EN60CH18-Beebe ARI 26 November 2014 14:24

Anopheles punctulatus Group:Evolution, Distribution,and Control∗

Nigel W. Beebe,1,† Tanya Russell,2 Thomas R. Burkot,2

and Robert D. Cooper3

1The University of Queensland, St. Lucia, Brisbane, Australia and CSIRO Ecosystem Sciences,Brisbane, Australia; email: n.beebe@uq.edu.au2James Cook University, Cairns, Australia; email: tanya.russell@jcu.edu.au,tom.burkot@jcu.edu.au3Australian Army Malaria Institute, Brisbane, Australia; email: bob.cooper@defence.gov.au

Annu. Rev. Entomol. 2015. 60:335–50

First published online as a Review in Advance onOctober 17, 2014

The Annual Review of Entomology is online atento.annualreviews.org

This article’s doi:10.1146/annurev-ento-010814-021206

Copyright c© 2015 by Annual Reviews.All rights reserved

∗This paper was authored by employees of theBritish Government as part of their official dutiesand is therefore subject to Crown Copyright.

†Corresponding author

Keywords

punctulatus group, malaria vectors, Australasia, cryptic species

Abstract

The major malaria vectors of the Southwest Pacific belong to a group ofclosely related mosquitoes known as the Anopheles punctulatus group. Thegroup comprises 13 co-occurring species that either are isomorphic or carryoverlapping morphological features, and today several species remain infor-mally named. The advent of species-diagnostic molecular tools in the 1990spermitted a new raft of studies into the newly differentiated mosquitoesof this group, and these have revealed five species as the region’s primarymalaria vectors: An. farauti, An. hinesorum, An. farauti 4, An. koliensis, andAn. punctulatus. Species’ distributions are now well established across PapuaNew Guinea, northern Australia, and the Solomon Archipelago, but littlehas been documented thus far in eastern Indonesia. As each species revealssignificant differences in distribution and biology, the relative paucity ofknowledge of their biology or ecology in relation to malaria transmission isbrought into clearer focus. Only three of the species have undergone someform of spatial or population genetics analyses, and this has revealed strikingdifferences in their genetic signatures throughout the region. This reviewcompiles and dissects the key findings for this important mosquito groupand points to where future research should focus to maximize the output offield studies in developing relevant knowledge on these malaria vectors.

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INTRODUCTION

The members of the Anopheles punctulatus group are found from the Moluccas in Indonesia andthroughout New Guinea to the islands of Papua New Guinea (PNG), northern Australia, theSolomon Islands, and Vanuatu (8, 16) (Figure 1). The group contains many of the major vectorsof malaria and lymphatic filariasis in the region (Table 1) and has undergone intensive study tounderstand the transmission of these diseases and to devise, implement, and evaluate effectivecontrol strategies. The ancestors of this group are believed to be from the Oriental region, theirmovement from Southeast Asia facilitated by the formation of the Indo-Malayan Archipelago 5mya (68). Further dispersal throughout the Australian region was aided by the glaciation eventsof the Pleistocene (1.6–0.01 mya), when sea levels were approximately 130 m lower, Australia andNew Guinea were connected, and sea gaps between the islands of the region were reduced (42).Discontinuities in topography and climate throughout this region and the existence of numerousisolated islands have provided opportunities for population isolation, genetic drift, and speciation(8). The group includes the An. farauti complex and currently contains 13 species (Table 1). Anumber of these species contain geographically isolated and apparently independently evolvinggenotypes (see Evolution of the Group, below).

