Adaptation to climate change: contrasting patterns of thermal-reaction-norm evolution in Pacific...

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Hannes Baumann and David O Conover silversidesthermal-reaction-norm evolution in Pacific versus Atlantic Adaptation to climate change contrasting patterns of

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ReceivedAccepted

Adaptation to climate change contrastingpatterns of thermal-reaction-norm evolution

in Pacific versus Atlantic silversidesHannes Baumann and David O Conover

School of Marine and Atmospheric Sciences Stony Brook University Stony Brook NY 11794-5000 USA

How organisms may adapt to rising global temperatures is uncertain but concepts can emerge from

studying adaptive physiological trait variations across existing spatial climate gradients Many ectotherms

particularly fish have evolved increasing genetic growth capacities with latitude (ie countergradient vari-

ation (CnGV) in growth) which are thought to be an adaptation primarily to strong gradients in

seasonality In contrast evolutionary responses to gradients in mean temperature are often assumed to

involve an alternative mode lsquothermal adaptationrsquo We measured thermal growth reaction norms in Pacific

silverside populations (Atherinops affinis) occurring across a weak latitudinal temperature gradient with

invariant seasonality along the North American Pacific coast Instead of thermal adaptation we found

novel evidence for CnGV in growth suggesting that CnGV is a ubiquitous mode of reaction-norm evolution

in ectotherms even in response to weak spatial and by inference temporal climate gradients A novel large-

scale comparison between ecologically equivalent Pacific versus Atlantic silversides (Menidia menidia)

revealed how closely growth CnGV patterns reflect their respective climate gradients While steep growth

reaction norms and increasing growth plasticity with latitude in M menidia mimicked the strong highly

seasonal Atlantic coastal gradient shallow reaction norms and much smaller latitude-independent growth

plasticity in A affinis resembled the weak Pacific latitudinal temperature gradient

Keywords countergradient variation growth capacity conversion efficiency latitudinal gradients

temperature seasonality

1 INTRODUCTIONThe need to understand how organisms adapt to climatic

variability has increased with the evidence for unprece-

dented global climate change [1] Because temperature

greatly influences the expression and fitness of many

phenotypic traits adaptive landscapes will be altered

substantially by long-term changes in mean temperature

and seasonality [2] Anticipating evolutionary responses

to climate change remains a complex challenge Retro-

spective analyses or other temporal approaches are often

inconclusive owing to a lack of replication and difficulties

in distinguishing genetic from plastic responses [34]

An alternative is to study adaptations to climate change

across spatial scales among extant populations Many

species occur across temperature and seasonality clines

along latitudinal altitudinal depth or continentality gra-

dients and exhibit apparent adaptive variations in

morphological and physiological traits [5] Spatial climate

gradients provide opportunities to rigorously identify

mechanisms of adaptation that by analogy may elucidate

evolutionary responses to temporal climate change

One form of spatial adaptation that has gained strong

empirical support across taxa is countergradient variation

(CnGV reviewed by [6]) CnGV occurs when genotypes

with a higher (or lower) value for a given trait are predo-

minantly found in environments that tend to decrease

(or increase) the traitrsquos phenotypic value (figure 1) The

r for correspondence (hannesbaumannstonybrookedu)

ic supplementary material is available at httpdxdoiorgrspb20102479 or via httprspbroyalsocietypublishingorg

12 November 20107 December 2010 1

most common form of CnGV involves metabolic com-

pensation and is displayed mostly in physiological traits

for example in the genetically higher growth capacities

of many poikilotherms at high versus low latitudes

(eg [7] (Reptilia) [8] (Pisces) [9] (Insecta) [10]

(Gastropoda) [11] (Amphibia)) In cases of CnGV in

growth genetic growth capacities are adjusted upward

or downward over a speciesrsquo entire viable temperature

range with thermal reaction norms (frac14temperature-

specific phenotypic trait expressions figure 1) shifted in

parallel to higher or lower levels This mode of adaptation

is currently interpreted as an evolutionary response to

gradients in seasonality ie the degree of seasonal temp-

erature fluctuations influencing the length of the growing

season [61213] However latitudinal adaptations could

also evolve without changing the overall growth capacity

but via shifts in thermal reaction norms toward a higher

or lower range of temperatures in accordance to those

most often experienced in nature [14] In this case ther-

mal reaction norms would cross (figure 1) and represent a

form of genotype environment interaction rather than

CnGV [15] Such thermal adaptation is thought to be

the primary adaptive response to gradients in mean

temperature [1516] However this distinction is still

uncertain as it remains largely based on studies that

examined trait variations in single species and across

single latitudinal gradients where mean temperature

and seasonality varied concomitantly (eg along the

North-American Atlantic coast [81517]) Hence the

confounding effects of mean temperature versus seasonal-

ity as agents of selection have yet to be disentangled

This uncertainty could be effectively addressed by a

This journal is q 2011 The Royal Society

temperature

Figure 1 Schematic diagram of two alternative modes ofthermal reaction norm evolution across thermal gradients

such as those across latitudes Consider the thermal reactionnorm (ie the trait expression at a range of temperatures) of ahypothetical organism adapted to some average temperatureregime (blue curve) A shift to lower average temperatureconditions (eg at higher latitudes) may lead to lsquothermal

adaptationrsquo ie a horizontal shift in the reaction norm anda new lower thermal optimum (1 black curve) This resultsin crossing reaction norms of different populations reared incommon garden environments Alternatively local adap-tation may involve CnGV which leads to genetic increases

in trait expression over the entire range of experienced temp-erature without changing the thermal optimum (2 red curvepopulation reaction norms do not cross)

