific planting configurationsin order to increase overall crop yield while re-ducing herbicide use Similar group-based per-spectives apply in animal husbandry where traitslike reduced aggressiveness favor group produc-tivity under domestication butmight have beenselected against in the wild (120) By combiningagronomy and environmental physiology withevolutionary modeling group-based agriculturalsystemsmay offer new andmore sustainable pathsto meet global production goals

Addressing evolution acrossmanagement sectors

One of the most significant outcomes of the scaleof human activity is that evolutionary concernsin one management sector often spill over intoor depend on others (Fig 4) These connectionsresult from novel biotic interactions because ofnatural intentional or inadvertent transport oforganisms and their genes by trade infrastruc-ture and waste streams (121 122) Further coor-dination of prevention control and monitoringwill be required to address growing interdepen-dencies among management sectors Increasedexchange of emerging pathogens between healthagricultural and natural systems is a key casein point (123ndash126) For example although do-mestic pigs are the principal reservoir of ldquoswineinfluenzardquo (H1N1) they simultaneously host otherinfluenza strains including those associated withhuman hosts and domestic and migratory avianhosts (127) The intensive communal raising ofpigs and poultry for food therefore encouragesvirus strains to exchange genes and adapt tomore host species (128) One overarching concernis that pigs hosting highly pathogenic wild avianstrains (H5N1) could contribute to selection for


RESEARCH | REVIEW

the direct mammal-to-mammal transmissionthat underlies human epidemics The conse-quences of such evolution (129) are foreshad-owed by the recent global outbreaks of H5N1in 2004 and H1N1 in 2009 (130) These eventsunderscore the need for initiatives in preventionand control that cross traditional disciplinaryboundaries including coordinated surveillanceof viral evolution and the monitoring of patho-gen reservoir species across the food health andenvironment spectrum (125 131)The unresolved problem of rapidly evolving

antimicrobial resistance is another pressing ex-ample of interdependence among managementsectors particularly between systems managedfor food production and human health Annualestimated costs of combatting multidrug-resistantmicrobes in the United States alone total $35

billion (132 133) and the failure to produce newantimicrobials as quickly as their predecessorslose efficacy (134 135) places a premium on stew-ardship of the few drugs that remain broadlyeffective (136 137) Although overprescribing ofantibiotics for human treatment is a very realconcern the major use of antimicrobial drugsin many parts of the world is to promote thehealth and growth of livestock (138 139) Thisuse selects for antimicrobial-resistant microbesthat may infect humans (Fig 4) (139 140) For ex-ample antibiotic-treated animals that are raisedas food for people are now implicated in the ori-gins of the most extensively resistant Escherichiacoli encountered in human sepsis (141) Partic-ularly worrisome is that once free in the envi-ronment resistance genes do not dissipate withdistance like many abiotic environmental pollu-

tants Resistance genes can replicate and thusthey can transfer horizontally among bacterialtaxa travel intact over great distances via hostsand rise to new abundances in the presence ofantimicrobials with similar modes of action Aspools of resistance genes become more preva-lent and disseminated through human activitiesthey are likely to become increasingly importantin new regions and management sectors (142)Because coupled evolutionary dynamics operateover such large spatial scales and multiple man-agement sectors their management requirespolitical coordination as exemplified by the Trans-atlantic Taskforce on Antimicrobial Resistance(143) Regulatory bodies have also taken the firststeps to restrict use of some antibiotics to singlemanagement sectors (144 145) Broader andmorerigorous implementation of such restrictions willbe needed to sustain the most critical public be-nefits of our modern antibiotic era

Next stepsApplied evolutionary biologyin international policy

Applied evolutionary biology addresses both therapidly evolving and the mismatched biologicalsystems that underlie many global challenges(146) Meeting international objectives for sus-tainable development [Millennium DevelopmentGoals and the anticipated Sustainable Develop-ment Goals (147)] and biodiversity conserva-tion [the Convention for Biological Diversityrsquos2020 ldquoAichirdquo Biodiversity Targets (148)] will re-quire much greater integration of evolutionaryprinciples into policy than has been widely ac-knowledged The potential policy contributionsof cases reviewed here are summarized in Box 1For example we must implement resistance-management strategies for pesticides and anti-biotics to meet newly proposed Sustainable De-velopment Goals for human health food andwater security (147) Likewise choices of adapt-able source populations will improve the resil-ience of restored habitats (Aichi Target 15 ldquorestore15 percent of degraded habitats before 2020rdquo)and increase the reliability of crop supplies Fur-ther sustainable harvest strategies (149 150)and early warning signs of unsustainable har-vest (151) will help to achieve lasting stocks offish and aquatic invertebrates (Aichi Target 6all stocks should be harvested sustainably) Theidentification and protection of diverse geno-types is also critical to the future of crop im-provement and for the discovery of chemicalcompounds such as new therapeutics In thisrealm the international Nagoya Protocol onAccess and Benefit-Sharing of genetic resources(152) may assist in securing public access toresources for adaptation to local conditions whilecoordinating with global research and develop-ment efforts (153ndash155)The extensive and targeted genetic manip-

ulations permitted through recent advances inbiotechnology are setting the stage for novelbiological functions for which we either lack anunderstanding of potential risks or knowledgeof how best to assess them (156) There is a need


Environment

Health

Food

ZoonosesAntimicrobial

resistance

Fig 4 Emerging pathogens such as zoonoses (black arrows) and resistant bacteria (orangearrows) illustrate interdependencies generated by gene flow among the economic sectors offood health and the environment In zoonoses vertebrates such as birds act as reservoirs forpathogens that can infect humans Through direct transmission or via domesticated animals zoonosesare passed to humans and cause regular local and rare global epidemics (such as the flu outbreaks ofH5N1-2004 and H1N1-2009) ldquoReverse zoonosesrdquo are transmitted from infected humans to wildlife (177)Antimicrobial resistance in bacterial stains associated with livestock evolves in response to widespreaduse of antibiotics in agriculture and to a lesser degree because of treatment in humans Via food itemsindustry workers and waste disposal resistant strains enter other human contexts In a public healthcontext resistant strains constitute a growing extra risk during treatment of illnesses for example inhospitals Antibiotics in human effluent cause widespread resistance selection in natural and seminaturalenvironments which together with resistance reservoirs in natural environments further increase therisks of resistant pathogens in humans In the figure the dashed line indicates a variety of poorly knowninteractions among wild species

RESEARCH | REVIEW

for an overarching international framework toregulate synthetic (156 157) as well as conven-tional and advanced GM organisms (158)ndashaframework that also would reduce conflict be-tween existing frameworks (159) Perhaps the

area of applied evolutionary biology where de-velopment of international policy is most urgentis the area of synthetic biology Synthesizingwholly or partially novel organisms offers tremen-dous opportunities inmany areas such as biofuels

medicine environmental restoration and conser-vation (160ndash162) but national and internationalguidelines are needed to avert potentially harmfuloutcomes (156 163) Segments of medicine andagriculture include social scientists and econo-mists in systematic risk assessment (76 164)Similar practices would benefit conservation bi-ology and natural resource management as in-creasingly proactive and intensive manipulationsappear on the horizon These prospects includeresurrected species and wild populations genet-ically engineered for resistance to lethal diseasessuch as chytrid fungus in frogs and white-nosesyndrome in bats (161 162)

Implementing applied evolutionarybiology locally and globally

Reconciliation of individual and group stake-holder interests plays a central role in the effortto achieve sustainability through applied evolu-tionary biology (165ndash168) Anthropogenic evolu-tionary change often has consequences that extendbeyond the immediate vicinity of the causal agentsand pose dilemmas in achieving cooperation fromlocal to global scales (169) Thus in some appliedevolutionary strategies individuals must exchangetheir private short-term gains for the long-termpublic good In managing pest resistance to trans-genic Bt crops farmers who plant refuges of con-ventional crops contribute to the long-term publicgood of sustained pest susceptibility to Bt toxinbut may incur the short-term private cost of pestdamage to their refuges However farmers in fivemidwestern states of the United States accruednearly two-thirds of the estimated $68 billion inBt corn benefits between 1996 and 2009 fromland planted with non-Bt corn refuges (170) Thisbenefit arose because widespread adoption ofBt corn caused regional suppression of the majortarget pest and non-Bt corn seed was less ex-pensive than Bt corn (170) Despite this benefitfarmer compliance with the refuge strategy forBt corn in the United States has steadily declinedand threatens the sustainability of resistance man-agement (171) Farmers are increasingly plantingBt seeds alone which may reflect their efforts toreduce the perceived risk of short-term lossesfrom pest damage to refuges Such conflicts be-tween individual and public good may be the rulerather than the exception in the implementationof applied evolutionary biologyThe economic theories of public choice pro-

vide tools for reconciling individual and groupconflicts (169) (Box 1) Governments can tax un-desirable actions subsidize desirable ones reg-ulate activities (144 145) and create tradableproperty rights For example subsidies and reg-ulated access to public schools can increase par-ticipation in vaccination programs that benefitpublic health but may increase risks to unvac-cinated individuals (170) Theoretical modelingsuggests that an unregulated vaccinationmarketwill yield too little advance vaccination and toomuch vaccination at the time of infection whichcould select for increased virulence (164) Withpathogen resistance both the relative fitness ofresistant genotypes in untreated environments


Box 1 Recommended contributions of applied evolutionary biology to proposed themesof new international sustainable development goals (147) based on examples presentedin this review For the currently negotiated draft of the sustainable development goals goto httpsustainabledevelopmentunorgfocussdgshtml

Goal 1 Thriving lives and livelihoods

- Reduce chronic lifestyle disease through environmental alignment of humanlifestyle

- Reduce environmental levels of human toxicants through application of reducedselection response techniques to biocides

- Apply reduced selection response techniques to maintain long-term efficacyof antimicrobials and to avert the antibiotics crisis

- Reconcile individual and group incentives in health systems to reduce virulenceand resistance of emerging and reemerging pathogens

Goal 2 Sustainable food security

- Increase crop yield through continued selection of varieties and improvedaccess to these

- Prolong efficacy of pesticides and artificially selected or GE crops throughreduced selectionndashresponse techniques

- Improve yields through integration of group selection in production of novelcrop varieties

- Reduce climate change impact by choosing crop varieties resilient todrought flooding and other extremes

Goal 3 Secure sustainable water

- Increase water security through use of reduced selectionndashresponsetechniques to water-polluting pesticides andor biocides

- Use genetic manipulation to produce crop varieties with improvedwater economy

Goal 4 Universal clean energy

- Improve biofuels through genetic manipulation with the aim to reduceCO2 emissions and land area for energy production

- Assess risks and benefits of synthetic organisms for biofuel productionwhile taking gene flow land use and property rights issues into account

Goal 5 Healthy and productive ecosystems

- Reduce biodiversity extinction rates through environmental alignmentand genetic manipulation of fitness

- Retain naturalness of captive biodiversity through environmental alignment- Choose preadapted or high-diversity sources for increased habitat restoration

success- Avoid collapse and protect genetic diversity of aquatic resources through

nonselective harvesting strategies informed by early warning signals

Goal 6 Governance for sustainable societies

- Incorporate externalities from rapid evolution as well as the loss of evolutionaryhistory and evolutionary potential into green accounting for sustainablegovernance of the Earth system

- Coordinate strategies of sustainable development goals in a coupled-systemsframework to reduce conflicts from inadvertent contemporary evolutionand phenotype-environment mismatch

ldquoReduced selectionndashresponse techniquesrdquo refer to the four tactics in Fig 3 thatslow evolution by varying selection in space and time diversifying selection and tar-geting of specific traits as well as adoption of alternatives to strong selection agentssuch as toxins

RESEARCH | REVIEW

(174 175) and the prevalence of resistance in nat-ural environments (176) may increase the cost oflost susceptibility to a drug Improved policiesthat reduce public costs may emerge from betteraccounting of the causes and consequences ofsuch evolutionary externalities (154 177)

Toward a unified discipline

As demonstrated by many of the examplesabove applied evolutionary biology uses princi-ples common to all areas of biology and be-cause of this progress in one area may oftenenable solutions in others New approaches inthis developing field may best be generatedand assessed through collaborations that spandisciplinary boundaries (178) (Fig 3) Promot-ing greater adoption and consistency in the useof evolutionary terminology which is currentlyinconsistent across disciplines (179) will there-fore be an important first step toward a moreunified field of applied evolutionary biologyThe global scale of human impacts is now

more widely appreciated than ever before Suc-cessful governance of living systems requiresunderstanding evolutionary history as well ascontemporary and future evolutionary dynam-ics Our current scientific capacity for evolution-arily informed management does not matchthe need but it can be increased through newand more widespread training and collabora-tion monitored experimentation and context-sensitive implementation Like engineering whichis a multifaceted applied science with commoncore principles shared vocabulary and coordi-nated methods applied evolutionary biology hasthe potential to serve society as a predictive andintegrative framework for addressing practicalconcerns in applied biology that share at theircore the basic evolutionary principles govern-ing life

REFERENCES AND NOTES

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2 E C Ellis et al Used planet A global history Proc NatlAcad Sci USA 110 7978ndash7985 (2013) doi 101073pnas1217241110 pmid 23630271

3 R G Latta Conservation genetics as applied evolutionFrom genetic pattern to evolutionary process Evol Appl 184ndash94 (2008) doi 101111j1752-4571200700008x

4 S R Palumbi Humans as the worldrsquos greatest evolutionaryforce Science 293 1786ndash1790 (2001) doi 101126science29355361786 pmid 11546863

5 P D Gluckman C T Bergstrom Evolutionary biologywithin medicine A perspective of growing value BMJ343 (dec19 suppl1) d7671 (2011) doi 101136bmjd7671pmid 22184558

6 F Gould Broadening the application of evolutionarilybased genetic pest management Evolution 62 500ndash510 (2008)doi 101111j1558-5646200700298x pmid 17999722

7 P H Thrall et al Evolution in agriculture The applicationof evolutionary approaches to the management of bioticinteractions in agro-ecosystems Evol Appl 4 200ndash215(2011) doi 101111j1752-4571201000179x

8 R F Denison Darwinian Agriculture How UnderstandingEvolution Can Improve Agriculture (Princeton Univ PressPrinceton NJ 2012)

9 D W Hollomon Do we have the tools to manage resistancein the future Pest Manag Sci 68 149ndash154 (2012)doi 101002ps2291 pmid 22223198

10 C A Stockwell A P Hendry M K Kinnison Contemporaryevolution meets conservation biology Trends Ecol Evol 1894ndash101 (2003) doi 101016S0169-5347(02)00044-7