Identification of the member species of any vector group is vital in terms of studying their role indisease transmission and evaluating potential control strategies. Until the late 1980s, identificationof this group relied on proboscis morphology with the three then-known species—An. farauti,An. koliensis, and An. punctulatus—distinguished by three morphological markers: An. farauti hadan all-black scaled labium; An. koliensis had a small pale patch of scales on the ventral surface at the

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New BritainNew Britain

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SOLOMON ISLANDS

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Bougainville

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PAPUA

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Figure 1Map of the Southwest Pacific and where the members of the An. punctulatus group of species are endemic. Species members of theAn. punctulatus group extend from the Moluccas in Indonesia in the west, throughout New Guinea, to the islands of Papua NewGuinea, northern Australia, and the Solomon Islands, and as far south as Vanuatu. Follow the Supplemental Materials link from theAnnual Reviews home page at http://www.annualreviews.org to download an interactive PowerPoint version of this figure thatdocuments distribution of several Anopheles species in the Southwest Pacific.

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Supplemental Material

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Table 1 Currently recognized members of the Anopheles punctulatus group

Species Date discovered Vectorial Status Reference(s)

Malaria FilariasisAnopheles punctulatus 1901 Major Major 25, 37, 45, 48, 51Anopheles farauti 1902 Major Major 27, 45, 48, 69Anopheles koliensis 1945 Major Major 25, 48, 77Anopheles clowi 1946 None None 47, 82Anopheles hinesorum 1973 Major Unknown 24, 48Anopheles torresiensis 1982 Unknown Unknown 73Anopheles rennellensis 1991 Unknown Unknown 102Anopheles farauti 4 1993 Major Unknown 48, 52Anopheles farauti 5 1993 None None 52Anopheles farauti 6 1993 Minor Unknown 48, 52Anopheles irenicus 1994 None None 55Anopheles sp. nr. punctulatus 1995 Unknown Unknown 54Anopheles farauti 8 2008 Minor Unknown 22, 48

anterior of the labium; and An. punctulatus had pale scaling covering the apical half of the labium(82). These markers were overt and practical for identifying specimens under field conditions. Butanomalies in the distribution and biology existed across some of the members of the group: Forexample, An. farauti was recognized as a coastal species capable of breeding in brackish water butwas also found in the highlands of PNG more than 1,000 m above sea level (50). This suggestedthe existence of additional species within the group.

Then, through the 1980s and 1990s, the application of molecular techniques—allozyme elec-trophoresis (46, 52, 55, 73, 100), DNA hybridization (14, 43), and polymerase chain reaction(PCR) restriction fragment length polymorphism (RFLP) methods (17)—resolved the speciescomposition of the group (Table 1). These studies revealed that some An. punctulatus group mem-bers shared similar proboscis morphology with members of the An. farauti complex: An. farauti,An. hinesorum [formally An. farauti 2 (86)], An. torresiensis [formally An. farauti 3 (86)], An. farauti4–6, An. irenicus [formally An. farauti 7 (85)], and An. farauti 8 all have an all-black scaled labium.Additionally An. farauti 4 was found to be polymorphic for this marker, and specimens of thisspecies can display An. koliensis, An. farauti s.l., and An. punctulatus proboscis types (18, 50).

The PCR-RFLP method of identification (described below) is now the most commonly usedspecies diagnostic tool, and although its throughput cannot match those using morphologicalmarkers and DNA-based identification, it appears robust and accurate (44, 50).

EVOLUTION OF THE GROUP

Species Identification at the Molecular Level

An. farauti was first described in 1902 (69). Five species (An. farauti, An. koliensis, and An. punctula-tus as well as the rarely found An. clowi and An. rennellensis) were initially described through overtmorphological variation. Cross-mating experiments and polytene chromosomal banding studiessplit An. farauti in Australia into three species [An. farauti 1, 2, and 3; now known as An. farauti,An. hinesorum, and An. torresiensis (86)]. Allozyme studies confirmed the reproductive isolation inthese three species and suggested three additional isomorphic species in PNG, subsequently des-ignated An. farauti 4, 5, and 6 (52). Another reproductively isolated population in PNG’s Western

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Province, isomorphic to An. punctulatus, was found and called Anopheles species near punctulatus(54). Subsequent allozyme studies on Guadalcanal in the Solomon Islands also characterizedAn. farauti 7 (55), now called An. irenicus (85).