2 H Baumann amp D O Conover Growth adaptations to climate change

large-scale comparative approach using latitudinal gradi-

ents that differ substantially in their seasonality and

temperature change

Consider for example the highly contrasting latitudi-

nal temperature and seasonality gradients that exist along

the North American Atlantic versus Pacific coast [18] We

quantified this contrast by extracting mean coastal

sea surface temperatures (SST) per week and degree lati-

tude from a publicly available dataset of in situ and

satellite observations (httpdssucaredudatasetsds277

0 1982ndash2008 figure 2) Between 278 N and 498 N the

absolute magnitude of temperature fluctuations along

the Atlantic coast is twice as large (2098C to 2938C

DTAtl frac14 3028C) as on the Pacific side (76ndash2208C

DTPac frac14 1448C) On average mean temperatures

decrease almost three times faster with latitude along

the Atlantic (21118C per latitude) than on the Pacific

coast (20408C per latitude) Seasonality ie the

latitude-specific maximum summerndashwinter difference

is small and independent of latitude along the

Pacific coast (26ndash678C) but strong and increasing

with latitude along the Atlantic coast particularly

north of Cape Hatteras (DTAtl 2858N frac14 638C DTAtl

4558N frac14 1868C figure 2)

We used these two gradients to contrast latitudinal

growth adaptations between two broadly distributed eco-

logically equivalent atherinopsid fish species Pacific

topsmelt (Atherinops affinis) and the Atlantic silverside

(Menidia menidia) To reveal extant genetic variation

in growth capacity and efficiency A affinis offspring

from four different populations were reared in common

garden experiments similar to those published previously

for M menidia [819] Given the small Pacific tempera-

ture gradient with its relatively invariant seasonality we

Proc R Soc B

expected A affinis latitudinal growth adaptations to be

either undetectable or occur via shifts in thermal optima

of growth capacity (crossing thermal reaction norms

figure 1) Instead we found novel evidence for CnGV

ie higher growth capacities with increasing latitude over

the entire thermal range of A affinis While CnGV thus

appears to be the prevalent mode of thermal-reaction-

norm evolution even across simple temperature gradients

(Pacific coast) a strong seasonality gradient (Atlantic

coast) probably necessitates additional adaptive increases

in growth plasticity in high-latitude populations

2 MATERIAL AND METHODS(a) Study species

Menidia menidia and A affinis are two silverside species

(Atherinopsidae) that occur over a broad and similar latitudi-

nal range along the Atlantic and Pacific coast respectively

(M menidia 30ndash468 N [8] A affinis 24ndash458 N [20])

Both are estuarine schooling omnivorous fish of equivalent

trophic levels Both are multiple batch spawners laying

benthic intertidal eggs on a semilunar cycle mainly between

spring and summer [2122] In M menidia onset and length

of the spawning season shift with latitude while the same is

not known for A affinis Both species mature and spawn at

age 1 but differ in their maximum size and age M menidia

is essentially an annual silverside reaching as much as

15 cm in total length with less than 1 per cent of fish reaching

age 2 [21] while A affinis reaches up to 37 cm and typically

lives to ages 4ndash5 [23]

(b) Atherinops affinis offspring collection

Fertilized A affinis eggs were collected by strip-spawning

ripe adults caught with beach seines in four Pacific estuaries

For the first year of experiments (2008) populations P2338N

P3378N and P4438N were sampled whereas in the second year

(2009) populations P1288N P2338N and P3378N were

sampled (table 1) Re-sampling of P2338N and P3378N was

done to facilitate inter-annual comparisons Sufficient gen-

etic diversity representative of each population was

assumed after strip-spawning at least 20 individuals of each

sex To transfer embryos to our laboratory facility at Flax

Pond (Stony Brook University Long Island NY USA)

screens with attached egg masses were wrapped in moist

paper towels and stored in common thermos cans Upon

arrival eggs were placed in aerated 20 l containers sitting

in large (700 l) temperature-controlled baths at three

(ie 15 21 278C in 2008) or four (15 21 24 278C in

2009) temperature treatments Containers were equipped

with screened holes to ensure water exchange with the

baths The photoperiod was 15 L 9 D A salinity of 30+2 psu was maintained during both years using water drawn

from saline ground wells Addition of commercial sea salt

(Instant Ocean) allowed controlling for variation in salinity

among years Depending on the temperature A affinis

larvae hatched 6ndash16 days post-fertilization at approximately

6 mm (population independent) and were start-fed with a

mix of larval powder food (Otohime Marine Weaning Diet

size A Reed Mariculture) and newly hatched brine shrimp

nauplii (Artemia salina San Francisco strain Brine Shrimp

Direct Inc)

Growth capacity ie the temperature-specific growth rate

at unlimited feeding conditions was measured during the

first experimental period Trials started 4ndash13 days

5 10 15 20

25week of year

52 wk 25 wk

52 wk 52 wk

Cape Flattery(484deg N)

(a) (b)Cape NorthNova Scotia

(471deg N)

Cape Cod(418deg N)

Cape Hatteras(352deg N)

Vero Beach(276deg N)

Monterey(365deg N)

Pt Conception(344deg N)

Pt EugeniaBaja California

(278deg N)30 35 40 45 50

475deg N

455deg N

435deg N

415deg N

395deg N

375deg N

355deg N

335deg N

315deg N

295deg N

275deg N5 10

1215 18

21 24 27

15 20 25week of year

30 35 40 45 50

ndash1 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29degC

Figure 2 Contour representation of latitude-specific weekly mean SSTs along the (a) Pacific and (b) Atlantic coast derivedfrom long-term SST data (1982ndash2008) For every 18 of latitude data from the grid cell next to land in the land-sea mask wereused For orientation geographical reference points are given next to each panel Grey lines and values denote the number ofweeks per year when average temperature conditions are above the growth permitting thermal threshold in Pacific (108C) and

Atlantic silversides (128C)

Table 1 Atherinops affinis sampling sites and dates during the two experimental years

estuary site state location sampling date(s) acronym

Laguna Manuela northern arm Baja California MX 28258 N April 2009 (22ndash24) P1288N