11 A P Hendry et al Evolutionary biology in biodiversityscience conservation and policy A call to action Evolution64 1517ndash1528 (2010) pmid 20067518

12 A P Hendry et al Evolutionary principles and theirpractical application Evol Appl 4 159ndash183 (2011)doi 101111j1752-4571201000165x

13 WHO Antimicrobial resistance Global report on surveillance(2014) wwwwhointdrugresistancedocumentssurveillancereporten

14 B E Tabashnik D Mota-Sanchez M E WhalonR M Hollingworth Y Carriegravere Defining terms forproactive management of resistance to Bt crops andpesticides J Econ Entomol 107 496ndash507 (2014)doi 101603EC13458 pmid 24772527

15 P D Gluckman M A Hanson Mismatch Why Our World NoLonger Fits Our Bodies (Oxford Univ Press Oxford 2006)

16 A D Barnosky et al Has the Earthrsquos sixth mass extinctionalready arrived Nature 471 51ndash57 (2011) doi 101038nature09678 pmid 21368823

17 J J Bull H A Wichman Applied evolution Annu RevEcol Syst 32 183ndash217 (2001) doi 101146annurevecolsys32081501114020

18 S P Carroll C W Fox Conservation Biology Evolution inAction (Oxford Univ Press Oxford 2008)

19 P D Gluckman M A Hanson T Buklijas F M LowA S Beedle Epigenetic mechanisms that underpinmetabolic and cardiovascular diseases Nat Rev Endocrinol 5401ndash408 (2009) doi 101038nrendo2009102pmid 19488075

20 D Hartl A Primer of Population Genetics (Sinauer AssociatesInc Sunderland MA 1988)

21 P A Abrams Modelling the adaptive dynamics of traitsinvolved in inter- and intraspecific interactions Anassessment of three methods Ecol Lett 4 166ndash175 (2001)doi 101046j1461-0248200100199x

22 C K Ghalambor J K McKay S P Carroll D N ReznickAdaptive versus non-adaptive phenotypic plasticity and thepotential for contemporary adaptation in new environmentsFunct Ecol 21 394ndash407 (2007) doi 101111j1365-2435200701283x

23 M T Kinnison N G Hairston Eco-evolutionary conservationbiology Contemporary evolution and the dynamics ofpersistence Funct Ecol 21 444ndash454 (2007) doi 101111j1365-2435200701278x

24 C A Aktipis V S Kwan K A Johnson S L NeubergC C Maley Overlooking evolution A systematic analysis ofcancer relapse and therapeutic resistance research PLoSONE 6 e26100 (2011) doi 101371journalpone0026100pmid 22125594

25 N Mouquet et al Ecophylogenetics Advances andperspectives Biol Rev Camb Philos Soc 87 769ndash785(2012) doi 101111j1469-185X201200224xpmid 22432924

26 G M Mace A Purvis Evolutionary biology and practicalconservation Bridging a widening gap Mol Ecol 179ndash19 (2008) doi 101111j1365-294X200703455xpmid 17696991

27 L-M Chevin R Gallet R Gomulkiewicz R D Holt S FellousPhenotypic plasticity in evolutionary rescue experimentsPhilos Trans R Soc Lond B Biol Sci 368 20120089(2013) doi 101098rstb20120089 pmid 23209170

28 A F Read S Huijben Evolutionary biology and the avoidanceof antimicrobial resistance Evol Appl 2 40ndash51 (2009)doi 101111j1752-4571200800066x

29 A F Read T Day S Huijben The evolution of drugresistance and the curious orthodoxy of aggressivechemotherapy Proc Natl Acad Sci USA 108 (suppl 2)10871ndash10877 (2011) doi 101073pnas1100299108pmid 21690376

30 M V Ashley et al Evolutionarily enlightened managementBiol Conserv 111 115ndash123 (2003) doi 101016S0006-3207(02)00279-3

31 S E Williams E A Hoffman Minimizing genetic adaptationin captive breeding programs A review Biol Conserv 1422388ndash2400 (2009) doi 101016jbiocon200905034

32 K Leus K Traylor-Holzer R C Lacy Genetic and demographicpopulation management in zoos and aquariums Recentdevelopments future challenges and opportunities forscientific research Int Zoo Yearb 45 213ndash225 (2011)doi 101111j1748-1090201100138x

33 P D Gluckman F M Low T Buklijas M HansonA S Beedle How evolutionary principles improve theunderstanding of human health and disease Evol Appl 4249ndash263 (2011) doi 101111j1752-4571201000164x

34 L Cordain et al Origins and evolution of the Western dietHealth implications for the 21st century Am J Clin Nutr 81341ndash354 (2005) pmid 15699220

35 R C Brownson D Haire-Joshu D A Luke Shaping thecontext of health A review of environmental and policyapproaches in the prevention of chronic diseases Annu RevPublic Health 27 341ndash370 (2006) doi 101146annurevpublhealth27021405102137 pmid 16533121

36 T A Gaziano N Pagidipati Scaling up chronic diseaseprevention interventions in lower- and middle-income countriesAnnu Rev Public Health 34 317ndash335 (2013) doi 101146annurev-publhealth-031912-114402 pmid 23297660

37 C D Mathers D Loncar Projections of global mortality andburden of disease from 2002 to 2030 PLoS Med 3 e442(2006) doi 101371journalpmed0030442 pmid 17132052

38 D E Bloom et al ldquoThe global economic burden ofnoncommunicable diseasesrdquo (Working paper no 87Program on the Global Demography of Aging Harvard Schoolof Public Health World Economic Forum Geneva 2012)

39 J Woodcock O H Franco N Orsini I Roberts Non-vigorousphysical activity and all-cause mortality Systematic reviewand meta-analysis of cohort studies Int J Epidemiol 40121ndash138 (2011) doi 101093ijedyq104 pmid 20630992

40 WHO Environmental and occupational cancers wwwwhointmediacentrefactsheetsfs350en

41 J Lynch G D Smith A life course approach to chronicdisease epidemiology Annu Rev Public Health 26 1ndash35(2005) doi 101146annurevpublhealth26021304144505pmid 15760279

42 D A Chokshi T A Farley The cost-effectiveness ofenvironmental approaches to disease prevention N EnglJ Med 367 295ndash297 (2012) doi 101056NEJMp1206268pmid 22830461

43 J Flannick et al Go-T2D ConsortiumT2D-GENESConsortium Loss-of-function mutations in SLC30A8 protectagainst type 2 diabetes Nat Genet 46 357ndash363 (2014) doi101038ng2915 pmid 24584071

44 G S Omenn Evolution in health and medicine Sacklercolloquium Evolution and public health Proc Natl AcadSci USA 107 (suppl 1) 1702ndash1709 (2010) doi 101073pnas0906198106 pmid 19966311

45 J C Denny et al Systematic comparison of phenome-wideassociation study of electronic medical record data andgenome-wide association study data Nat Biotechnol 311102ndash1111 (2013) doi 101038nbt2749 pmid 24270849

46 M Travisano R G Shaw Lost in the map Evolution 67305ndash314 (2013) doi 101111j1558-5646201201802xpmid 23356605

47 S M Rappaport Implications of the exposome for exposurescience J Expo Sci Environ Epidemiol 21 5ndash9 (2011)doi 101038jes201050 pmid 21081972

48 H C J Godfray et al Food security The challenge offeeding 9 billion people Science 327 812ndash818 (2010)doi 101126science1185383 pmid 20110467

49 C James ldquoExecutive summary Global status ofcommercialized biotechGM cropsrdquo (ISAAA Brief 46International Service for the Acquisitions of Agri-BiotechApplications New York 2013)

50 M Ashraf Inducing drought tolerance in plants Recentadvances Biotechnol Adv 28 169ndash183 (2010) doi 101016jbiotechadv200911005 pmid 19914371

51 E Pauwels Public understanding of synthetic biologyBioscience 63 79ndash89 (2013) doi 101525bio20136324

52 P Aerni Resistance to agricultural biotechnology Theimportance of distinguishing between weak and strong publicattitudes Biotechnol J 8 1129ndash1132 (2013) pmid 23857924

53 S-E Jacobsen M Soslashrensen S M Pedersen J WeinerFeeding the world Genetically modified crops versusagricultural biodiversity Agron Sustain Dev 33 651ndash662(2013) doi 101007s13593-013-0138-9

54 R K Varshney K C Bansal P K Aggarwal S K DattaP Q Craufurd Agricultural biotechnology for cropimprovement in a variable climate Hope or hype TrendsPlant Sci 16 363ndash371 (2011) doi 101016jtplants201103004 pmid 21497543

55 A Marshall Drought-tolerant varieties begin global marchNat Biotechnol 32 308ndash308 (2014) doi 101038nbt2875

56 R K Varshney et al Can genomics boost productivity oforphan crops Nat Biotechnol 30 1172ndash1176 (2012)doi 101038nbt2440 pmid 23222781

57 S Yang B Vanderbeld J Wan Y Huang Narrowing downthe targets Towards successful genetic engineering ofdrought-tolerant crops Mol Plant 3 469ndash490 (2010)doi 101093mpssq016 pmid 20507936


RESEARCH | REVIEW

58 A C M Gaudin A Henry A H Sparks I H Slamet-LoedinTaking transgenic rice drought screening to the field J ExpBot 64 109ndash117 (2013) doi 101093jxbers313pmid 23202133

59 International Service for the Acquisition of Agri-BiotechApplications Approval database 2013 httpwwwisaaaorggmapprovaldatabasedefaultasp (2013)

60 K L Mercer H R Perales J D Wainwright Climate changeand the transgenic adaptation strategy Smallholderlivelihoods climate justice and maize landraces in MexicoGlob Environ Change 22 495ndash504 (2012) doi 101016jgloenvcha201201003

61 M Tachibana et al Towards germline gene therapy ofinherited mitochondrial diseases Nature 493 627ndash631(2013) doi 101038nature11647 pmid 23103867

62 J H Kordower D Kirik Introduction Neurobiol Dis 48151ndash152 (2012) doi 101016jnbd201207014 pmid 22841531

63 I-K Choi C-O Yun Recent developments in oncolyticadenovirus-based immunotherapeutic agents for use againstmetastatic cancers Cancer Gene Ther 20 70ndash76 (2013)doi 101038cgt201295 pmid 23306610

64 D M Lipinski M Thake R E MacLaren Clinical applicationsof retinal gene therapy Prog Retin Eye Res 32 22ndash47 (2013)doi 101016jpreteyeres201209001 pmid 22995954

65 K J Wert R J Davis J Sancho-Pelluz P M NishinaS H Tsang Gene therapy provides long-term visual functionin a pre-clinical model of retinitis pigmentosa Hum MolGenet 22 558ndash567 (2013) doi 101093hmgdds466pmid 23108158

66 K Suzuki H Matsubara Recent advances in p53 researchand cancer treatment J Biomed Biotechnol 2011 978312(2011) doi 1011552011978312 pmid 21765642

67 O Kilpivaara L A Aaltonen Diagnostic cancer genomesequencing and the contribution of germline variants Science339 1559ndash1562 (2013) doi 101126science1233899pmid 23539595

68 P R Lowenstein M G Castro Uncertainty in the translationof preclinical experiments to clinical trials Why do mostphase III clinical trials fail Curr Gene Ther 9 368ndash374(2009) doi 102174156652309789753392 pmid 19860651

69 M Edelstein Gene therapy clinical trials worldwide J GeneMedicine database (2014) httpwwwabediacomwileyindexhtml

70 C C Vigueira K M Olsen A L Caicedo The red queen inthe corn Agricultural weeds as models of rapid adaptiveevolution Heredity 110 303ndash311 (2013) doi 101038hdy2012104 pmid 23188175

71 S E Greene A Reid Moving Targets Fighting theEvolution of Resistance in Infections Pests and Cancer(American Society of Microbiology Washington DC 2013)httpbitlyYeNhoS

72 S B Powles Q Yu Evolution in action Plants resistantto herbicides Annu Rev Plant Biol 61 317ndash347 (2010)doi 101146annurev-arplant-042809-112119 pmid 20192743

73 I HeapThe International Survey of Herbicide Resistant Weeds(2013) wwwweedsciencecomsummaryhomeaspx

74 B E Tabashnik Evolution of resistance to Bacillusthuringiensis Annu Rev Entomol 39 47ndash79 (1994)doi 101146annureven39010194000403

75 F Gould Sustainability of transgenic insecticidal cultivarsIntegrating pest genetics and ecology Annu Rev Entomol43 701ndash726 (1998) doi 101146annurevento431701pmid 15012402

76 EPA ldquoThe Environmental Protection Agencyrsquos White Paper onBacillus thuringiensis plant-pesticide resistance managementrdquo(EPA Washington DC 1998)

77 B E Tabashnik T Breacutevault Y Carriegravere Insect resistance toBt crops Lessons from the first billion acres Nat Biotechnol31 510ndash521 (2013) doi 101038nbt2597 pmid 23752438

78 B E Tabashnik A J Gassmann D W Crowder Y CarrieacutereInsect resistance to Bt crops Evidence versus theoryNat Biotechnol 26 199ndash202 (2008) doi 101038nbt1382pmid 18259177

79 E S Dunlop M L Baskett M Heino U Dieckmann Thepropensity of marine reserves to reduce the evolutionaryeffects of fishing in a migratory species Evol Appl 2371ndash393 (2009) doi 101111j1752-4571200900089x

80 R A Gatenby J Brown T Vincent Lessons from appliedecology Cancer control using an evolutionary double bindCancer Res 69 7499ndash7502 (2009) doi 1011580008-5472CAN-09-1354 pmid 19752088

81 A S Silva R A Gatenby A theoretical quantitative model forevolution of cancer chemotherapy resistance Biol Direct 525 (2010) doi 1011861745-6150-5-25 pmid 20406443

82 R J Gillies D Verduzco R A Gatenby Evolutionarydynamics of carcinogenesis and why targeted therapy doesnot work Nat Rev Cancer 12 487ndash493 (2012) doi 101038nrc3298 pmid 22695393

83 M Greaves C C Maley Clonal evolution in cancerNature 481 306ndash313 (2012) doi 101038nature10762pmid 22258609

84 D B Longley P G Johnston Molecular mechanisms of drugresistance J Pathol 205 275ndash292 (2005) doi 101002path1706 pmid 15641020