With a dozen species in the An. punctulatus group, allozyme-based species identification was nolonger conducive to high-throughput analyses, as specimens needed to be stored frozen to preservethe mosquitoes’ protein enzymes. Genomic DNA-based methods were first developed for thethree Australian species (An. farauti, An. hinesorum, and An. torresiensis) in the early 1990s usingisotopic, chromogenic, and chemiluminescence detection systems (43). Subsequently, genomicDNA probes were developed to distinguish An. punctulatus; An. koliensis; and four sibling species,An. farauti and An. farauti 4, 5, and 6 (14), with identification of An. irenicus from the SolomonIslands following (13). Eventually, high-throughput species identifications using genomic probeson squash blots were developed for the ten most common species (44–46, 50).

Complementary to the genomic DNA probes, a PCR-based tool was designed around therapidly evolving repetitive gene family spacer—ribosomal DNA (rDNA) ITS2 (17)—that sup-ported the initial allozyme species groupings identified by Foley & Bryan (52). The ITS2 remainsa popular target region for species identification: Despite the paucity of knowledge on its non-Mendelian evolution, it retains practical utility as a genetic marker that can show recent geneticdiscontinuity within and between Anopheles populations (1, 9, 15). Using the ITS2 PCR-RFLPspecies diagnostic tool in conjunction with the genomic probes contributed significantly to theextensive species distribution studies on the An. punctulatus group (Figure 1) (7, 45, 46, 50).

Today, two additional DNA-based species diagnostic methods are available that distinguishthe five common malaria vector species in PNG: An. punctulatus, An. koliensis, An. farauti,An. hinesorum, and An. farauti 4. One is a Luminex-based multiplex ligase detection reactionand fluorescent microsphere–based assay based around polymorphisms in the rDNA ITS2 (61),and the second is a PCR-based multiplex assay based around mutations in the voltage-gated sodiumchannel or knockdown resistance gene (60), although field studies utilizing these two methods areyet to emerge, and so it is difficult to evaluate their utility.

Species Evolution

The evolutionary relationships between group members have been investigated through severalDNA sequence phylogenetic studies using either mitochondrial DNA (mtDNA) cytochrome oxidase2 gene (COII ) markers (53), whole mtDNA genomes (71), nuclear rDNA ITS2 (12), nuclearrDNA small subunits (11), or both mtDNA and nuclear rDNA small subunits (10). Commonrelationships have revealed two major clades, one containing all the An. farauti–like species (withall-black proboscises) but excluding An. farauti 4, which is in the second clade with An. punctulatusand Anopheles species near An. punctulatus (half-black, half-white proboscises). The position ofAn. koliensis varies slightly, as it sits basal to all species in the COII tree, positioned betweenAn. punctulatus and An. farauti 4 in the whole mtDNA genome study, or is positioned betweenthe An. farauti and An. punctulatus clades in the rDNA trees. More detail on these evolutionaryrelationships relative to external morphology and biology is available (11, 16).

Population Genetics

As each species exists as a collection of local subpopulations with varying degrees of movementbetween them, population genetics studies can provide important insights into vector movementsand population dynamics by quantifying the levels of movement (gene flow) between subpopula-tions. Early population genetics studies have been generated for An. punctulatus group members,with the coastally restricted An. farauti receiving the lion’s share.