114088 W

Tijuana estuary Oneonta Slough California USA 32578 N May 2008 (19) P2338N

117138 W May 2009 (11)Elkhorn Slough South Marsh California USA 36828 N May 2008 (16 and 17) P3378N

121748 W May 2009 (7ndash9)Coos Bay North Bend Oregon US 43388 N June 2008 (19) P4438N

124208 W

Growth adaptations to climate change H Baumann amp D O Conover 3

post-hatch after larvae had reached a mean+ sd total length

(TL) of 80+09 mm (measured to the nearest 01 mm via

calibrated digital pictures and ImagePro software) A

random sample of 10ndash20 larvae per temperaturepopulation

was measured for initial TL and wet weights (W nearest

01 mg Mettler AE163) followed by randomly placing

35+2 larvae in each of three replicate containers (20 l)

per temperaturepopulation Fish were subsequently reared

on ad libitum rations of newly hatched brine shrimp nauplii

until reaching a mean+ sd TL of 232+21 mm (consist-

ent with [815]) At this point a sub-sample of at least 10 fish

per container was measured for TL (01 mm using callipers)

and W (same scale) During the first 3 days of each trial dead

specimens were replaced to correct for initial mortality owing

to handling Total mortality was low averaging 42 (2008)

and 23 fish per replicate (2009) Growth capacity in length

(mm d21) and weight (dimensionless) was calculated for

each replicate by dividing the difference in mean TL and

W (cube-root transformed) by the corresponding duration

of the first experimental period (ie 18ndash80 days)

Dry weight-based food consumption and conversion

efficiency (frac14 the increase in body mass per unit food

ingested ) was assessed during the second experimental

Proc R Soc B

period when the remaining fish grew at excess feeding con-

ditions from 232 mm TL (see above) to an average (+sd)

of 325+27 mm TL The number of remnant nauplii was

estimated daily by taking three 5 ml water samples from each

container and counting all live nauplii in each using Bokorov

chambers and a dissecting microscope Nauplii added to con-

tainers were similarly quantified by counting sub-samples

from nauplii hatching cones The method had an estimated

average precision of 209 per cent (CV) Daily nauplii con-

sumption per container ie remaining thorn added nauplii on

any given day minus nauplii remaining on the following day

was then converted to dry weights (dW ) using a value of

21 mg nauplius21 consistent with Present amp Conover [19]

Fish W was converted to dW using the relationship

dW frac14 00706 W12046 (r2 frac14 0997 p 0001 n frac14 56)

derived from a representative sub-sample that was oven-

dried at 658C for 98 h Mean daily consumption estimates

( body dW ) were scaled by the daily mean dW of all fish in

each replicate derived via calculating a mean dW growth

rate of each replicate during the second period Food conver-

sion efficiency () was calculated for each replicate as the

mean total increase of all fish dW during the second period

relative to the total dW of consumed nauplii

(c) Minimum temperature permitting juvenile growth

To determine the lowest growth-permitting temperature in

A affinis some excess juveniles from reservoir containers in

2009 were reared at ad libitum rations of brine shrimp nau-

plii at 128C 108C and 88C for four to five weeks Prior to

each trial 30 juveniles of similar size were randomly assigned

to each of three (128C) or two replicates (108C 88C) per

population and acclimatized for 5ndash6 days to target tempera-

ture and excess food Trials started by sacrificing a random of

10ndash12 fish for initial W measurements and ended 25ndash38

days later by determining W of all remaining specimens

Mean W of initial and final samples were tested for signifi-

cant differences by t-tests Average mortality was less than

one fish per replicate

(d) Menidia menidia growth capacity and efficiency

We used original data from two analogous common garden

experiments conducted at the same laboratory facility with

identical culturing equipment [8] Laboratory-spawned off-

spring from three populations originating from South

Carolina (SC328N) New York (NY418N) and Nova Scotia

(NS448N) were reared over a similar larval size range

(7ndash18 mm TL) on excess brine shrimp nauplii and at four

replicated temperatures (17 21 28 328C) Estimates of

M menidia food consumption and conversion efficiencies

were derived from slightly smaller fish than A affinis moni-

tored either individually over 24 h (consumption) or in small

groups over 5 days (efficiency) as described in Present amp

Conover [19]

Statistical analyses were conducted in SPSS Statistics 170

(SPSS Inc) using replicate means (containers) as individual

statistical entities Growth capacities (length weight) food

consumptions and conversion efficiencies were first tested for

significant (p 005) effects of temperature using separate

analyses of variance (ANOVA) per year and population Like-

wise population effects were assessed through ANOVAs per

year and temperature Least-significant difference (LSD) or

Dunnet-T3 post hoc tests were used in case of homogeneous

or heterogeneous variances between groups respectively For

growth capacities (GC length weight) data from both years

were used to construct general linear models (LM) of the

form GC frac14 T thorn P thorn T P thorn Y thorn e to test for significant over-

all effects of temperature (T ) population (P) temperature population interaction and year (Y e frac14 error)

3 RESULTS(a) Atherinops affinis thermal reaction norms

In both years growth capacity significantly increased with

temperature and from southern to northern populations

(13 separate ANOVAs p 005 figure 3ab) In 2008

the P4438N population grew on average 030 055 and

076 mm d21 at 15 21 and 278C respectively which

was significantly faster than the P3378N (LSD p

0001) and P2338N populations (LSD p 0001) Popu-

lation growth differences of about 005 mm d21 remained

similar across experimental temperatures in the first year

(ie temperature population interaction term not sig-

nificant LM F426 frac14 109 p frac14 039 figure 3a) During

the second year P3378N fish again grew significantly

faster at all temperatures than P2338N (Dunnet-T3 p

005) which in turn grew faster than those from P1288N

(Dunnet-T3 p 005) Second year growth rates were

7ndash26 higher in the repeated P2338N and P3378N

Proc R Soc B

populations There was also a weak but significant

temperature population interaction (LM F635 frac14 407

p frac14 0006) mainly due to steeper growth capacity

increases with temperature in the P3378N population

(figure 3b) The 248C treatment proved meaningful in

revealing the general nonlinearity of the A affinis

growth reaction norm suggesting 278C to be close to

the thermal growth capacity maximum of A affinis Initial

trials at 128C and 308C failed owing to poor hatching suc-

cess and near total mortality of larvae within the first few

days thus indicating the thermal tolerance limits of the

youngest A affinis life stages Patterns in weight growth

were the same as those described for length Overall an

LM with data from both years returned statistically signifi-

cant effects (p 0001 electronic supplementary material

table S1) of temperature population and year with a weak

temperature population interaction (p frac14 0017)