85 R A Gatenby A change of strategy in the war on cancer Nature459 508ndash509 (2009) doi 101038459508a pmid 19478766

86 V Almendro et al Inference of tumor evolution duringchemotherapy by computational modeling and in situanalysis of genetic and phenotypic cellular diversityCell Rep 6 514ndash527 (2014) doi 101016jcelrep201312041 pmid 24462293

87 J-B Michel P J Yeh R Chait R C Moellering JrR Kishony Drug interactions modulate the potential forevolution of resistance Proc Natl Acad Sci USA 10514918ndash14923 (2008) doi 101073pnas0800944105pmid 18815368

88 REX Consortium Heterogeneity of selection and theevolution of resistance Trends Ecol Evol 28 110ndash118(2013) doi 101016jtree201209001 pmid 23040463

89 J J Cunningham R A Gatenby J S Brown Evolutionarydynamics in cancer therapy Mol Pharm 8 2094ndash2100(2011) doi 101021mp2002279 pmid 21815657

90 R M Gulick Antiretroviral treatment 2010 Progress andcontroversies J Acquir Immune Defic Syndr 55 (suppl 1)S43ndashS48 (2010) doi 101097QAI0b013e3181f9c09epmid 21045599

91 R K Gupta D A Van de Vijver S Manicklal M A WainbergEvolving uses of oral reverse transcriptase inhibitors inthe HIV-1 epidemic From treatment to preventionRetrovirology 10 82 (2013) doi 1011861742-4690-10-82pmid 23902855

92 H Brun et al Quantitative resistance increases the durabilityof qualitative resistance to Leptosphaeria maculans inBrassica napus New Phytol 185 285ndash299 (2010)doi 101111j1469-8137200903049x pmid 19814776

93 B E Tabashnik Managing resistance with multiplepesticide tactics theory evidence and recommendationsJ Econ Entomol 82 1263ndash1269 (1989) pmid 2689487

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95 J P Torella R Chait R Kishony Optimal drug synergy inantimicrobial treatments PLOS Comput Biol 6 e1000796(2010) doi 101371journalpcbi1000796 pmid 20532210

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99 A M Shelton et al in Field Manual of Techniques in InvertebratePathology (Springer Amsterdam 2007) pp 793ndash811

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106 M Byrne L Stone M A Millar Assessing genetic riskin revegetation J Appl Ecol 48 1365ndash1373 (2011)doi 101111j1365-2664201102045x

107 K Vander Mijnsbrugge A Bischoff B Smith A questionof origin Where and how to collect seed for ecologicalrestoration Basic Appl Ecol 11 300ndash311 (2010)doi 101016jbaae200909002

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109 D J Merritt K W Dixon Conservation Restoration seedbanksmdasha matter of scale Science 332 424ndash425 (2011)doi 101126science1203083 pmid 21512021

110 AdapTRee website httpadaptreesitesoltubcca111 J A Hicke J C Jenkins Mapping lodgepole pine stand

structure susceptibility to mountain pine beetle attackacross the western United States For Ecol Manage 2551536ndash1547 (2008) doi 101016jforeco200711027

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116 P R Jennings Plant type as a rice breeding objectiveCrop Sci 4 13ndash15 (1964) doi 102135cropsci19640011183X000400010005x

117 W G Duncan W A Williams R S Loomis Tassels andproductivity of maize Crop Sci 7 37ndash39 (1967)doi 102135cropsci19670011183X000700010013x

118 D N Duvick K G Cassman Post-green-revolution trends inyield potential of temperate maize in the north-central UnitedStates Crop Sci 39 1622ndash1630 (1999) doi 102135cropsci19993961622x

119 J Weiner S B Andersen W K M Wille H W GriepentrogJ M Olsen Evolutionary Agroecology The potential forcooperative high density weed-suppressing cerealsEvol Appl 3 473ndash479 (2010) doi 101111j1752-4571201000144x

120 M J Wade P Bijma E D Ellen W Muir Group selectionand social evolution in domesticated animals Evol Appl 3453ndash465 (2010) doi 101111j1752-4571201000147x

121 J Liu et al Coupled human and natural systems Ambio 36639ndash649 (2007) doi 1015790044-7447(2007)36[639CHANS]20CO2 pmid 18240679

122 P Rabinowitz L Conti Links among human health animalhealth and ecosystem health Annu Rev Public Health34 189ndash204 (2013) doi 101146annurev-publhealth-031912-114426 pmid 23330700

123 M E J Woolhouse S Gowtage-Sequeria Host range andemerging and reemerging pathogens Emerg Infect Dis11 1842ndash1847 (2005) doi 103201eid1112050997pmid 16485468

124 B Olsen et al Global patterns of influenza a virus in wild birdsScience 312 384ndash388 (2006) doi 101126science1122438pmid 16627734

125 G J D Smith et al Origins and evolutionary genomicsof the 2009 swine-origin H1N1 influenza A epidemicNature 459 1122ndash1125 (2009) doi 101038nature08182pmid 19516283

126 K E Jones et al Global trends in emerging infectiousdiseases Nature 451 990ndash993 (2008) doi 101038nature06536 pmid 18288193

127 W Ma R E Kahn J A Richt The pig as a mixing vesselfor influenza viruses Human and veterinary implicationsJ Mol Genet Med 3 158ndash166 (2008) pmid 19565018

128 H M Yassine C W Lee Y M Saif Interspecies transmissionof influenza A viruses between swine and poultry Curr TopMicrobiol Immunol 370 227ndash240 (2011) doi 10100782_2011_180 pmid 22167468


RESEARCH | REVIEW

129 S Altizer R Bartel B A Han Animal migration andinfectious disease risk Science 331 296ndash302 (2011)doi 101126science1194694 pmid 21252339

130 K R Riacuteos-Soto B Song C Castillo-Chavez Epidemic spreadof influenza viruses The impact of transient populationson disease dynamics Math Biosci Eng 8 199ndash222 (2011)doi 103934mbe20118199 pmid 21361408

131 K M Pepin S Lass J R Pulliam A F Read J O Lloyd-SmithIdentifying genetic markers of adaptation for surveillanceof viral host jumps Nat Rev Microbiol 8 802ndash813 (2010)doi 101038nrmicro2440 pmid 20938453

132 European Center for Disease Prevention and Control andEuropean Medicines Agency The Bacterial ChallengeTime to React (ECDCEMEA Joint Technical Report EMEA5761762009 Stockholm 2009)

133 Alliance for the Prudent Use of Antibiotics The Cost ofAntibiotic Resistance to US Families and the HealthcareSystem (APUA Boston MA 2010)

134 M A Cooper D Shlaes Fix the antibiotics pipeline Nature472 32ndash32 (2011) doi 101038472032a pmid 21475175

135 M S Butler M A Blaskovich M A Cooper Antibiotics in theclinical pipeline in 2013 J Antibiot (Tokyo) 66 571ndash591(2013) doi 101038ja201386 pmid 24002361

136 A M Bal I M Gould Antibiotic stewardship Overcomingimplementation barriers Curr Opin Infect Dis 24357ndash362 (2011) doi 101097QCO0b013e3283483262pmid 21587070

137 C MacDougall R E Polk Antimicrobial stewardshipprograms in health care systems Clin Microbiol Rev 18638ndash656 (2005) doi 101128CMR184638-6562005pmid 16223951

138 US Food and Drug Administration ldquo2009 Summary report onantimicrobials sold or distributed for use in food-producinganimalsrdquo (FDA Washington DC 2010)

139 E K Silbergeld J Graham L B Price Industrial foodanimal production antimicrobial resistance and humanhealth Annu Rev Public Health 29 151ndash169 (2008)doi 101146annurevpublhealth29020907090904pmid 18348709

140 M E J Woolhouse M J W Ward Sources of antimicrobialresistance Science 341 1460ndash1461 (2013) doi 101126science1243444 pmid 24030495

141 A R Manges J R Johnson Food-borne origins of Escherichiacoli causing extraintestinal infections Clin Infect Dis 55712ndash719 (2012) doi 101093cidcis502 pmid 22615330

142 J L Martinez J Olivares in Antimicrobial Resistancein the Environment P L Keen M H M M Montforts(Wiley-Blackwell Hoboken NJ 2011) chap 9 pp 157ndash172

143 Transatlantic Taskforce on Antimicrobial ResistanceRecommendations for future collaboration between theUS and EU (TATFAR Report 2011) httpwwwecdceuropaeuenactivitiesdiseaseprogrammesTATFARDocuments210911_TATFAR_Reportpdf

144 European Commission Communication from the Commissionto the European Parliament and the Council Action planagainst the rising threats from Antibmicrobial ResistanceCOM 748 (2011) httpeceuropaeudgshealth_consumerdocscommunication_amr_2011_748_enpdf

145 FDA New animal drugs cephalosporin drugs extralabelanimal drug use order of prohibition Fed Regist 77 735httpfederalregistergova2012-35 (2012)

146 S P Carroll M T Kinnison L Bernatchez In light ofevolution Interdisciplinary challenges in food health andthe environment Evol Appl 4 155ndash158 (2011) doi 101111j1752-4571201100182x

147 D Griggs et al Policy Sustainable development goalsfor people and planet Nature 495 305ndash307 (2013)doi 101038495305a pmid 23518546

148 Convention of Biological Diversity Aichi BiodiversityTargets Strategic Plan for Biodiversity 2011ndash2020 (2010)wwwcbdintsptargets

149 C Joslashrgensen et al Managing evolving fish stocks Science318 1247ndash1248 (2007) doi 101126science1148089pmid 18033868

150 A T Laugen et al Evolutionary impact assessment Accountingfor evolutionary consequences of fishing in an ecosystemapproach to fisheries management Fish Fish 15 1ndash32 (2012)

151 M L Baskett R S Waples Evaluating alternative strategiesfor minimizing unintended fitness consequences ofcultured individuals on wild populations Conserv Biol 2783ndash94 (2013) doi 101111j1523-1739201201949xpmid 23082984

152 Convention on Biological Diversity The Nagoya Protocol onAccess and Benefit-Sharing (2013) wwwcbdintabs

153 L Santamariacutea P F Meacutendez Evolution in biodiversitypolicy - current gaps and future needs Evol Appl 5202ndash218 (2012) doi 101111j1752-4571201100229x

154 E W Welch Potential implications of the Nagoya Protocol forthe livestock sector J Anim Breed Genet 129 423ndash424(2012) pmid 23148966

155 J A Jackson L Laikre C S Baker K C Kendall Guidelinesfor collecting and maintaining archives for geneticmonitoring Conserv Genet Resour 4 527ndash536 (2012)doi 101007s12686-011-9545-x

156 G V Dana T Kuiken D Rejeski A A Snow Synthetic biologyFour steps to avoid a synthetic-biology disaster Nature 48329ndash29 (2012) doi 101038483029a pmid 22382962

157 Convention on Biological Diversity Conference of the PartiesCOP 11 Decision XI11 New and emerging issues relating tothe conservation and sustainable use of biodiversity (2012)wwwcbdintdecisioncopdefaultshtmlid=13172

158 K A Oye et al Regulating gene drives Science 345626ndash628 (2014) doi 101126science1254287

159 S Oberthuumlr T Gehring Institutional interaction in globalenvironmental governance The case of the CartagenaProtocol and the World Trade Organization Global EnvironPolit 6 1ndash31 (2006) doi doi101162glep2006621

160 A A Snow V H Smith Genetically engineered algae forbiofuels A key role for ecologists Bioscience 62 765ndash768(2012) doi 101525bio20126289

161 P Mali et al RNA-guided human genome engineering viaCas9 Science 339 823ndash826 (2013) doi 101126science1232033 pmid 23287722

162 M A Thomas et al Ecology Gene tweaking for conservationNature 501 485ndash486 (2013) doi 101038501485apmid 24073449

163 K H Redford W Adams G M Mace Synthetic biology andconservation of nature Wicked problems and wickedsolutions PLoS Biol 11 e1001530 (2013) doi 101371journalpbio1001530 pmid 23565062

164 B M Althouse T C Bergstrom C T Bergstrom Evolution inhealth and medicine Sackler colloquium A public choiceframework for controlling transmissible and evolving diseasesProc Natl Acad Sci USA 107 (suppl 1) 1696ndash1701(2010) doi 101073pnas0906078107 pmid 20018681

165 J Liu et al Complexity of coupled human and naturalsystems Science 317 1513ndash1516 (2007) doi 101126science1144004 pmid 17872436

166 E Ostrom A general framework for analyzing sustainabilityof social-ecological systems Science 325 419ndash422 (2009)doi 101126science1172133 pmid 19628857

167 E Ostrom A diagnostic approach for going beyond panaceasProc Natl Acad Sci USA 104 15181ndash15187 (2007)doi 101073pnas0702288104 pmid 17881578

168 G Hardin The tragedy of the commons Science 1621243ndash1248 (1968) pmid 5699198

169 F Baquero J Campos The tragedy of the commons inantimicrobial chemotherapy Rev Esp Quimioter 16 11ndash13(2003) [Editorial] pmid 12750754

170 W D Hutchison et al Areawide suppression of Europeancorn borer with Bt maize reaps savings to non-Bt maizegrowers Science 330 222ndash225 (2010) doi 101126science1190242 pmid 20929774

171 G Jaffe Complacency on the Farm Significant Noncompliancewith EPAs Refuge Requirements Threatens the Future Effectivenessof Genetically Engineered Pest-Protected Corn (Center for Sciencein the Public Interest Washington DC 2009)

172 P A Samuelson The pure theory of public expenditureRev Econ Stat 36 387ndash389 (1954) doi 1023071925895

173 D J Nokes R M Anderson Vaccine safety versus vaccineefficacy in mass immunisation programmes Lancet 3381309ndash1312 (1991) doi 1010160140-6736(91)92601-Wpmid 1682694

174 K Kaier U Frank Measuring the externality ofantibacterial use from promoting antimicrobial resistancePharmacoeconomics 28 1123ndash1128 (2010) doi 10216511535640-000000000-00000 pmid 21108531

175 K Kaier Economic modeling of the persistence ofantimicrobial resistance Nat Resour Model 25 388ndash402(2012) doi 101111j1939-7445201100114x

176 G D Wright Antibiotic resistance in the environmentA link to the clinic Curr Opin Microbiol 13 589ndash594 (2010)doi 101016jmib201008005 pmid 20850375

177 M Herrmann R Laxminarayan Antibiotic effectivenessNew challenges in natural resource management Annu RevResour Econom 2 125ndash138 (2010) doi 101146annurevresource050708144125

178 C N Cook M B Mascia M W Schwartz H P PossinghamR A Fuller Achieving conservation science that bridgesthe knowledge-action boundary Conserv Biol 27 669ndash678(2013) doi 101111cobi12050 pmid 23574343