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Broad-scale population genetics studies of An. farauti include intraspecific genotyping of therDNA ITS1 and ITS2 (9), phylogeographic studies using ITS1 DNA sequences (22), and sequenc-ing of the mitochondrial cytochrome oxidase I gene (COI) and a nuclear ribosomal protein (rpS9)(3). These studies show a complex population genetic distribution for this malaria vector andhave revealed two genetically distinct populations in Australia (in the Northern Territory andQueensland) most likely maintained by the lower rainfall in the southern region of the Gulf ofCarpentaria (Carpentarian Gap) that acts as an east/west biological filter across northern Australia(23). The rDNA ITS1 and ITS2 studies showed three genetically distinct populations in PNG(in Western Province, southern Papuan Peninsula coast, and PNG northern coast; 9, 22). Theone mtDNA COI and nuclear rpS9 sequencing study undertaken distinguished only two geneticgroups in PNG (Western Province and the rest of PNG, 3); however, the An. farauti mtDNA cladefound in southern New Guinea and Queensland shows deeper affinities to its cryptic sympatricrelative An. hinesorum, with evidence of a putative introgression event of An. hinesorum mtDNAonto the nuclear background of An. farauti reinforcing their close relationship. An. hinesorum per-sists in the New Guinea highlands and has adapted to the cooler climate with its closest relativesAn. farauti 5 and 6, which are only found in these highland regions. Could the presence of theAn. hinesorum mitochondrial genome in An. farauti provide some thermal adaptation to coolerclimates for An. farauti populations and permit its southern expansion into Queensland (5)? Thebarriers to movement and gene flow for this coastal species through Australia and PNG appearto correlate with climate disjunctions and ocean gaps. The An. farauti population carrying theAn. hinesorum mtDNA genome ends in the Gulf of Papua, where the monsoon region meets thecontinual wet region of PNG.

Overt population genetic structure through the Solomon Archipelago is well documented, withthe northern Solomon Islands standing distinct from the southern Vanuatu Islands, and a fewstudies attempt to drill into the population genetic relationships within the Solomon Archipelago.A DNA sequencing study using the mtDNA NADH dehydrogenase subunits 4–5 (NAD 4–5)across five islands in Vanuatu found significantly distinct fixation index values (FST —a measureof population differentiation due to genetic structure) between all pairs of islands (81). A phylo-geographic study using the mtDNA COII sequence comparing An. farauti populations in PNGand the Solomon Islands also identified significant FST values between the islands of Guadalcanaland Malaita, which are only 60 km apart (59), substantiating the idea that small sea gaps arepresent as identifiable barriers to gene flow. A mtDNA COI and microsatellite study throughoutthe Solomon Archipelago followed up on observed variations in the time of night feeding forAn. farauti on different islands in the archipelago, and this revealed significant and often large FST

values between different island populations with restricted gene flow between islands separated byas little as 40 km (2). In this study, discordance between the maternally inherited mtDNA and thebiparentally inherited nuclear microsatellites was found to be present, and male-biased dispersalwas hypothesized as one mechanism to account for nuclear gene flow between islands withoutmitochondrial gene flow—a tantalizing idea, as we still understand little of the male Anophelesmosquitoes’ biology.

The population genetics of An. hinesorum provides an interesting counterpoint to its crypticsister species An. farauti (3). A putative introgression event may have pushed An. hinesorum mtDNAinto the An. farauti nuclear background in populations now existing through its southern rangeof New Guinea and Queensland. An. hinesorum is not restricted to the coast and exists bothinland and on elevated land. Thus, it is exposed to the region’s complex biogeography—unlikeAn. farauti, whose coastal distribution is usually more uniform (8, 16). Accordingly, An. hinesorumshows a complex population genetics signature through its Southwest Pacific (SWP) distribution,suggesting a long history in the region (3). Mitochondrial and nuclear rpS9 studies reveal genetic