In both years weight-specific food consumption

increased significantly with temperature (ANOVA

F(2008)224 frac14 87 p 0001 F(2009)332 frac14 420 p

0001) from daily mean values of 21ndash39 body dW at

158C to 45ndash53 body dW at 278C (electronic sup-

plementary material figure S1ab) However there were

no significant differences between populations except for

lower values of P4438N at 158C compared with P3378N

and P2338N (ANOVA F(158C)26 frac14 276 p frac14 001)

In both years food conversion efficiencies showed a

tendency to increase with latitude however data were

very heterogeneous and most differences non-significant

(electronic supplementary material figure S1cd)

In 2008 P4438N converted on average 16 20 and 17

per cent of consumed food into weight at 15 21 and

278C respectively values that were 5 per cent higher

(ANOVA df frac14 2 p 005) than P3378N and P2338N

efficiencies (electronic supplementary material figure

S2c) The two repeated populations showed significantly

(ANOVA df frac14 1 p 005) higher conversion efficien-

cies in the second year at 158C and 218C (electronic

supplementary material figure S2d) consistent with the

observed overall increase in growth rates For P2338N

and P3378N highest mean efficiencies of 212 and 246

per cent occurred at 248C while P1288N values peaked

at 218C (electronic supplementary material figure S2d)

(b) Juvenile growth at low temperatures and

unlimited food

At 128C juveniles from the three populations tested

(P1288N P2338N P3378N) grew in mean weight although

increases were only significant (t-test p 001 table 2)

for the two northernmost populations At 108C weight

changes were still positive but not significantly different

from zero At 88C both P1288N replicates and one of

two P2338N replicates showed slight weight losses while

weight in P3378N did not change significantly (table 2)

(c) Atlantic compared with Pacific patterns of

CnGV in growth capacity

Both in M menidia and A affinis latitudinal growth

adaptations were achieved via increases in growth capacity

across all temperatures from low- to high-latitude popu-

lations not by intra-specific horizontal shifts in thermal

reaction norms Still reaction norms differed greatly

between species but the divergence was owing to the

09(a) (b)

dndash1

18 21temperature (degC)

24 27 15 18 21temperature (degC)

Figure 3 Atherinops affinis Thermal reaction norms of growth capacity in offspring from four populations along the US andMexican Pacific coast as revealed by common garden experiments in (a) 2008 and (b) 2009 Lines intersect means+1 se Forclarity means are slightly jittered along the x-axis Dash-dotted line P1288 N (Laguna Manuela) solid line P2338 N (Tijuana

estuary) dashed line P3378 N (Elkhorn Slough) dotted line P4438 N (Coos Bay)

much greater increase in thermal growth plasticity with

increasing latitude in M menidia When averaged across

populations M menidia growth capacity increased from

032 mm d21 (178C) to 112 mm d21 (288C) which cor-

responds to an average slope of 0074 mm d218C21 or a

Q10 of 312 (electronic supplementary material figure

S2a) In contrast average A affinis growth capacities

increased only from 026 mm d21 at 158C to

078 mm d21 at 278C corresponding to a much smaller

slope of 0043 mm d218C21 (Q10 frac14 249 P4438N values

adjusted for year effect) More importantly the slopes

of growth reaction norms were relatively similar between

A affinis populations but differed greatly between M

menidia populations thus causing the temperature population interaction term to be very strong in Atlantic

but relatively weak in Pacific silversides Menidia menidia

from SC328N grew 029ndash088 mm d21 (17ndash288C)