179 J Antonovics et al Evolution by any other nameAntibiotic resistance and avoidance of the E-word PLoSBiol 5 e30 (2007) doi 101371journalpbio0050030pmid 17298172

ACKNOWLEDGMENTS

MTK RFD SPC SYS and TBS were supported by grantsfrom NSF CTB is supported by National Institute of GeneralMedical Sciences NIH grant number U54GM088558 MTK issupported by Maine Agricultural and Forest Experiment StationPDG by the National Research Centre for Growth andDevelopment SPC by Commonwealth Scientific and IndustrialResearch Organization (Australia) and the Australian-AmericanFulbright Commission SYS by grants from the College ofBiological Sciences University of California Davis TBS bygrants from NIH and BET by US Department of AgricultureBiotechnology Risk Assessment grant 2011-33522-30729 PSJacknowledges the Danish National Research Foundation forsupport to the Center for Macroecology Evolution and Climateand the American-Scandinavian Foundation S Singhal J BoomsmaC Rahbek N Strange and T Fuller provided useful commentson previous versions of the manuscript G Reygondeau providedadvice for the summary figure

SUPPLEMENTARY MATERIALS

wwwsciencemagorgcontent34662071245993supplDC1Materials and MethodsSupplementary TextTables S1 to S2References (180ndash246)

101126science1245993


RESEARCH | REVIEW

wwwsciencemagorgcgicontentfullscience1245993DC1

Supplementary Materials for


Scott P Carroll Peter Soslashgaard Joslashrgensen Michael T Kinnison Carl T Bergstrom R Ford Denison Peter Gluckman Thomas B Smith Sharon Y Strauss

Bruce E Tabashnik

Corresponding author E-mail spcarrollucdavisedu (SPC) psjorgensenbiokudk (PSJ)

Published 11 September 2014 on Science Express DOI 101126science1245993

This PDF file includes

Materials and Methods Supplementary Text Tables S1 and S2 References

Carroll et al 1 Supplementary Materials

Materials and Methods Choice sources and explanation of information used to create Fig 1

In creating Fig 1 we focused on organisms in all or some of areas of the applied life sciences that are the main focus of the manuscript namely the areas of Medicine Agriculture and Natural Resources and Conservation Biology

The aim here was to show that these areas of the applied life sciences share concerns for the two evolutionary dilemmas and that these concerns can be mapped through the traits of the organisms Secondly we also wanted to illustrate characteristics that help to differentiate some disciplines from others such as the management of small population sizes in some contexts of conservation biology and medicine

Since it can be argued that every organism is affected by human management actions to some degree it follows directly that a conceptual figure trying to span such a diversity of life necessarily must make some very rough generalizations and omit many interesting exceptions to the rule

We focused on organisms important in all areas of the applied life-sciences as well as those important in sectors which are the main focus of the manuscript namely Medicine Agriculture and Natural Resources and Conservation Biology

The data We gathered representative estimates of minimum and maximum generation times and population sizes for organisms that are direct or indirect targets of management actions in the applied life-sciences) These estimates were used to draw the lower and upper boundaries of ovals on the x- and y-axes Estimates were gathered from the published literature supplemented with estimates of woody plant generation times from the COMPADRE III database (178)

Table S1 outlines the sources and assumptions for each estimate For some minimum and maximum values we could not find good published estimates and therefore chose artificial cutoff values that reflect the general notion of how the organisms in each group (oval) relate to the organisms in other groups It was especially hard to find estimates for minimum and maximum population size In this case we chose several of the cutoff values to reflect the general notion that conservation biology often operates to protect smaller global population sizes than do agriculture and natural resource management


Table S1 References for Fig 1 Group Generation time

Population size

(individuals cells viruses) Minimum Central Maximum Minimum Central Maximum All applied life sciences Viral and microbial pathogens mutualists and commensals

Escherichia coli 17 min (179) HIV 12 d (180)

Algae 11 hours (181

182)

Mycobacterium leprae 30 d

(183)

Arbitrary limit at 106 (184)

14x107 to 195x108 cells of a

strain EA25 per gram of soil (185)

(14 gcm3 soil assumed)

1014 to 14x1015 cells 10 m3 soil

Pests weeds invasive species Macrocheles

muscaedomes-ticae 45 d

(186) Drosophila 14

d

Annual life cycles are

common in weedy species

Generally less than 10 yr

Arbitrary limit at 5104

indicating large

minimum global

population sizes

Arbitrary limit at 1010 indicating large maximum

global population sizes

Medicine Human myelocytes

29 days (187)

70x108 cells kg times 80 kg =561010 cells (187)

Human epithelia 5 d (188) intestinal

gt101011 (189)

Human adipocytes 84 yr (190) 401010 (190) 701010 (190) Human neurons lt1 of neocortica

neurons turnover 86 plusmn 81 x109

neurons in


during human life (191) limit set to

100 yr

brain (192)

Humans 25-30 yr (193) ~1 human

109 projected population size in

2050 (194) Agriculture and Natural Resources AquaAgricultureBiofuels

Tree Pinus

sylvestris 14 yr (195 196)


Eucalyptus globulus 50109 (Australia) (197)

Natural resources Small crustacean

food sources 14 d (198)

Pollinators eg 1 yr (199)

Salmon 1-4 yr (200)

Pinus ponderosa 348

yr (201) Eucalyptus 30-

200 yr (197)


Eucalyptus globulus 50x109 (Australia) (197)

Conservation Biology Conservation biology Arbitrary limit

at 30 d representative of eg some

fast reproducing

insects

Sabal palmetto 861 yr (178

202) Sea turtles gt 20 yr (200) Elephant 33 yr

(200)

10-50 set as lower limit

106 set as cut-off Most species-level conservation plans

deal with population sizes

below 106

Table S2 Expanded and referenced presentation of the examples shown in Fig 3 Management objective Challenge Strategy

applied Evolutionary

principle Tactic Agriculture Health Environment


Control pests and pathogens

Slow evolution

Spatial heterogeneity in selection

Refuge Gene flow

from treatment-free space favors the preferred

form

Slow pest adaptation to insecticidal GE crops by providing

host plants on which susceptible pests can

survive (74 75)

Slow chemoresistance

evolution in tumors (80) and to

antimicrobial resistance evolution in pathogens (81) by sheltering susceptible

strains

Protect evolving resistance to non-native

competitor (203) control evolution of undesirable traits in wild-harvested

species [small size early reproduction (204)]

Temporal heterogeneity in selection

Alternating treatments

slows adaptation to

a single treatment

Slow pest adaptation by rotating crops or pesticides (97 205

206)

Slow resistance evolution in

infectious disease by cycling (94 207)

Little explored from evolutionary perspective

employing different techniques in sequence may improve efficacy

(208) for counter-example see (209)

Diversify selection to

exploit adaptive tradeoffs

Apply multiple stressors

with different modes of

action together

Slow pest adaptation to control measures with integrated pest management (4 96

210)

Slow resistance evolution in infectious

disease by mixing (139) multitarget vaccines (211)

complementary tumor therapies (81)

complement partial vaccines with

transmission control (212) increase

longevity of live attenuated vaccines

(213)

Target multiple vulnerabilities at once

(eg via multiple modes of action [physical

chemical ecological (214)]


Selection for acceptable

traits in adversaries

Select for less injurious

genotypes

Field management eg frequent mowing of forage crop selects for weeds that shade

less (215)

Increase relative survival of more

benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load

Transgenic deleterious mutation

Reduce fitness of insect vectors of crop

viruses (216)

Accelerate rate of deleterious viral

mutations (217 218) reduce dengue virus vector populations

(219)

No cases found

Promote adaptation of desired organisms

Reduce phenotype-

environment mismatch

Reduce selection in

situ or shift to better

environment

Modify environment

or move population to

a suitable one

Migration of agricultural economies

(220) switch crops (221) factor mismatch

in cues like photoperiod in

breeding programs (222)

Employ adaptive dietary and lifestyle approaches to reduce

cardiovascular disease (223) cancer (224) and adult and offspring metabolic

disease (225)

Assist migration of threatened populations to

more suitable environments (226 227) alter land use regime to

improve habitat for natives (228)

Increase adaptation to present and

environments

GE hybridization and artificial

selection

Preserve Vg in wild crop relatives (229)

favor heat and drought resistant cereals (230)

enhance artificial selection with

molecular breeding (54) novel GE and hybrid phenotypes

(230)

Employ recombinant DNA technologies for vaccine (231) drug (232) and hormone (233)

production gene therapy (234)

Select for tolerance and resistance in

reintroduction or translocation (235)

introgress genes across existing gradients (79 236) facilitate in situ

evolution (237 238) use hybrid introgression of resistance genes (239)


Increase group

performance

Group selection

cooperation intrapopulation diversification

Select or produce variants based on

group performance

Productivity (240 241) resource use

efficiency (242) weed suppression (119)

Formalize public health strategies to incorporate public

and private benefits (161)

Manage environment to produce more diverse phenotypes reducing

intrapopulation competition and

increasing population resilience (243) reduce unwanted selection with marine reserves (79 204)

Carroll et al 7

Supplementary Text

Image credits for Fig 1 A Methicillin-resistant Staphylococcus aureus bacteria MRSA (yellow) being

ingested by neutrophil (purplish blue) Photo credit NIAID License Creative Commons Attribution 20 Generic httpscreativecommonsorglicensesby20legalcode Web httpswwwflickrcomphotosniaid5614218718

B Killer whale Orcinus orca viewed by child Cropped Photo credit cmiper License Creative Commons Attribution-NonCommercial 20 Generic (CC BY-NC 20) httpscreativecommonsorglicensesby-nc20 Web httpswwwflickrcomphotoscmiper666163487inphotolist-21Sgcn-dEwNMP-dEwY68-dEwReZ-dECmRQ-bVGQav-cd5aSs-Juysf-7HzMs-7cV6tM-9RNj3j-itCDm-itCmg-itCoJ-itCgn-itCL6-itCmw-itCk3-dMYi3y-YWkUF-7DBsjF-2THYc5-2THXAb-acDTat-ejQD7x-mRihre-dBA89W-7236f4-4j5w2T-5

Image credits for Fig 2 A Bt corn comparison Photo credit Gary Munkvold Iowa State University

B Measles vaccination Photo credit Pete LewisDepartment for International Development License Creative Commons Attribution 20 Generic httpscreativecommonsorglicensesby20legalcode Web httpswwwflickrcomphotosdfid5815109843inphotolist-9RRXyx-9wwhXH-cHXCff-NgLky-NgLjA-a5BCyY-LAg1G-do33qb-aaq1jL-aancAK-aaq1gd-9XM1gh-jxueq5-76tSgJ-do33iN-do33Au-do334N-do33kW-do32L9-do33y1-do2VMe-do2W7n-do2VPv-do33go-do32S5-do2Wqx-do32NN-do2VDn-do

C Dam removal Photo credit Penobscot River Restoration Trust License Copyright Penobscot River Restoration Trust

Image credits for Fig 4 Images have been chosen for their illustrative value and conveying of message None

of the images relate specifically to works cited in the manuscript

A Mallards Photo credit Petri Pusa License Copyright Petri Pusa

B Flying birds clip art Photo credit Naresh Clker License Public Domain

Web httpwwwclkercomcliparts2ec11338759819101833965birds-flying-silhouette-clip-art20(1)-hipng

C Chickens Photo credit US Department of Agriculture License Creative Commons ShareAlike Web httpcommonswikimediaorgwikiFile20110420-RD-LSC-0893_-_Flickr_-_USDAgovjpg

D Meat packages Photo credit Mattes License Creative Commons ShareAlike WebhttpcommonswikimediaorgwikiFileMeat_packages_in_a_Roman_supermark

etjpg

Carroll et al 8

E Hospital beds Photo credit Канопус Киля License Public Domain Web httpcommonswikimediaorgwikiFile3AHospital_bedsjpg

F Discharge pipe Photo credit US Department of Agriculture License Public Domain

Web httpcommonswikimediaorgwikiFileDischarge_pipejpg file

Author contributions SPC PSJ and MTK conceived and wrote the initial manuscript PSJ and SPC led the

subsequent revision and work process with input from MTK and conducted the review of management examples with important contributions from all coauthors BET contributed especially to writing about resistance management and to overall editing CTB and RFD led the review of regulatory mechanisms and evolutionary manipulation of group performance in crops respectively PDG contributed especially to the analysis of evolutionary mismatch and implementing applied evolution in medicine and public health TBS and SYS contributed text and perspectives on evolutionary conservation management and participated in general editing

References and Notes 1 Millennium Ecosystem Assessment Ecosystems and Human Well-being Synthesis

(Island Press Washington DC 2005)

2 E C Ellis J O Kaplan D Q Fuller S Vavrus K Klein Goldewijk P H Verburg Used planet A global history Proc Natl Acad Sci USA 110 7978ndash7985 (2013) Medline doi101073pnas1217241110

3 R G Latta Conservation genetics as applied evolution From genetic pattern to evolutionary process Evol Appl 1 84ndash94 (2008) doi101111j1752-4571200700008x

4 S R Palumbi Humans as the worldrsquos greatest evolutionary force Science 293 1786ndash1790 (2001) Medline doi101126science29355361786

5 P D Gluckman C T Bergstrom Evolutionary biology within medicine A perspective of growing value BMJ 343 (dec19 1) d7671 (2011) Medline doi101136bmjd7671

6 F Gould Broadening the application of evolutionarily based genetic pest management Evolution 62 500ndash510 (2008) Medline doi101111j1558-5646200700298x

7 P H Thrall J G Oakeshott G Fitt S Southerton J J Burdon A Sheppard R J Russell M Zalucki M Heino R Ford Denison Evolution in agriculture The application of evolutionary approaches to the management of biotic interactions in agro-ecosystems Evol Appl 4 200ndash215 (2011) doi101111j1752-4571201000179x

8 R F Denison Darwinian Agriculture How Understanding Evolution Can Improve Agriculture (Princeton Univ Press Princeton NJ 2012)

9 D W Hollomon Do we have the tools to manage resistance in the future Pest Manag Sci 68 149ndash154 (2012) Medline doi101002ps2291

10 C A Stockwell A P Hendry M K Kinnison Contemporary evolution meets

Carroll et al 9

conservation biology Trends Ecol Evol 18 94ndash101 (2003) doi101016S0169-5347(02)00044-7

11 A P Hendry L G Lohmann E Conti J Cracraft K A Crandall D P Faith C Haumluser C A Joly K Kogure A Larigauderie S Magalloacuten C Moritz S Tillier R Zardoya A H Prieur-Richard B A Walther T Yahara M J Donoghue Evolutionary biology in biodiversity science conservation and policy A call to action Evolution 64 1517ndash1528 (2010) Medline

12 A P Hendry M T Kinnison M Heino T Day T B Smith G Fitt C T Bergstrom J Oakeshott P S Joslashrgensen M P Zalucki G Gilchrist S Southerton A Sih S Strauss R F Denison S P Carroll Evolutionary principles and their practical application Evol Appl 4 159ndash183 (2011) doi101111j1752-4571201000165x

13 WHO Antimicrobial resistance global report on surveillance (2014) wwwwhointdrugresistancedocumentssurveillancereporten

14 B E Tabashnik D Mota-Sanchez M E Whalon R M Hollingworth Y Carriegravere Defining terms for proactive management of resistance to Bt crops and pesticides J Econ Entomol 107 496ndash507 (2014) Medline doi101603EC13458

15 P D Gluckman M A Hanson Mismatch Why Our World No Longer Fits Our Bodies (Oxford Univ Press Oxford 2006)

16 A D Barnosky N Matzke S Tomiya G O Wogan B Swartz T B Quental C Marshall J L McGuire E L Lindsey K C Maguire B Mersey E A Ferrer Has the Earthrsquos sixth mass extinction already arrived Nature 471 51ndash57 (2011) Medline doi101038nature09678

17 J J Bull H A Wichman Applied evolution Annu Rev Ecol Syst 32 183ndash217 (2001) doi101146annurevecolsys32081501114020

18 S P Carroll C W Fox Conservation Biology Evolution in Action (Oxford Univ Press Oxford 2008)

19 P D Gluckman M A Hanson T Buklijas F M Low A S Beedle Epigenetic mechanisms that underpin metabolic and cardiovascular diseases Nat Rev Endocrinol 5 401ndash408 (2009) Medline doi101038nrendo2009102

20 D Hartl A Primer of Population Genetics (Sinauer Associates Inc Sunderland MA 1988)

21 P A Abrams Modelling the adaptive dynamics of traits involved in inter- and intraspecific interactions An assessment of three methods Ecol Lett 4 166ndash175 (2001) doi101046j1461-0248200100199x

22 C K Ghalambor J K McKay S P Carroll D N Reznick Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments Funct Ecol 21 394ndash407 (2007) doi101111j1365-2435200701283x

23 M T Kinnison N G Hairston Eco-evolutionary conservation biology Contemporary evolution and the dynamics of persistence Funct Ecol 21 444ndash454 (2007) doi101111j1365-2435200701278x

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24 C A Aktipis V S Kwan K A Johnson S L Neuberg C C Maley Overlooking evolution A systematic analysis of cancer relapse and therapeutic resistance research PLOS ONE 6 e26100 (2011) Medline doi101371journalpone0026100

25 N Mouquet V Devictor C N Meynard F Munoz L F Bersier J Chave P Couteron A Dalecky C Fontaine D Gravel O J Hardy F Jabot S Lavergne M Leibold D Mouillot T Muumlnkemuumlller S Pavoine A Prinzing A S Rodrigues R P Rohr E Theacutebault W Thuiller Ecophylogenetics Advances and perspectives Biol Rev Camb Philos Soc 87 769ndash785 (2012) Medline doi101111j1469-185X201200224x

26 G M Mace A Purvis Evolutionary biology and practical conservation Bridging a widening gap Mol Ecol 17 9ndash19 (2008) Medline doi101111j1365-294X200703455x

27 L-M Chevin R Gallet R Gomulkiewicz R D Holt S Fellous Phenotypic plasticity in evolutionary rescue experiments Philos Trans R Soc Lond B Biol Sci 368 20120089 (2013) Medline doi101098rstb20120089

28 A F Read S Huijben Evolutionary biology and the avoidance of antimicrobial resistance Evol Appl 2 40ndash51 (2009) doi101111j1752-4571200800066x

29 A F Read T Day S Huijben The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy Proc Natl Acad Sci USA 108 (suppl 2) 10871ndash10877 (2011) Medline doi101073pnas1100299108

30 M V Ashley M F Willson O R W Pergams D J OrsquoDowd S M Gende J S Brown Evolutionarily enlightened management Biol Conserv 111 115ndash123 (2003) doi101016S0006-3207(02)00279-3

31 S E Williams E A Hoffman Minimizing genetic adaptation in captive breeding programs A review Biol Conserv 142 2388ndash2400 (2009) doi101016jbiocon200905034

32 K Leus K Traylor-Holzer R C Lacy Genetic and demographic population management in zoos and aquariums Recent developments future challenges and opportunities for scientific research Int Zoo Yearb 45 213ndash225 (2011) doi101111j1748-1090201100138x

33 P D Gluckman F M Low T Buklijas M Hanson A S Beedle How evolutionary principles improve the understanding of human health and disease Evol Appl 4 249ndash263 (2011) doi101111j1752-4571201000164x

34 L Cordain S B Eaton A Sebastian N Mann S Lindeberg B A Watkins J H OrsquoKeefe J Brand-Miller Origins and evolution of the Western diet Health implications for the 21st century Am J Clin Nutr 81 341ndash354 (2005) Medline

35 R C Brownson D Haire-Joshu D A Luke Shaping the context of health A review of environmental and policy approaches in the prevention of chronic diseases Annu Rev Public Health 27 341ndash370 (2006) Medline doi101146annurevpublhealth27021405102137

36 T A Gaziano N Pagidipati Scaling up chronic disease prevention interventions in

Carroll et al 11

lower- and middle-income countries Annu Rev Public Health 34 317ndash335 (2013) Medline doi101146annurev-publhealth-031912-114402

37 C D Mathers D Loncar Projections of global mortality and burden of disease from 2002 to 2030 PLOS Med 3 e442 (2006) Medline doi101371journalpmed0030442

38 D E Bloom et al ldquoThe global economic burden of noncommunicable diseasesrdquo (Working paper no 87 Program on the Global Demography of Aging Harvard School of Public Health World Economic Forum Geneva 2012)

39 J Woodcock O H Franco N Orsini I Roberts Non-vigorous physical activity and all-cause mortality Systematic review and meta-analysis of cohort studies Int J Epidemiol 40 121ndash138 (2011) Medline doi101093ijedyq104


41 J Lynch G D Smith A life course approach to chronic disease epidemiology Annu Rev Public Health 26 1ndash35 (2005) Medline doi101146annurevpublhealth26021304144505

42 D A Chokshi T A Farley The cost-effectiveness of environmental approaches to disease prevention N Engl J Med 367 295ndash297 (2012) Medline doi101056NEJMp1206268

43 T Rolph et al Loss-of-function mutations in SLC30A8 protect against type 2 diabetes Nat Genet 2 March 2014

44 G S Omenn Evolution in health and medicine Sackler colloquium Evolution and public health Proc Natl Acad Sci USA 107 (suppl 1) 1702ndash1709 (2010) Medline doi101073pnas0906198106

45 J C Denny L Bastarache M D Ritchie R J Carroll R Zink J D Mosley J R Field J M Pulley A H Ramirez E Bowton M A Basford D S Carrell P L Peissig A N Kho J A Pacheco L V Rasmussen D R Crosslin P K Crane J Pathak S J Bielinski S A Pendergrass H Xu L A Hindorff R Li T A Manolio C G Chute R L Chisholm E B Larson G P Jarvik M H Brilliant C A McCarty I J Kullo J L Haines D C Crawford D R Masys D M Roden Systematic comparison of phenome-wide association study of electronic medical record data and genome-wide association study data Nat Biotechnol 31 1102ndash1111 (2013) Medline doi101038nbt2749

46 M Travisano R G Shaw Lost in the map Evolution 67 305ndash314 (2013) Medline doi101111j1558-5646201201802x

47 S M Rappaport Implications of the exposome for exposure science J Expo Sci Environ Epidemiol 21 5ndash9 (2011) Medline doi101038jes201050

48 H C J Godfray J R Beddington I R Crute L Haddad D Lawrence J F Muir J Pretty S Robinson S M Thomas C Toulmin Food security The challenge of feeding 9 billion people Science 327 812ndash818 (2010) Medline doi101126science1185383

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49 C James ldquoExecutive summary Global status of commercialized biotechGM cropsrdquo (ISAAA Brief 46 International Service for the Acquisitions of Agri-Biotech Applications New York 2013)

50 M Ashraf Inducing drought tolerance in plants Recent advances Biotechnol Adv 28 169ndash183 (2010) Medline doi101016jbiotechadv200911005

51 E Pauwels Public understanding of synthetic biology BioScience 63 79ndash89 (2013) doi101525bio20136324

52 P Aerni Resistance to agricultural biotechnology The importance of distinguishing between weak and strong public attitudes Biotechnol J 8 1129ndash1132 (2013) Medline

53 S-E Jacobsen M Soslashrensen S M Pedersen J Weiner Feeding the world Genetically modified crops versus agricultural biodiversity Agron Sustain Dev 33 651ndash662 (2013) doi101007s13593-013-0138-9

54 R K Varshney K C Bansal P K Aggarwal S K Datta P Q Craufurd Agricultural biotechnology for crop improvement in a variable climate Hope or hype Trends Plant Sci 16 363ndash371 (2011) Medline doi101016jtplants201103004

55 A Marshall Drought-tolerant varieties begin global march Nat Biotechnol 32 308ndash308 (2014) doi101038nbt2875

56 R K Varshney J M Ribaut E S Buckler R Tuberosa J A Rafalski P Langridge Can genomics boost productivity of orphan crops Nat Biotechnol 30 1172ndash1176 (2012) Medline doi101038nbt2440

57 S Yang B Vanderbeld J Wan Y Huang Narrowing down the targets Towards successful genetic engineering of drought-tolerant crops Mol Plant 3 469ndash490 (2010) Medline doi101093mpssq016

58 A C M Gaudin A Henry A H Sparks I H Slamet-Loedin Taking transgenic rice drought screening to the field J Exp Bot 64 109ndash117 (2013) Medline doi101093jxbers313

59 International Service for the Acquisition of Agric -Biotech Applications Approval Database 2013 httpwwwisaaaorggmapprovaldatabasedefaultasp (2013)

60 K L Mercer H R Perales J D Wainwright Climate change and the transgenic adaptation strategy Smallholder livelihoods climate justice and maize landraces in Mexico Glob Environ Change 22 495ndash504 (2012) doi101016jgloenvcha201201003

61 M Tachibana P Amato M Sparman J Woodward D M Sanchis H Ma N M Gutierrez R Tippner-Hedges E Kang H S Lee C Ramsey K Masterson D Battaglia D Lee D Wu J Jensen P Patton S Gokhale R Stouffer S Mitalipov Towards germline gene therapy of inherited mitochondrial diseases Nature 493 627ndash631 (2013) Medline doi101038nature11647

62 J H Kordower D Kirik Introduction Gene therapy has gone from a pipe dream to clinical reality Neurobiol Dis 48 151ndash152 (2012) Medline doi101016jnbd201207014

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63 I-K Choi C-O Yun Recent developments in oncolytic adenovirus-based immunotherapeutic agents for use against metastatic cancers Cancer Gene Ther 20 70ndash76 (2013) Medline doi101038cgt201295

64 D M Lipinski M Thake R E MacLaren Clinical applications of retinal gene therapy Prog Retin Eye Res 32 22ndash47 (2013) Medline doi101016jpreteyeres201209001

65 K J Wert R J Davis J Sancho-Pelluz P M Nishina S H Tsang Gene therapy provides long-term visual function in a pre-clinical model of retinitis pigmentosa Hum Mol Genet 22 558ndash567 (2013) Medline doi101093hmgdds466

66 K Suzuki H Matsubara Recent advances in p53 research and cancer treatment J Biomed Biotechnol 2011 1 (2011) Medline doi1011552011978312

67 O Kilpivaara L A Aaltonen Diagnostic cancer genome sequencing and the contribution of germline variants Science 339 1559ndash1562 (2013) Medline doi101126science1233899

68 P R Lowenstein M G Castro Why do Most Phase III Clinical Trials Fail Uncertainty in the translation of preclinical experiments to clinical trials Why do most phase III clinical trials fail Curr Gene Ther 9 368ndash374 (2009) Medline doi102174156652309789753392

69 M Edelstein M Gene Therapy Clinical Trials Worldwide J Gene Medicine database at httpwwwabediacomwileyindexhtml (2014) (accessed April 13 2014)

70 C C Vigueira K M Olsen A L Caicedo The red queen in the corn Agricultural weeds as models of rapid adaptive evolution Heredity 110 303ndash311 (2013) Medline doi101038hdy2012104

71 S E Greene A Reid Moving Targets Fighting the Evolution of Resistance in Infections Pests and Cancer (American Society of Microbiology Washington DC 2013) httpbitlyYeNhoS

72 S B Powles Q Yu Evolution in action Plants resistant to herbicides Annu Rev Plant Biol 61 317ndash347 (2010) Medline doi101146annurev-arplant-042809-112119

73 I Heap The International Survey of Herbicide Resistant Weeds (2013) wwwweedsciencecomsummaryhomeaspx

74 B E Tabashnik Evolution of resistance to Bacillus thuringiensis Annu Rev Entomol 39 47ndash79 (1994) doi101146annureven39010194000403

75 F Gould Sustainability of transgenic insecticidal cultivars Integrating pest genetics and ecology Annu Rev Entomol 43 701ndash726 (1998) Medline doi101146annurevento431701

76 US Environmental Protection Agency The Environmental Protection Agencyrsquos White Paper on Bt Plant-pesticide Resistance Management (EPA Washington DC 1998)

77 B E Tabashnik T Breacutevault Y Carriegravere Insect resistance to Bt crops Lessons from the first billion acres Nat Biotechnol 31 510ndash521 (2013) Medline doi101038nbt2597

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78 B E Tabashnik A J Gassmann D W Crowder Y Carrieacutere Insect resistance to Bt crops Evidence versus theory Nat Biotechnol 26 199ndash202 (2008) Medline doi101038nbt1382

79 E S Dunlop M L Baskett M Heino U Dieckmann The propensity of marine reserves to reduce the evolutionary effects of fishing in a migratory species Evol Appl 2 371ndash393 (2009) doi101111j1752-4571200900089x