while those from NS448N grew 033ndash136 mm d21 (17ndash

288C) which means a doubling in slopes from 0049 to

0098 mm d218C21 In contrast southernmost A affinis

(P1288N) grew 020ndash066 mm d21 (15ndash278C) while

northernmost P4438N grew 033ndash090 mm d21 (15ndash

278C adjusted for year effect) corresponding to similar

slopes of 0038 and 0048 mm d218C21 respectively

Food consumption and conversion efficiency of

M menidia increased more strongly with temperature and

latitude than in A affinis (electronic supplementary material

figure S2b [19]) Southernmost M menidia had average

efficiencies of 125 and 213 per cent (at 17 and 288C

respectively) that were comparable to values observed in A

affinis Efficiencies beyond 30 per cent on the other hand

as measured in northernmost M menidia at 288C were con-

siderably above all A affinis estimates However the general

heterogeneity of both datasets and slightly differing exper-

imental protocols place limitations on consumption

efficiency comparisons between the two species

4 DISCUSSIONThis study determined thermal growth reaction norms of

Pacific silverside populations to test the paradigm that

Proc R Soc B

species distributed across simple temperature gradients

evolve local adaptations via shifting thermal growth

optima towards each populationrsquos average temperature

experience (ie lsquothermal adaptationrsquo figure 1) Instead

we found that Pacific silversides evolved CnGV in

growth (figure 1) an alternative mode of reaction norm

evolution previously assumed to be an adaptation to

strong seasonality gradients (eg in Atlantic silversides

[15]) If CnGV is the prevalent adaptive mechanism

across simple temperature gradients in space it probably

plays an important role too for adaptations in time

across thermal gradients such as those elicited by

global warming In addition our novel coast-to-coast

comparison has broadened the current understanding

about CnGV by suggesting a strong link between the

characteristics of latitudinal climate gradients and the

different corresponding CnGV patterns in reaction

norm evolution

(a) Latitudinal growth adaptation in Pacific

silversides

Our results clearly indicated CnGV in growth capacity

among populations of A affinis thereby documenting

the first case of growth CnGV in a coastal Pacific fish

Thermal reaction norms in growth capacity were gener-

ally parallel and differed primarily in elevation with

more northern populations growing faster than those

from the south Because mean growth capacity changed

in rank order with latitude this pattern of variation is

probably the outcome of natural selection not random

genetic drift [5] This suggests that sub-maximal growth

capacities are adaptive probably because evolutionary

incentives for maximizing body size are countered by

physiological trade-offs of fast growth [6] with the

balance being temperature- and therefore latitude-

dependent Selection for increased body size via faster

growth follows from survival advantages during the early

life stages of fish known as lsquobigger-is-betterrsquo or lsquostage-

durationrsquo paradigms [24ndash26] In many fishes larger

body size also increases juvenile survival during the first

winter [27ndash29] and confers higher fertility during

Table 2 Atherinops affinis Growth of juveniles (45ndash50 mm TL) at low temperatures and unlimited food Average fish wet

weights (g) at the beginning (Wini) and end (Wend) of trials at 12 10 and 88C and trial lengths are given per replicateItalicized pairs denote weight loss bold pairs with asterisks denote significant weight changes (t-test)

88C 108C 128C

population replicate WinindashWend (g) days WinindashWend (g) days WinindashWend (g) days

P3378 N 1 057ndash064 25 053ndash061 26 049ndash073 282 058ndash060 25 056ndash061 26 mdash mdash

P2338 N 1 066ndash077 25 070ndash070 26 043ndash061 38

2 070ndash064 25 067ndash070 26 046ndash061 383 mdash mdash mdash mdash 048ndash068 38

P1288 N 1 104ndash078 25 078ndash081 26 039ndash046 322 091ndash083 25 075ndash084 26 044ndash051 323 mdash mdash mdash mdash 045ndash057 32

p 005p 001

adulthood [30] Trade-offs of fast growth on the other

hand include smaller activity scopes and thus poorer burst

and routine swimming of faster compared with slower grow-

ing fish of the same size [31ndash33] which implies higher

predation vulnerabilities for fast growers [34ndash36] The pre-

sent findings for A affinis suggest that the countervailing

selection pressures on growth capacity operate even across

latitudinal scales where the change in mean temperature is

very small For example mean annual temperature differed

by as little as 128C between our Pacific study sites

(figure 4c) but still evoked detectable shifts in growth

capacity The existence of CnGV in Pacific silversides there-

fore indicates that growth is finely tuned to local selection

pressures even across modest changes in climate

Growth capacity variations necessitate changes in either

food consumption conversion efficiency or both yet phys-

iological efficiencies within a species are often assumed to

become maximized by natural selection [3738] Common

garden experiments on vertebrate and invertebrate species

have challenged that notion by finding higher food con-

sumptions and higher conversion efficiencies in faster

growing higher latitude populations (eg [193940])

Our data for A affinis also showed higher conversion effi-

ciencies in northern compared with southern populations

Changes in consumption were not evident either because

the small magnitude of A affinis growth CnGV did not

require them or because the differences were masked by

the large uncertainty of our nauplii counting method

Overall this study supports the notion that sub-maximal

growth rates in fish involve sub-maximal growth efficien-

cies either because directional selection for maximizing

efficiency is weak or because high efficiencies are associ-

ated with so far unknown trade-offs related or

conceptually similar to the trade-offs of fast growth

(b) Countergradient growth variation across

different gradients

When comparing Pacific with Atlantic silversides it is rel-

evant that the same general mode of latitudinal growth

adaptation CnGV has evolved despite such contrasting

gradients in climate Although mean temperature

decreases with latitude along both coasts the Atlantic

gradient is three times steeper than the Pacific tempera-

ture gradient Moreover seasonality ie the degree of

seasonal temperature fluctuations changes greatly with

Proc R Soc B

latitude along the Atlantic coast while being latitude-

independent along the Pacific coast (figure 4cd)

Evidence for growth CnGV in Pacific silversides suggest

that this form of adaptation can evolve in response to

changes in mean temperature alone independent of

changes in seasonality [817]

In M menidia size-selective overwinter mortality acts as

a strong agent of selection in driving the evolution of CnGV

in growth [1215] In many species with distributions across

large seasonality gradients growth is limited to a fraction of

the year when temperatures exceed a species-specific

threshold (eg 128C [8]) In Atlantic silversides this results

in a threefold decrease in growing season length from

southern- to northernmost populations (figure 2b) yet a

reduction in body size is penalized by the increasingly

severe and size-selective winter mortality in latitudes

above approximately 368N ([2841] figure 4d) In contrast

winter mortality is unlikely to be responsible for growth

CnGV in Pacific silversides because ambient temperatures

would permit year-round growth if food is not a constrain-

ing factor (figure 2) Ad libitum-fed juveniles in our

experiments were able to sustain growth above 108C

Temperatures exceeding this threshold occur year-round

in coastal Pacific waters south of 458 N (figures 2 and 4c)

Other studies have documented latitudinal growth CnGV

in fish species where size-selective winter mortality

is equally unlikely (eg M peninsulae [15]) Hence size-

selective winter mortality is not necessary to trigger the

evolution of CnGV in growth rate

Even though CnGV is the common mode of adaptation

in both speciescoasts the norms of reaction differed

greatly in a manner that reflected the gradients in which

they evolved Average growth plasticity is much greater in

Atlantic than Pacific silversides resulting in a two-fold

difference in average slopes of reaction norms between

the two species This coincides with the steeper latitudinal

decrease in mean temperature along the Atlantic than the

Pacific coast (figure 4) More importantly growth plas-

ticity increases greatly from southern to northern Atlantic

silverside populations but remains similar between Pacific

silverside populations This mimics the presence versus

absence of a latitudinal seasonality gradient along the

Atlantic versus Pacific coast (figures 2 and 4) Northern

populations of M menidia must accelerate their growth

rate rapidly with temperature in order to compensate for

16(a) (b)

(c) (d)

3030 35 40 45

30 35 40latitude (degN) latitude (degN)

45 30 35 40 45

30 35 40 45

dndash1

growthgrowth

California Currentupwelling

no growthno growth

15 17 19 21 23

temperature (degC)

25 27 29 31 15 17 19 21 23

temperature (degC)

25 27 29 31

Figure 4 Correspondence of latitudinal growth adaptations in (a) Pacific and (b) Atlantic silversides to large-scale climate gradientsalong the (c) Pacific and (d) Atlantic coast (ab) Population-specific colour shading depicts areas between 10th and 90th percentilesof temperature-specific growth capacity calculated from combined data by dividing the percentile differences in TL before and after

each growth trial by its duration (days) P4438N data were adjusted for year effect (cd) Colour shading depicts areas between averagelong-term annual minima (winter) and maxima (summer) of temperature per 18 latitude along the Atlantic and Pacific coast Thecharacteristic mid-latitude depression in Pacific summer temperatures coincides with the extent of the California Current upwellingsystem [51]Dotted lines denote the latitudinal origin of investigated silverside populations solid lines depict the thermal threshold ofspecies-specific growth potentials (A affinis 108C M menida 128C) (a) PacificmdashAtherinops affinis red linesarea P1288 N green

linesarea P2338 N blue linesarea P3378 N black linesarea P4438 N (b) AtlanticmdashMenidia mendia red linesarea SC328 N greenlinesarea NY418 N blue linesarea NS448 N

the thermally constrained growing season at higher lati-

tudes ([8] figure 2) The greater acceleration of growth

capacity with temperature in northern Atlantic silversides

might therefore be the result of additive selection forces

ie those generally compensating for latitudinal decreases

in mean temperature plus those compensating for the

decrease in growing season

We conclude that small latitudinal gradients in mean

temperature are sufficient to elicit adaptive CnGV in Paci-

fic silversides which display parallel growth reaction norms

across latitudes In contrast Atlantic silversides display

much higher plasticity in growth and also increased plas-

ticity at higher latitudes It is the plasticity of growth that

represents adaptation to highly seasonal environments

driven by the size-selectivity of winter mortality Thus sea-

sonality gradients have a strong magnifying effect on

thermal growth plasticity of high-latitude populations

These conclusions are not restricted to fish but probably

shape local adaptation patterns in other vertebrate and in

Proc R Soc B

invertebrate taxa in a similar way Metabolic compensation

via CnGV is equally prominent in amphibians [11] mol-

luscs [10] and insects [94042] hence gradient effects

should also be evaluated across taxa eg by a meta-analysis

of all published cases of growth CnGV

Noteworthy constraints of our approach include first

its focus on a brief early period in both species life

cycle While growth differences in Atlantic silversides are

known to persist until adult life [43] this is not known yet

for Pacific silversides although growth differences in our

experiment persisted well beyond the reported growth

interval (until approx 4ndash5 cm TL H Baumann 2010

unpublished data) Second it is not known yet for A

affinis how traits like growth rate or body size vary phenoty-

pically in the wild hence whether the genetic differences

partially compensate equalize or overcompensate for

latitudinal temperature differences Third comparing

the Pacific (weak-temperatureno-seasonality) with the

Atlantic gradient (strong-temperaturestrong-seasonality)

and contrasting two species (even if ecologically and

taxonomically equivalent) is inevitably imperfect from a

strict lsquoexperimental designrsquo point of view Atherinops affinis

lives longer attains larger sizes and spawns repeatedly

(iteroparity) more so than M menidia Species-specific

life-history differences may have contributed to the observed

differences in CnGV patterns

(c) Implications for a changing climate

We posit that CnGV will be the principal mechanism by

which ectotherms adapt to temporal gradients such as

those elicited by global climate change If so our findings

indicate that even small increases in mean temperature

will alter local genotype frequencies in many species

Within species ranges phenotypic similarity rather than

divergence is expected owing to the opposing effects of

genetic and plastic responses In silversides for example

some sub-maximal growth capacity presently confers the

highest fitness at a given latitude A rise in temperature

would result in lsquotoo fastrsquo growth of the previously fittest

genotypes meaning that they will incur higher physiologi-

cal growth costs than previously less-successful slower

growing genotypes which then will become the fittest at

this location The overall effect is a poleward migration

of genotypes either literally (if possible) or via natural

selection which remains masked by plastic responses to

temperature Empirical evidence for such temporal

CnGV is still sparse but increasingly emerging [44ndash47]

Genetic shifts may produce little phenotypic change

within a species range [6] but at its extremes climate

change will have visible consequences Species ranges

should gradually shift towards higher latitudes because

at low latitudes the genetic potential to evolve lower

growth capacities in response to higher temperatures is

exhausted and habitat will be lost At high latitudes

new habitat will become available to the most extreme

genotypes ie those with the highest species-specific

growth capacities This prediction is consistent with the

already large and expanding evidence for shifting distri-

butions in many marine and terrestrial taxa worldwide

(eg [48ndash50]) In addition the predicted increases in

poleward heat transport [1] entail that warming will

likely be disproportional at higher than lower latitudes

thus altering seasonality gradients and implying poleward

expansions rather than uniform shifts of species ranges

We are grateful to the many persons who helped during fieldsampling Elizabeth Brown Greg Callier Jorge A RosalesCasian Jeff Crooks Tara Duffy Rikke Preisler GaryVonderhohe and Kerstin Wasson Bill Chamberlain andSteve Abrams greatly facilitated our experiments at FlaxPond Laboratory Soojin Jeon and Annalyse Moskelandhelped with daily nauplii counts during the growthefficiency trials while Owen Doherty assisted in retrievingtemperature data from the Research Data Archive (RDA)RDA is maintained by the Computational and InformationSystems Laboratory (CISL) at the National Center forAtmospheric Research (NCAR) This study was funded bya grant from the US National Science Foundation(OCE0425830) to DOC