80 R A Gatenby J Brown T Vincent Lessons from applied ecology Cancer control using an evolutionary double bind Cancer Res 69 7499ndash7502 (2009) Medline doi1011580008-5472CAN-09-1354

81 A S Silva R A Gatenby A theoretical quantitative model for evolution of cancer chemotherapy resistance Biol Direct 5 25 (2010) Medline doi1011861745-6150-5-25

82 R J Gillies D Verduzco R A Gatenby Evolutionary dynamics of carcinogenesis and why targeted therapy does not work Nat Rev Cancer 12 487ndash493 (2012) Medline doi101038nrc3298

83 M Greaves C C Maley Clonal evolution in cancer Nature 481 306ndash313 (2012) Medline doi101038nature10762

84 D B Longley P G Johnston Molecular mechanisms of drug resistance J Pathol 205 275ndash292 (2005) Medline doi101002path1706

85 R A Gatenby A change of strategy in the war on cancer Nature 459 508ndash509 (2009) Medline doi101038459508a

86 V Almendro Y K Cheng A Randles S Itzkovitz A Marusyk E Ametller X Gonzalez-Farre M Muntildeoz H G Russnes A Helland I H Rye A L Borresen-Dale R Maruyama A van Oudenaarden M Dowsett R L Jones J Reis-Filho P Gascon M Goumlnen F Michor K Polyak Inference of tumor evolution during chemotherapy by computational modeling and in situ analysis of genetic and phenotypic cellular diversity Cell Reports 6 514ndash527 (2014) Medline doi101016jcelrep201312041

87 J-B Michel P J Yeh R Chait R C Moellering Jr R Kishony Drug interactions modulate the potential for evolution of resistance Proc Natl Acad Sci USA 105 14918ndash14923 (2008) Medline doi101073pnas0800944105

88 REX Consortium Heterogeneity of selection and the evolution of resistance Trends Ecol Evol 28 110ndash118 (2013) Medline doi101016jtree201209001

89 J J Cunningham R A Gatenby J S Brown Evolutionary dynamics in cancer therapy Mol Pharm 8 2094ndash2100 (2011) Medline doi101021mp2002279

90 R M Gulick Antiretroviral treatment 2010 Progress and controversies J Acquir Immune Defic Syndr 55 (suppl 1) S43ndashS48 (2010) Medline doi101097QAI0b013e3181f9c09e

91 R K Gupta D A Van de Vijver S Manicklal M A Wainberg Evolving uses of oral reverse transcriptase inhibitors in the HIV-1 epidemic From treatment to prevention Retrovirology 10 82 (2013) Medline doi1011861742-4690-10-82

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92 H Brun A M Chegravevre B D Fitt S Powers A L Besnard M Ermel V Huteau B Marquer F Eber M Renard D Andrivon Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus New Phytol 185 285ndash299 (2010) Medline doi101111j1469-8137200903049x

93 B E Tabashnik Managing resistance with multiple pesticide tactics Theory evidence and recommendations J Econ Entomol 82 1263ndash1269 (1989) Medline

94 C T Bergstrom M Lo M Lipsitch Ecological theory suggests that antimicrobial cycling will not reduce antimicrobial resistance in hospitals Proc Natl Acad Sci USA 101 13285ndash13290 (2004) Medline doi101073pnas0402298101

95 J P Torella R Chait R Kishony Optimal drug synergy in antimicrobial treatments PLOS Comput Biol 6 e1000796 (2010) Medline doi101371journalpcbi1000796

96 B Jacquemin J Gasquez X Reboud Modelling binary mixtures of herbicides in populations resistant to one of the components Evaluation for resistance management Pest Manag Sci 65 113ndash121 (2009) Medline doi101002ps1647

97 R T Roush Twondashtoxin strategies for management of insecticidal transgenic crops Can pyramiding succeed where pesticide mixtures have not Philos Trans R Soc Lond B Biol Sci 353 1777ndash1786 (1998) doi101098rstb19980330

98 J-Z Zhao J Cao H L Collins S L Bates R T Roush E D Earle A M Shelton Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants Proc Natl Acad Sci USA 102 8426ndash8430 (2005) Medline doi101073pnas0409324102

99 A M Shelton et al Resistance to insect pathogens and strategies to manage resistance an update in Field Manual of Techniques in Invertebrate Pathology (Springer Amsterdam 2007)

100 J H Pedlar et al Placing forestry in the assisted migration debate Bioscience 62 835ndash842 (2012) doi101525bio201262910

101 L K Gray T Gylander M S Mbogga P-Y Chen A Hamann Assisted migration to address climate change Recommendations for aspen reforestation in western Canada Ecol Appl 21 1591ndash1603 (2011) Medline doi10189010-10541

102 K M Potter W W Hargrove Determining suitable locations for seed transfer under climate change A global quantitative method New For 43 581ndash599 (2012) doi101007s11056-012-9322-z

103 S Godefroid C Piazza G Rossi S Buord A-D Stevens R Aguraiuja C Cowell C W Weekley G Vogg J M Iriondo I Johnson B Dixon D Gordon S Magnanon B Valentin K Bjureke R Koopman M Vicens M Virevaire T Vanderborght How successful are plant species reintroductions Biol Conserv 144 672ndash682 (2011) doi101016jbiocon201010003

104 L M Broadhurst et al Seed supply for broadscale restoration Maximizing evolutionary potential Evol Appl 1 587ndash597 (2008)

105 A R Weeks C M Sgro A G Young R Frankham N J Mitchell K A Miller M Byrne D J Coates M D Eldridge P Sunnucks M F Breed E A James A A

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Hoffmann Assessing the benefits and risks of translocations in changing environments A genetic perspective Evol Appl 4 709ndash725 (2011) Medline doi101111j1752-4571201100192x

106 M Byrne L Stone M A Millar Assessing genetic risk in revegetation J Appl Ecol 48 1365ndash1373 (2011) doi101111j1365-2664201102045x

107 K Vander Mijnsbrugge A Bischoff B Smith A question of origin Where and how to collect seed for ecological restoration Basic Appl Ecol 11 300ndash311 (2010) doi101016jbaae200909002

108 S Godefroid T Vanderborght Plant reintroductions The need for a global database Biodivers Conserv 20 3683ndash3688 (2011) doi101007s10531-011-0120-2

109 D J Merritt K W Dixon Conservation Restoration seed banksmdasha matter of scale Science 332 424ndash425 (2011) Medline doi101126science1203083

110 AdapTRee website httpadaptreesitesoltubcca

111 J A Hicke J C Jenkins Mapping lodgepole pine stand structure susceptibility to mountain pine beetle attack across the western United States For Ecol Manage 255 1536ndash1547 (2008) doi101016jforeco200711027

112 C Moritz Conservation units and translocations Strategies for conserving evolutionary processes Hereditas 130 217ndash228 (1999) doi101111j1601-5223199900217x

113 C M Donald The breeding of crop ideotypes Euphytica 17 385ndash403 (1968) doi101007BF00056241

114 A Gardner A Grafen Capturing the superorganism A formal theory of group adaptation J Evol Biol 22 659ndash671 (2009) Medline doi101111j1420-9101200801681x

115 A Kumar N C Turner D P Singh P Singh M Barr Diurnal and seasonal patterns of water potential photosynthesis evapotranspiration and water use efficiency of clusterbean Photosynthetica 37 601ndash607 (2000) doi101023A1007127726207

116 P R Jennings Plant type as a rice breeding objective Crop Sci 4 13ndash15 (1964) doi102135cropsci19640011183X000400010005x

117 W G Duncan W A Williams R S Loomis Tassels and productivity of maize Crop Sci 7 37ndash39 (1967) doi102135cropsci19670011183X000700010013x

118 D N Duvick K G Cassman Post-green-revolution trends in yield potential of temperate maize in the north-central United States Crop Sci 39 1622ndash1630 (1999) doi102135cropsci19993961622x

119 J Weiner S B Andersen W K M Wille H W Griepentrog J M Olsen Evolutionary Agroecology The potential for cooperative high density weed-suppressing cereals Evol Appl 3 473ndash479 (2010) doi101111j1752-4571201000144x

120 M J Wade P Bijma E D Ellen W Muir Group selection and social evolution in domesticated animals Evol Applic 3 453ndash465 (2010) doi101111j1752-4571201000147x

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121 J Liu T Dietz S R Carpenter C Folke M Alberti C L Redman S H Schneider E Ostrom A N Pell J Lubchenco W W Taylor Z Ouyang P Deadman T Kratz W Provencher Coupled human and natural systems Ambio 36 639ndash649 (2007) Medline doi1015790044-7447(2007)36[639CHANS]20CO2

122 P Rabinowitz L Conti Links among human health animal health and ecosystem health Annu Rev Public Health 34 189ndash204 (2013) Medline doi101146annurev-publhealth-031912-114426

123 M E J Woolhouse S Gowtage-Sequeria Host range and emerging and reemerging pathogens Emerg Infect Dis 11 1842ndash1847 (2005) Medline doi103201eid1112050997

124 B Olsen V J Munster A Wallensten J Waldenstroumlm A D Osterhaus R A Fouchier Global patterns of influenza a virus in wild birds Science 312 384ndash388 (2006) Medline doi101126science1122438

125 G J D Smith D Vijaykrishna J Bahl S J Lycett M Worobey O G Pybus S K Ma C L Cheung J Raghwani S Bhatt J S Peiris Y Guan A Rambaut Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic Nature 459 1122ndash1125 (2009) Medline doi101038nature08182

126 K E Jones N G Patel M A Levy A Storeygard D Balk J L Gittleman P Daszak Global trends in emerging infectious diseases Nature 451 990ndash993 (2008) Medline doi101038nature06536

127 W Ma R E Kahn J A Richt The pig as a mixing vessel for influenza viruses Human and veterinary implications J Molec Genet Med 3 158ndash166 (2008) Medline

128 H M Yassine C W Lee Y M Saif Interspecies transmission of influenza a viruses between swine and poultry Curr Top Microbiol Immunol 370 227ndash240 (2013) Medline doi10100782_2011_180

129 S Altizer R Bartel B A Han Animal migration and infectious disease risk Science 331 296ndash302 (2011) Medline doi101126science1194694

130 K R Riacuteos-Soto B Song C Castillo-Chavez Epidemic spread of influenza viruses The impact of transient populations on disease dynamics Math Biosci Eng 8 199ndash222 (2011) Medline doi103934mbe20118199

131 K M Pepin S Lass J R Pulliam A F Read J O Lloyd-Smith Identifying genetic markers of adaptation for surveillance of viral host jumps Nat Rev Microbiol 8 802ndash813 (2010) Medline doi101038nrmicro2440

132 European Center for Disease Prevention and Control and European Medicines Agency The Bacterial Challenge Time to React (ECDCEMEA Joint Technical Report EMEA5761762009 Stockholm 2009)

133 Alliance for the Prudent Use of Antibiotics The Cost of Antibiotic Resistance to US Families and the Healthcare System (APUA Boston MA 2010)

134 M A Cooper D Shlaes Fix the antibiotics pipeline Nature 472 32ndash32 (2011) Medline doi101038472032a

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135 M S Butler M A Blaskovich M A Cooper Antibiotics in the clinical pipeline in 2013 J Antibiot (Tokyo) 66 571ndash591 (2013) Medline doi101038ja201386

136 A M Bal I M Gould Antibiotic stewardship Overcoming implementation barriers Curr Opin Infect Dis 24 357ndash362 (2011) Medline doi101097QCO0b013e3283483262

137 C MacDougall R E Polk Antimicrobial stewardship programs in health care systems Clin Microbiol Rev 18 638ndash656 (2005) Medline doi101128CMR184638-6562005

138 US Food and Drug Administration 2009 Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals (FDA Washington DC 2010)

139 E K Silbergeld J Graham L B Price Industrial food animal production antimicrobial resistance and human health Annu Rev Public Health 29 151ndash169 (2008) Medline doi101146annurevpublhealth29020907090904

140 M E J Woolhouse M J W Ward Microbiology Sources of antimicrobial resistance Science 341 1460ndash1461 (2013) 101126science1243444 Medline doi101126science1243444

141 A R Manges J R Johnson Food-borne origins of Escherichia coli causing extraintestinal infections Clin Infect Dis 55 712ndash719 (2012) Medline doi101093cidcis502

142 J L Martinez J Olivares in Antimicrobial Resistance in the Environment P L Keen M H M M Montforts (Wiley-Blackwell 2011) chap 9 pp 157ndash172

143 Transatlantic Taskforce on Antimicrobial Resistance Recommendations for future collaboration between the US and EU (TATFAR Report 2011) httpwwwecdceuropaeuenactivitiesdiseaseprogrammesTATFARDocuments210911_TATFAR_Reportpdf

144 European Commission Communication from the Commission to the European Parliament and the Council Action plan against the rising threats from Antibmicrobial Resistance COM 748 (2011) httpeceuropaeudgshealth_consumerdocscommunication_amr_2011_748_enpdf

145 FDA New animal drugs cephalosporin drugs extralabel animal drug use order of prohibition Fed Regist 77 735 (2012) httpfederalregistergova2012-35

146 S P Carroll M T Kinnison L Bernatchez In light of evolution Interdisciplinary challenges in food health and the environment Evol Appl 4 155ndash158 (2011) doi101111j1752-4571201100182x

147 D Griggs M Stafford-Smith O Gaffney J Rockstroumlm M C Ohman P Shyamsundar W Steffen G Glaser N Kanie I Noble Policy Sustainable development goals for people and planet Nature 495 305ndash307 (2013) Medline doi101038495305a

148 Convention of Biological Diversity Aichi Biodiversity Targets Strategic Plan for Biodiversity 2011-2020 (2010) wwwcbdintsptargets

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149 C Joslashrgensen K Enberg E S Dunlop R Arlinghaus D S Boukal K Brander B Ernande A Gardmark F Johnston S Matsumura H Pardoe K Raab A Silva A Vainikka U Dieckmann M Heino A D Rijnsdorp Ecology Managing evolving fish stocks Science 318 1247ndash1248 (2007) Medline doi101126science1148089

150 A T Laugen et al Evolutionary impact assessment Accounting for evolutionary consequences of fishing in an ecosystem approach to fisheries management Fish Fish 15 1ndash32 (2012)

151 M L Baskett R S Waples Evaluating alternative strategies for minimizing unintended fitness consequences of cultured individuals on wild populations Conserv Biol 27 83ndash94 (2013) Medline doi101111j1523-1739201201949x