REFERENCES1 IPCC 2007 Summary for policymakers In Climate

change 2007 the physical science basis Contribution of work-ing group I to the fourth assessment report of the

Proc R Soc B

Intergovernmental Panel on Climate Change (eds S Solo-mon D Qin M Manning Z Chen M Marquis KB Averyt M Tignor amp H L Miller) Cambridge

New York UKUSA Cambridge University Press2 Via S Gomulkiewicz R De Jong G Scheiner S M

Schlichtning C D amp van Tienderen P H 1995 Adap-tive phenotypic plasticity consensus and controversyTrends Ecol Evol 10 212ndash217 (doi101016S0169-

5347(00)89061-8)3 Gould S J amp Lewontin R C 1979 The spandrels of

San Marco and the panglossian paradigm a critique ofthe adaptationist programme Proc R Soc Lond B205 581ndash598 (doi101098rspb19790086)

4 Kuparinen A amp Merila J 2008 The role of fisheries-induced evolution Science 320 47ndash48 (doi101126science320587247b)

5 Endler J A 1986 Natural selection in the wild Mono-

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6 Conover D O Duffy T A amp Hice L A 2009 Thecovariance between genetic and environmental influencesacross ecological gradients reassessing the evolutionary

significance of countergradient and cogradient variationYear Evol Biol 1168 100ndash129

7 Caley M J amp Schwarzkopf L 2004 Complex growthrate evolution in a latitudinally widespread species Evol-ution 58 862ndash869

8 Conover D O amp Present T M C 1990 Countergradi-ent variation in growth rate compensation for length ofthe growing season among Atlantic silversides fromdifferent latitudes Oecologia 83 316ndash324

9 De Block M Slos S Johansson F amp Stoks R 2008Integrating life history and physiology to understand lati-tudinal size variation in a damselfly Ecography 31 115ndash123 (doi101111j20070906-759005313x)

10 Parsons K E 1997 Contrasting patterns of heritable

geographic variation in shell morphology and growthpotential in the marine gastropod Bembicium vittatumevidence from field experiments Evolution 51 784ndash796 (doi1023072411154)

11 Riha V F amp Berven K A 1991 An analysis of latitudi-

nal variation in the larval development of the wood frog(Rana sylvatica) Copeia 1991 209ndash221 (doi1023071446264)

12 Conover D O 1992 Seasonality and the scheduling oflife history at different latitudes J Fish Biol 41 161ndash

178 (doi101111j1095-86491992tb03876x)13 Yamahira K Kawajiri M Takeshi K amp Irie T 2007

Inter- and intrapopulation variation in thermal reactionnorms for growth rate evolution of latitudinal compen-

sation in ectotherms with a genetic constraint Evolution61 1577ndash1589 (doi101111j1558-5646200700130x)

14 Hutchings J A Swain D P Rowe S EddingtonJ D Puvanendran V amp Brown J A 2007 Genetic vari-ation in life-history reaction norms in a marine fish

Proc R Soc B 274 1693ndash1699 (doi101098rspb20070263)

15 Yamahira K amp Conover D O 2002 Intra- vs interspecificlatitudinal variation in growth adaptation to temperature orseasonality Ecology 83 1252ndash1262 (doi1018900012-

9658(2002)083[1252IVILVI]20CO2)16 Levinton J S amp Monahan R K 1983 The latitudinal

compensation hypothesis growth data and a model oflatitudinal growth differentiation based upon energy bud-gets II Intraspecific comparisons between subspecies of

Ophryotrocha puerilis (polychaeta dorvilleidae) BiolBull 165 699ndash707 (doi1023071541472)

17 Schultz E T Reynolds K E amp Conover D O 1996Countergradient variation in growth among newlyhatched Fundulus heteroclitus geographic differences

revealed by common-environment experiments FunctEcol 10 366ndash374 (doi1023072390285)

18 Fischer A G 1960 Latitudinal variations in organic

diversity Evolution 14 64ndash81 (doi1023072405923)19 Present T M C amp Conover D O 1992 Physiological

basis of latitudinal growth differences in Menidia menidiavariation in consumption or efficiency Funct Ecol 623ndash31 (doi1023072389767)

20 OrsquoReilly K M amp Horn M H 2004 Phenotypic vari-ation among populations of Atherinops affinis(Atherinopsidae) with insights from a geometric morpho-metric analysis J Fish Biol 64 1117ndash1135 (doi10

1111j1095-8649200400379x)21 Conover D O amp Kynard B E 1984 Field and labora-

tory observations of spawning periodicity and behavior ofa northern population of the Atlantic silverside Menidiamenidia (Pisces Atherinidae) Environ Biol Fishes 11

161ndash171 (doi101007BF00000462)22 Schultz L P 1933 The age and growth of Atherinops affi-

nis oregonia (Jordan and Snyder) and other subspecies ofbaysmelt along the Pacific coast of the United StatesUniv Washington Publ Biol 2 45ndash102

23 Emmett R L Hinton S A Stone S L amp MonacoM E 1991 Distribution and abundance of fishes and invert-ebrates in west coast estuaries vol 2 ELMR Report No 8Rockville MD NOAANOS Strategic EnvironmentalAssessments Division

24 Anderson J T 1988 A review of size dependent survivalduring pre-recruit stages of fishes in relation to recruit-ment J Northwest Atl Fishery Sci 8 55ndash66

25 Cushing D H 1990 Plankton production and year-class

strength in fish populations an update of the matchmis-match hypothesis Adv Mar Biol 26 249ndash293 (doi101016S0065-2881(08)60202-3)

26 Leggett W C amp Deblois E 1994 Recruitment inmarine fishes is it regulated by starvation and predation

in the egg and larval stages Netherlands J Sea Res 32119ndash134 (doi1010160077-7579(94)90036-1)

27 Hurst T P 2007 Causes and consequences of wintermortality in fishes J Fish Biol 71 315ndash345 (doi101111j1095-8649200701596x)

28 Schultz E T Conover D O amp Ehtisham A 1998 Thedead of winter size dependent variation and geneticdifferences in seasonal mortality among Atlantic silver-side (Atherinidae Menidia menidia) from differentlatitudes Can J Fish Aquat Sci 55 1149ndash1157

(doi101139cjfas-55-5-1149)29 Sogard S M 1997 Size-selective mortality in the juven-

ile stage of teleost fishes a review Bull Mar Sci 601129ndash1157

30 Blanckenhorn W U 2000 The evolution of body size whatkeeps organisms small Q Rev Biol 75 385ndash407 (doi101086393620)

31 Arnott S A Chiba S amp Conover D O 2006 Evol-ution of intrinsic growth rate metabolic costs drive

tradeoffs between growth and swimming performancein Menidia menidia Evolution 60 1269ndash1278

32 Billerbeck J M Lankford T E amp Conover D O 2001Evolution of intrinsic growth and energy acquisitionrates I Trade-offs with swimming performance in Meni-dia menidia Evolution 55 1863ndash1872

33 Munch S B amp Conover D O 2004 Nonlinear growthcost in Menidia menidia theory and empirical evidenceEvolution 58 661ndash664

34 Biro P A Post J R amp Abrahams M V 2005 Ontogeny

of energy allocation reveals selective pressure promotingrisk-taking behaviour in young fish cohortsProc R Soc B 272 1443ndash1448 (doi101098rspb20053096)

Proc R Soc B

35 Lankford T E Billerbeck J M amp Conover D O 2001Evolution of intrinsic growth and energy acquisitionrates II Trade-offs with vulnerability to predation in

Menidia menidia Evolution 55 1873ndash1881 (doi101111j0014-38202001tb00836x)

36 Munch S B amp Conover D O 2003 Rapid growthresults in increased susceptibility to predation in Menidiamenidia Evolution 57 2119ndash2127

37 Priede I G 1977 Natural selection for energetic efficiencyand the relationship between activity level and mortalityNature 267 610ndash611 (doi101038267610a0)

38 Priede I G 1985 Metabolic scope in fishes In Fishenergetics new perspectives (eds P Tytler amp P Calow)pp 33ndash64 Baltimore MD The John Hopkins UniversityPress

39 Jonassen T M Imsland A K Fitzgerald R BongaS W Ham E V Naeligvdal G Stefansson M O amp

Stefansson S O 2000 Geographic variation in growthand food conversion efficiency of juvenile Atlantic halibutrelated to latitude J Fish Biol 56 279ndash294 (doi101111j1095-86492000tb02106x)

40 Robinson S J W amp Partridge L 2001 Temperature and

clinal variation in larval growth efficiency in Drosophilamelanogaster J Evol Biol 14 14ndash21 (doi101046j1420-9101200100259x)

41 Munch S B Mangel M amp Conover D O 2003 Quan-tifying natural selection on body size from field data

winter mortality in Menidia menidia Ecology 84 2168ndash2177 (doi10189002-0137)

42 Blanckenhorn W U 1991 Life-history differences inadjacent water strider populations phenotypic plasticity

or heritable responses to stream temperature Evolution45 1520ndash1525 (doi1023072409899)

43 Billerbeck J M Schultz E T amp Conover D O 2000Adaptive variation in energy acquisition and allocationamong latitudinal populations of the Atlantic silverside

Oecologia 122 210ndash219 (doi101007PL00008848)44 Ellegren H amp Sheldon B C 2008 Genetic basis of

fitness differences in natural populations Nature 452169ndash175 (doi101038nature06737)

45 Garant D L Kruuk L E B McCleery R H amp

Sheldon B C 2004 Evolution in a changing environ-ment a case study with great tit fledging mass AmNat 164 115ndash129 (doi101086424764)

46 Merila J Kruuk L E B amp Sheldon B C 2001Cryptic evolution in a wild bird population Nature 412

76ndash79 (doi10103835083580)47 Wilson A Pemberton J Pilkington J Clutton-Brock

T Coltman D amp Kruuk L 2007 Quantitative geneticsof growth and cryptic evolution of body size in an island

population Evol Ecol 21 337ndash356 (doi101007s10682-006-9106-z)

48 Beaugrand G Reid P C Ibanez F Lindley J A ampEdwards M 2002 Reorganization of North Atlanticmarine copepod biodiversity and climate Science 296

1692ndash1694 (doi101126science1071329)49 Gardner J L Heinsohn R amp Joseph L 2009 Shifting

latitudinal clines in avian body size correlate with globalwarming in Australian passerines Proc R Soc B 2763845ndash3852 (doi101098rspb20091011)

50 Nye J A Link J S Hare J A amp Overholtz W J 2009Changing spatial distribution of fish stocks in relation toclimate and population size on the Northeast UnitedStates continental shelf Mar Ecol Prog Ser 393 111ndash129 (doi103354meps08220)

51 Snyder M A Sloan L C Diffenbaugh N S amp BellJ L 2003 Future climate change and upwelling in theCalifornia Current Geophys Res Lett 30 1823(doi1010292003GL017647)