152 Convention on Biological Diversity The Nagoya Protocol on Access and Benefit-Sharing (2013) wwwcbdintabs

153 L Santamariacutea P F Meacutendez Evolution in biodiversity policy - current gaps and future needs Evol Appl 5 202ndash218 (2012) doi101111j1752-4571201100229x

154 E W Welch Potential implications of the Nagoya Protocol for the livestock sector J Anim Breed Genet 129 423ndash424 (2012) Medline

155 J A Jackson L Laikre C S Baker K C Kendall Guidelines for collecting and maintaining archives for genetic monitoring Conserv Genet Resour 4 527ndash536 (2011) doi101007s12686-011-9545-x

156 G V Dana T Kuiken D Rejeski A A Snow Synthetic biology Four steps to avoid a synthetic-biology disaster Nature 483 29ndash29 (2012) Medline doi101038483029a

157 A A Snow V H Smith Genetically engineered algae for biofuels A key role for ecologists Bioscience 62 765ndash768 (2012) doi101525bio20126289

158 P Mali L Yang K M Esvelt J Aach M Guell J E DiCarlo J E Norville G M Church RNA-guided human genome engineering via Cas9 Science 339 823ndash826 (2013) Medline doi101126science1232033

159 M A Thomas G W Roemer C J Donlan B G Dickson M Matocq J Malaney Ecology Gene tweaking for conservation Nature 501 485ndash486 (2013) Medline doi101038501485a

160 K H Redford W Adams G M Mace Synthetic biology and conservation of nature Wicked problems and wicked solutions PLOS Biol 11 e1001530 (2013) Medline doi101371journalpbio1001530

161 B M Althouse T C Bergstrom C T Bergstrom Evolution in health and medicine Sackler colloquium A public choice framework for controlling transmissible and evolving diseases Proc Natl Acad Sci USA 107 (suppl 1) 1696ndash1701 (2010) Medline doi101073pnas0906078107

162 J Liu T Dietz S R Carpenter M Alberti C Folke E Moran A N Pell P Deadman T Kratz J Lubchenco E Ostrom Z Ouyang W Provencher C L Redman S H Schneider W W Taylor Complexity of coupled human and natural systems Science 317 1513ndash1516 (2007) Medline doi101126science1144004

Carroll et al 20

163 E Ostrom A general framework for analyzing sustainability of social-ecological systems Science 325 419ndash422 (2009) Medline doi101126science1172133

164 E Ostrom A diagnostic approach for going beyond panaceas Proc Natl Acad Sci USA 104 15181ndash15187 (2007) Medline doi101073pnas0702288104

165 G Hardin The tragedy of the commons The population problem has no technical solution it requires a fundamental extension in morality Science 162 1243ndash1248 (1968) Medline

166 F Baquero J Campos The tragedy of the commons in antimicrobial chemotherapy Rev Esp Quimioter 16 11ndash13 (2003) [Editorial] Medline

167 W D Hutchison E C Burkness P D Mitchell R D Moon T W Leslie S J Fleischer M Abrahamson K L Hamilton K L Steffey M E Gray R L Hellmich L V Kaster T E Hunt R J Wright K Pecinovsky T L Rabaey B R Flood E S Raun Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers Science 330 222ndash225 (2010) Medline doi101126science1190242

168 G Jaffe Complacency on the farm significant noncompliance with EPAs refuge requirements threatens the future effectiveness of genetically engineered pest-protected corn (Center for Science in the Public Interest Washington DC 2009)

169 P A Samuelson The pure theory of public expenditure Rev Econ Stat 36 387ndash389 (1954) doi1023071925895

170 D J Nokes R M Anderson Vaccine safety versus vaccine efficacy in mass immunisation programmes Lancet 338 1309ndash1312 (1991) Medline doi1010160140-6736(91)92601-W

171 K Kaier U Frank Measuring the externality of antibacterial use from promoting antimicrobial resistance Pharmacoeconomics 28 1123ndash1128 (2010) Medline doi10216511535640-000000000-00000

172 K Kaier Economic modeling of the persistence of antimicrobial resistance Nat Resour Model 25 388ndash402 (2012) doi101111j1939-7445201100114x

173 G D Wright Antibiotic resistance in the environment A link to the clinic Curr Opin Microbiol 13 589ndash594 (2010) Medline doi101016jmib201008005

174 M Herrmann R Laxminarayan Antibiotic Effectiveness New Challenges in Natural Resource Management Annu Rev Resource Econom 2 125ndash138 (2010) doi101146annurevresource050708144125

175 C N Cook M B Mascia M W Schwartz H P Possingham R A Fuller Achieving conservation science that bridges the knowledge-action boundary Conserv Biol 27 669ndash678 (2013) Medline doi101111cobi12050

176 J Antonovics J L Abbate C H Baker D Daley M E Hood C E Jenkins L J Johnson J J Murray V Panjeti V H Rudolf D Sloan J Vondrasek Evolution by any other name Antibiotic resistance and avoidance of the E-word PLOS Biol 5 e30 (2007) Medline doi101371journalpbio0050030

Carroll et al 21

177 A M Messenger A N Barnes G C Gray Reverse zoonotic disease transmission (zooanthroponosis) A systematic review of seldom-documented human biological threats to animals PLOS ONE 9 e89055 (2014) Medline doi101371journalpone0089055

178 R Salguero-Gomez ComPADRe III demographic database wwwdemogrmpgdeenlaboratoriesevolutionary_biodemography_1171projectscompadre_plant_matrix_database_comadre_animal_matrix_database_1867htm

179 K Todar The Growth of Bacterial Populations Textbook of Bacteriology httptextbookofbacteriologynetgrowth_3html

180 A G Rodrigo E G Shpaer E L Delwart A K Iversen M V Gallo J Brojatsch M S Hirsch B D Walker J I Mullins Coalescent estimates of HIV-1 generation time in vivo Proc Natl Acad Sci USA 96 2187ndash2191 (1999) Medline doi101073pnas9652187

181 N R Boyle J A Morgan Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii BMC Syst Biol 3 4 (2009) Medline doi1011861752-0509-3-4

182 K Goulding M Merrett The photometabolism of acetate by Chlorella pyrenoidosa J Exp Bot 17 678ndash689 (1966) doi101093jxb174678

183 R W Truman J L Krahenbuhl Viable M leprae as a research reagent Int J Lepr Other Mycobact Dis 69 1ndash12 (2001) Medline

184 M P Zwart J A Darograves S F Elena One is enough In vivo effective population size is dose-dependent for a plant RNA virus PLOS Pathog 7 e1002122 (2011) Medline doi101371journalppat1002122

185 S Y Lee J Bollinger D Bezdicek A Ogram Estimation of the abundance of an uncultured soil bacterial strain by a competitive quantitative PCR method Appl Environ Microbiol 62 3787ndash3793 (1996) Medline

186 H Danks Short life cycles in insects and mites Can Entomol 138 407ndash463 (2006) doi104039n06-803

187 G E Cartwright J W Athens M M Wintrobe The kinetics of granulopoiesis in normal man Blood 24 780ndash803 (1964) Medline

188 E Marshman C Booth C S Potten The intestinal epithelial stem cell BioEssays 24 91ndash98 (2002) Medline doi101002bies10028

189 R Flindt Biologie in Zahlen (Elsevier Spektrum Akademischer Verlag Heidelberg ed 6 2003)

190 K L Spalding E Arner P O Westermark S Bernard B A Buchholz O Bergmann L Blomqvist J Hoffstedt E Naumlslund T Britton H Concha M Hassan M Rydeacuten J Friseacuten P Arner Dynamics of fat cell turnover in humans Nature 453 783ndash787 (2008) Medline doi101038nature06902

191 R D Bhardwaj M A Curtis K L Spalding B A Buchholz D Fink T Bjoumlrk-Eriksson C Nordborg F H Gage H Druid P S Eriksson J Friseacuten Neocortical

Carroll et al 22

neurogenesis in humans is restricted to development Proc Natl Acad Sci USA 103 12564ndash12568 (2006) Medline doi101073pnas0605177103

192 F A C Azevedo L R B Carvalho L T Grinberg J M Farfel R E L Ferretti R E Leite W J Filho R Lent S Herculano-Houzel Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain J Comp Neurol 513 532ndash541 (2009) Medline doi101002cne21974

193 J N Fenner Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies Am J Phys Anthropol 128 415ndash423 (2005) Medline doi101002ajpa20188

194 Department of Economic and Social Affairs Population Division United Nations World Population Prospects The 2010 Revision (United Nations New York 2011) httpesaunorgunpdwpp

195 M B Usher A matrix approach to the management of renewable resources with special reference to selection forests J Appl Ecol 3 355ndash367 (1966) doi1023072401258

196 M Usher A matrix model for forest management Biometrics 25 309ndash315 (1969) doi1023072528791

197 S Southerton personal communication 29 April 2014

198 R G Wear S J Haslett N L Alexander Effects of temperature and salinity on the biology of Artemia fransiscana Kellogg from Lake Grassmere New Zealand 2 Maturation fecundity and generation times J Exp Mar Biol Ecol 98 167ndash183 (1986) doi1010160022-0981(86)90081-X

199 M L Winston The Biology of the Honey Bee (Harvard Univ Press Cambridge MA 1991)

200 A P Martin S R Palumbi Body size metabolic rate generation time and the molecular clock Proc Natl Acad Sci USA 90 4087ndash4091 (1993) Medline doi101073pnas9094087

201 P J Van Mantgem N L Stephenson The accuracy of matrix population model projections for coniferous trees in the Sierra Nevada California J Ecol 93 737ndash747 (2005) doi101111j1365-2745200501007x

202 K McPherson K Williams Establishment growth of cabbage palm Sabal palmetto (Arecaceae) Am J Bot 83 1566ndash1570 (1996) doi1023072445830

203 Aacute Ferrero-Serrano A L Hild B A Mealor Can invasive species enhance competitive ability and restoration potential in native grass populations Restor Ecol 19 545ndash551 (2011) doi101111j1526-100X200900611x

204 M L Baskett S A Levin S D Gaines J Dushoff Marine reserve design and the evolution of size at maturation in harvested fish Ecol Appl 15 882ndash901 (2005) doi10189004-0723

205 D R Shaw M D Owen P M Dixon S C Weller B G Young R G Wilson D L Jordan Benchmark study on glyphosate-resistant cropping systems in the United

Carroll et al 23

States Part 1 Introduction to 2006-2008 Pest Manag Sci 67 741ndash746 (2011) Medline doi101002ps2160

206 A L Melander Can insects become resistant to sprays J Econ Entomol 7 167ndash173 (1914)

207 M S Niederman Is ldquocrop rotationrdquo of antibiotics the solution to a ldquoresistantrdquo problem in the ICU Am J Respir Crit Care Med 156 1029ndash1031 (1997) Medline doi101164ajrccm1564ed-14

208 R E Rapp A Datta S Irmak T J Arkebauer S Z Knezevic Integrated management of common reed (Phragmites australis) along the Platte River in Nebraska Weed Technol 26 326ndash333 (2012) doi101614WT-D-11-001191

209 D M Bergstrom A Lucieer K Kiefer J Wasley L Belbin T K Pedersen S L Chown Indirect effects of invasive species removal devastate World Heritage Island J Appl Ecol 46 73ndash81 (2009) doi101111j1365-2664200801601x

210 R Van Den Bosch V M Stern The integration of chemical and biological control of arthropod pests Annu Rev Entomol 7 367ndash386 (1962) Medline doi101146annureven07010162002055

211 P Csermely V Aacutegoston S Pongor The efficiency of multi-target drugs The network approach might help drug design Trends Pharmacol Sci 26 178ndash182 (2005) Medline doi101016jtips200502007

212 M J Mackinnon S Gandon A F Read Virulence evolution in response to vaccination The case of malaria Vaccine 26 (suppl 3) C42ndashC52 (2008) Medline doi101016jvaccine200804012

213 K A Hanley L R Manlucu L E Gilmore J E Blaney Jr C T Hanson B R Murphy S S Whitehead A trade-off in replication in mosquito versus mammalian systems conferred by a point mutation in the NS4B protein of dengue virus type 4 Virology 312 222ndash232 (2003) Medline doi101016S0042-6822(03)00197-1

214 S Lavergne J Molofsky Control strategies for the invasive reed Canarygrass (Phalaris arundinacea L) in North American Wetlands The need for an Integrated Management Plan Nat Areas J 26 208ndash214 (2006) doi1033750885-8608(2006)26[208CSFTIR]20CO2

215 C A Schoner R F Norris W Chilcote Yellow foxtail (Setaria lutescens) biotype studies Growth and morphological characteristics Weed Sci 26 632ndash636 (1978)

216 M F Schetelig F Scolari A M Handler S Kittelmann G Gasperi E A Wimmer Site-specific recombination for the modification of transgenic strains of the Mediterranean fruit fly Ceratitis capitata Proc Natl Acad Sci USA 106 18171ndash18176 (2009) Medline doi101073pnas0907264106

217 S Crotty D Maag J J Arnold W Zhong J Y N Lau Z Hong R Andino C E Cameron The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen Nat Med 6 1375ndash1379 (2000) Medline doi10103882191

218 M Eigen Error catastrophe and antiviral strategy Proc Natl Acad Sci USA 99 13374ndash13376 (2002) Medline doi101073pnas212514799

Carroll et al 24

219 M R Wise de Valdez D Nimmo J Betz H F Gong A A James L Alphey W C Black 4th Genetic elimination of dengue vector mosquitoes Proc Natl Acad Sci USA 108 4772ndash4775 (2011) Medline doi101073pnas1019295108

220 D Bardsley G Hugo Migration and climate change Examining thresholds of change to guide effective adaptation decision-making Popul Environ 32 238ndash262 (2010) doi101007s11111-010-0126-9

221 T Jacobsen R M Adams Salt and Silt in Ancient Mesopotamian Agriculture Progressive changes in soil salinity and sedimentation contributed to the breakup of past civilizations Science 128 1251ndash1258 (1958) Medline doi101126science12833341251

222 J Berger S P Milroy N C Turner K H M Siddique M Imtiaz R Malhotra Chickpea evolution has selected for contrasting phenological mechanisms among different habitats Euphytica 180 1ndash15 (2011) doi101007s10681-011-0391-4

223 P Carrera-Bastos The western diet and lifestyle and diseases of civilization Res Rep Clinic Cardiol 2 15ndash35 (2011)

224 L B Turner A meta-analysis of fat intake reproduction and breast cancer risk An evolutionary perspective Am J Hum Biol 23 601ndash608 (2011) Medline doi101002ajhb21176

225 P D Gluckman M A Hanson F M Low The role of developmental plasticity and epigenetics in human health Birth Defects Res C Embryo Today 93 12ndash18 (2011) Medline doi101002bdrc20198

226 K R Rice N C Emery Managing microevolution Restoration in the face of global change Front Ecol Environ 1 469ndash478 (2003) doi1018901540-9295(2003)001[0469MMRITF]20CO2

227 C M Sgrograve A J Lowe A A Hoffmann Building evolutionary resilience for conserving biodiversity under climate change Evol Appl 4 326ndash337 (2011) doi101111j1752-4571201000157x

228 N Redpath L M Osgathorpe K Park D Goulson Crofting and bumblebee conservation The impact of land management practices on bumblebee populations in northwest Scotland Biol Conserv 143 492ndash500 (2010) doi101016jbiocon200911019

229 A Jarvis A Lane R J Hijmans The effect of climate change on crop wild relatives Agric Ecosyst Environ 126 13ndash23 (2008) doi101016jagee200801013

230 R M Trethowan M A Turner T M Chattha Breeding strategies to adapt crops to a changing climate in Climate Change and Food Security D Lobell M Burke Eds (Springer Netherlands 2010) pp 155ndash174

231 L C Dupuy C P Locher M Paidhungat M J Richards C M Lind R Bakken M D Parker R G Whalen C S Schmaljohn Directed molecular evolution improves the immunogenicity and protective efficacy of a Venezuelan equine encephalitis virus DNA vaccine Vaccine 27 4152ndash4160 (2009) Medline doi101016jvaccine200904049

Carroll et al 25

232 T A Yap C P Carden S B Kaye Beyond chemotherapy Targeted therapies in ovarian cancer Nat Rev Cancer 9 167ndash181 (2009) Medline doi101038nrc2583

233 H Cho T Daniel Y J Buechler D C Litzinger Z Maio A-M H Putnam V S Kraynov B C Sim S Bussell T Javahishvili S Kaphle G Viramontes M Ong S Chu G C Becky R Lieu N Knudsen P Castiglioni T C Norman D W Axelrod A R Hoffman P G Schultz R D DiMarchi B E Kimmel Optimized clinical performance of growth hormone with an expanded genetic code Proc Natl Acad Sci USA 108 9060ndash9065 (2011) Medline doi101073pnas1100387108

234 M A Bartel J R Weinstein D V Schaffer Directed evolution of novel adeno-associated viruses for therapeutic gene delivery Gene Ther 19 694ndash700 (2012) Medline doi101038gt201220

235 M D Venesky J R Mendelson III B F Sears P Stiling J R Rohr Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation Conserv Biol 26 586ndash592 (2012) Medline doi101111j1523-1739201201854x

236 S Lopez F Rousset F H Shaw R G Shaw O Ronce Joint effects of inbreeding and local adaptation on the evolution of genetic load after fragmentation Conserv Biol 23 1618ndash1627 (2009) Medline doi101111j1523-1739200901326x

237 E B Davis M S Koo C Conroy J L Patton C Moritz The California Hotspots Project Identifying regions of rapid diversification of mammals Mol Ecol 17 120ndash138 (2008) Medline doi101111j1365-294X200703469x

238 L Hannah A global conservation system for climate-change adaptation Conserv Biol 24 70ndash77 (2010) Medline doi101111j1523-1739200901405x

239 D F Jacobs Toward development of silvical strategies for forest restoration of American chestnut (Castanea dentata) using blight-resistant hybrids Biol Conserv 137 497ndash506 (2007) doi101016jbiocon200703013

240 W M Muir Group selection for adaptation to multiple-hen cages Selection program and direct responses Poult Sci 75 447ndash458 (1996) Medline doi103382ps0750447

241 R F Denison E T Kiers S A West Darwinian agriculture When can humans find solutions beyond the reach of natural selection Q Rev Biol 78 145ndash168 (2003) Medline doi101086374951

242 A G Condon R A Richards G J Rebetzke G D Farquhar Breeding for high water-use efficiency J Exp Bot 55 2447ndash2460 (2004) Medline doi101093jxberh277

243 S P Carroll J V Watters Managing phenotypic variability with genetic and environmental heterogeneity adaptation as a first principle of conservation practice In Conservation BiologymdashEvolution in Action S P Carroll C W Fox Eds (Oxford Univ Press Oxford 2008) pp 181ndash198

RESEARCH

17 OCTOBER 2014 bull VOL 346 ISSUE 6207 313SCIENCE sciencemagorg

BACKGROUND Differences among species

in their ability to adapt to environmental

change threaten biodiversity human health

food security and natural resource avail-

ability Pathogens pests and cancers often

quickly evolve resistance to control measures

whereas crops livestock wild species and

human beings often do not adapt

fast enough to cope with

climate change habi-

tat loss toxicants

and lifestyle

change To

addre s s


APPLIED EVOLUTION

Scott P Carroll Peter Soslashgaard Joslashrgensen Michael T Kinnison Carl T Bergstrom

R Ford Denison Peter Gluckman Thomas B Smith Sharon Y Strauss Bruce E Tabashnik

Tactics and tools of applied evolutionary biology (Top) Evolutionary tactics to address the

major societal challenges treated in the present study are shown as a wheel Challenges in the

food health and environment sectors are caused by rapid contemporary evolution or in more

slowly reproducing or threatened species phenotype-environment mismatch Gene f ow and

selection agents make challenges in one sector dependent on actions in others Current prog-

ress in implementing tactics of applied evolutionary biology to address challenges varies widely

(Bottom) Many of these tactics use a common toolbox of strategies to prevent unwanted evo-

lution or to reduce f tness in harmful organisms as well as to reduce mismatch between organ-

isms and human-altered environments or to increase group performance in desired organisms

Each of these strategies uses a combination of manipulations of the organismal genotype phe-

notypic plasticity (development) or environmental conditions

REVIEW SUMMARY

these challenges practices based on evolu-

tionary biology can promote sustainable out-

comes via strategic manipulation of genetic

developmental and environmental factors

Successful strategies effectively slow un-

wanted evolution and reduce fitness in costly

species or improve performance of valued

organisms by reducing phenotype-

environment mismatch or

increasing group pro-

ductivity Tactics

of applied

evolution-

ary bi-

ology range broadly from common policies

that promote public health or preserve habi-

tat for threatened speciesmdashbut are easily over-

looked as having an evolutionary rationale to

the engineering of new genomes

ADVANCES The scope and development

of current tactics vary widely In particular

genetic engineering attracts much attention

(and controversy) but now is used mainly

for traits under simple

genetic control Human

gene therapy which

mainly involves more

complex controls has

yet to be applied suc-

cessfully at large scales

In contrast other methods to alter complex

traits are improving These include artificial

selection for drought- and flood-tolerant

crops through bioinformatics and applica-

tion of ldquolife courserdquo approaches in medicine

to reduce human metabolic disorders

Successful control of unwanted evolution

depends on governance initiatives that ad-

dress challenges arising from both natural

and social factors Principal among these

challenges are (i) global transfer of genes

and selection agents (ii) interlinked evo-

lution across traditional sectors of society

(environment food and health) and (iii)

conflicts between individual and group in-

centives that threaten regulation of anti-

biotic use and crop refuges Evolutionarily

informed practices are a newer prospect in

some fields and require more systematic re-

search as well as ethical considerationmdashfor

example in attempts to protect wild species

through assisted migration in the choice of

source populations for restoration or in ge-

netic engineering

OUTLOOK A more unified platform will

better convey the value of evolutionary meth-

ods to the public scientists and decision-

makers For researchers and practitioners

applications may be expanded to other dis-

ciplines such as in the transfer of refuge

strategies that slow resistance evolution in

agriculture to slow unwanted evolution

elsewhere (for example cancer resistance

or harvest-induced evolution) For policy-

makers adoption of practices that minimize

unwanted evolution and reduce phenotype-

environment mismatch in valued species is

likely essential to achieve the forthcoming

Sustainable Development Goals and the

2020 Aichi Biodiversity Targets

The list of author affiliations is available in the full article online

Corresponding author E-mail spcarrollucdavisedu (SPC) psjorgensenbiokudk (PSJ) Cite this Review as Scott P Carroll et al Science 346 1245993 (2014) DOI 101126science1245993

Read the full article at httpdxdoiorg101126science1245993

ON OUR WEB SITE

SECTORS

CHALLENGES

by manipulation ofControl harmful organisms

1) slow unwanted evolution

Protect desirable organisms

3) reduce phenotype- environment mismatch

4) increase group performance2) reduce ftness bull Development

bull Environment

bull Genotype

Implementation

Toolbox

Emergingdiseasesurvei

llance

Integrated pest management

Reduceinbreeding

Cross-sector antibioticreg

ulation

Cross-secto

r antibiotic regulationNatural en

closures

Cancerresistan

ce

Habitat protection

Choice of seed sources

Reducetoxicants

Captivebreeding

programs

Genome-guided breeding strateg

iesHealt

hfuldietampactivitylevel

Restorationsources amp

assisted migration

Drought amp food tolerant GMcrops

Genetherapy

Biodiversity loss

Climate extremes reduceyield

Chronic disease

ENVIRONM

ENT

FOOD

HEALTLLH

Newcancertreatments

Refuge strategies foff r GM crops

Fewer generations incaptivity

Antibioticresistan

ce

Pesticide resistance

EvolutionincaptivityH

EALTLLH

FOOD

ENV

IRONMENT

TACTICS

GE

NE

F

LOW

SELECTIO

N A

GE

NTS

Emerginginfeffctiousdis

ease

Antibiotic resistance

Published by AAAS

REVIEW

APPLIED EVOLUTION














RESEARCH













log

(p

op

ula

tio

n s

ize

)

Conservationbiology

Annual organisms






MedicineHumans

MedicineHuman

bone marrow


pathogensmutualists

commensals


CropsLivestock

Trees

All

Multicellular


Pollinators


RESEARCH | REVIEW













Phenotype

distribution

Genotype

distribution

Optimum

phenotype

range

A

B C D

Manipulation

of mismatch

Fre

qu

en

cy

Trait value

Mismatch



RESEARCH | REVIEW





B





















Reducepest fitness












Transgenicmutation


Modify genotypes






Add mutationalload

Reduce selection



Space

Mix

Time

Now Later

hybrid



RESEARCH | REVIEW














RESEARCH | REVIEW









Environment

Health

Food


resistance


RESEARCH | REVIEW


































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













REVIEW

APPLIED EVOLUTION














RESEARCH













log

(p

op

ula

tio

n s

ize

)

Conservationbiology

Annual organisms






MedicineHumans

MedicineHuman

bone marrow


pathogensmutualists

commensals


CropsLivestock

Trees

All

Multicellular


Pollinators


RESEARCH | REVIEW













Phenotype

distribution

Genotype

distribution

Optimum

phenotype

range

A

B C D

Manipulation

of mismatch

Fre

qu

en

cy

Trait value

Mismatch



RESEARCH | REVIEW





B





















Reducepest fitness












Transgenicmutation


Modify genotypes






Add mutationalload

Reduce selection



Space

Mix

Time

Now Later

hybrid



RESEARCH | REVIEW














RESEARCH | REVIEW









Environment

Health

Food


resistance


RESEARCH | REVIEW


































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25























log

(p

op

ula

tio

n s

ize

)

Conservationbiology

Annual organisms






MedicineHumans

MedicineHuman

bone marrow


pathogensmutualists

commensals


CropsLivestock

Trees

All

Multicellular


Pollinators


RESEARCH | REVIEW













Phenotype

distribution

Genotype

distribution

Optimum

phenotype

range

A

B C D

Manipulation

of mismatch

Fre

qu

en

cy

Trait value

Mismatch



RESEARCH | REVIEW





B





















Reducepest fitness












Transgenicmutation


Modify genotypes






Add mutationalload

Reduce selection



Space

Mix

Time

Now Later

hybrid



RESEARCH | REVIEW














RESEARCH | REVIEW









Environment

Health

Food


resistance


RESEARCH | REVIEW


































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25

























Phenotype

distribution

Genotype

distribution

Optimum

phenotype

range

A

B C D

Manipulation

of mismatch

Fre

qu

en

cy

Trait value

Mismatch



RESEARCH | REVIEW





B





















Reducepest fitness












Transgenicmutation


Modify genotypes






Add mutationalload

Reduce selection



Space

Mix

Time

Now Later

hybrid



RESEARCH | REVIEW














RESEARCH | REVIEW









Environment

Health

Food


resistance


RESEARCH | REVIEW


































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25

















B





















Reducepest fitness












Transgenicmutation


Modify genotypes






Add mutationalload

Reduce selection



Space

Mix

Time

Now Later

hybrid



RESEARCH | REVIEW














RESEARCH | REVIEW









Environment

Health

Food


resistance


RESEARCH | REVIEW


































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25


























RESEARCH | REVIEW









Environment

Health

Food


resistance


RESEARCH | REVIEW


































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25





















Environment

Health

Food


resistance


RESEARCH | REVIEW


































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25














































RESEARCH | REVIEW
































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25












































































RESEARCH | REVIEW









































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25





















































































RESEARCH | REVIEW




















































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25
































































ACKNOWLEDGMENTS




101126science1245993


RESEARCH | REVIEW





Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25

















Bruce E Tabashnik















Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25























Population size



Algae 11 hours (181

182)


(183)








(186) Drosophila 14

d





indicating large

minimum global

population sizes




29 days (187)



gt101011 (189)



neurons in



100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25















100 yr

brain (192)




Tree Pinus







Salmon 1-4 yr (200)

Pinus ponderosa 348


200 yr (197)





fast reproducing

insects



(200)




below 106






Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25















Slow evolution


Refuge Gene flow


form



survive (74 75)




strains






slows adaptation to

a single treatment


206)










action together


210)







(213)








genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25

















genotypes


less (215)


benign strains (28)

No cases found

Reduce adversary

fitness

Add mutational

load



viruses (216)



(219)

No cases found


Reduce phenotype-


Reduce selection in


environment

Modify environment


a suitable one







disease (225)





environments


selection





(230)








Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25














Increase group

performance

Group selection



group performance








Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 7

Supplementary Text














etjpg

Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 8

















Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 9















Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 10














Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 11














Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 12















Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 13
















Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 14















Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 15















Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 16

















Carroll et al 17















Carroll et al 18















Carroll et al 19















Carroll et al 20















Carroll et al 21
















Carroll et al 22
















Carroll et al 23















Carroll et al 24














Carroll et al 25













Carroll et al 17















Carroll et al 18















Carroll et al 19















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Applying evolutionary biology to address global challenges

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