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structure that is strongly geographical. Like An. farauti, An. hinesorum presents two geneticallydistinct populations in Australia (Northern Territory and Queensland), again probably becauseof less rainfall through the Carpentarian Gap (23). In PNG, the Western Province contains agroup genetically distinct from that of Queensland, which extends east to a region of geographic,climatic, and genetic discontinuity in PNG’s southern Gulf region and on from the CentralRange to the Gulf of Papua (see Figure 1). Here, three distinct genetic groups identified by boththe mtDNA and nuclear rpS9 are found in close proximity and may represent distinct species,although evidence for nuclear rpS9 allele sharing and a single example of mtDNA haplotypesharing would indicate recent separation of these groups. The second PNG group appears to bespatially restricted to the Gulf region and Western Highlands, extending into the lowland Gulfregion—a region that receives very high rainfall (92). East of the Papuan Gulf region the third PNGgenetic group extends east along the Papuan Peninsula (north and south of the Central Range),with a fourth group found in northwest PNG. Three of these genetic groups have been identifiedas malaria vectors (48); however, evidence of interbreeding between these four geographicallydistinct populations is weak, as sympatric populations have not yet been available for study. Onenuclear rpS9 haplotype from the Western Province group was identified in the Papuan Peninsulagroup population but could be an ancestral polymorphism rather than evidence of recent gene flow.There is evidence of two founding events into the Solomon Archipelago from different geneticgroups in PNG along with additional evidence of gene flow occurring between these geneticallydistinct groups in the Solomon Islands. This could indicate that the PNG genetic groups ofAn. hinesorum may be reproductively compatible. However, extrapolation of data from malariavector studies between these genetically distinct lineages of An. hinesorum may be unwise, as eachgroup may well show variations in their biology.

Population genetics investigations into An. punctulatus present a different story. DNA sequenc-ing of the mtDNA COI and rpS9 as well as 12 microsatellite markers revealed much less geneticstructure through PNG compared with An. farauti or An. hinesorum (87). Here, An. punctulatusappears to have undergone a population bottleneck in PNG followed by a recent population andrange expansion (87). However, population structure was identified between populations in PNG,the northern Solomon Archipelago (Buka Islands), and central Solomon Archipelago (Guadal-canal). It is an important malaria vector of the region, and its ability to move into human-modifiedlandscapes and traverse unsealed roads may well enhance the movement of insecticide resistancegenes, whereas regional economic growth is likely to facilitate the expansion of the geographicrange of An. punctulatus. The population structure found through the Solomon Archipelago ismost likely the effect of sea barriers reducing gene flow between island populations, leading torapid lineage sorting.

Little is known about the population genetics of the other species in the group. Observationsfrom field studies in the Madang/Maprik areas of PNG identified three ITS2 PCR-RFLP variantgenotypes within An. koliensis and suggest some differences in biting times could be associated withthese genotypes, with mosquitoes of one genotype biting earlier in the night (18). Thus, althoughit is thought that An. koliensis may eventually split into three species, the study identifying thesegenotypes was not conclusive and further investigation is required.

DISTRIBUTION AND PAST AND PRESENT KNOWLEDGEOF THE AN. PUNCTULATUS GROUP

Our current knowledge of the species composition of the group and our ability to accuratelyidentify the member species using molecular-based tools have made it possible to determine thedistribution of the group’s members over much of their range (Figure 1).

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The Solomon Archipelago

An. farauti is a coastal species. It is the only member of the group found in Vanuatu, and, as it canbreed in brackish water, it is the only species found on the myriad of tiny islands and coral atollsthroughout the region (97). In the Solomon Islands An. farauti can be found with An. hinesorumand An. irenicus (7, 30); however, there is good evidence to suggest that the latter two species arezoophilic in the Solomon Islands and do not feed on humans. Therefore, specimens of An. farautis.l. collected as they bite humans should all be An. farauti (7, 55).

An. punctulatus also occurs in the Solomon Islands, though it appears to be uncommon, havingrecently been found only on the islands of Guadalcanal and Malaita (7, 84). Of all the members ofthe group, this species is the most reliably identified by proboscis morphology. An. koliensis is thefifth member of the group to be found in the Solomon Islands, but it may have subsequently beeneradicated by indoor residual insecticide spraying (IRS) and insecticide-treated bed nets (ITN),as it has not been recorded there since the early 1990s (7, 55, 84).

Thus, for the Solomon Islands, where An. farauti and An. punctulatus are the only malariavectors, proboscis morphology remains reliable. Because of its late-night, indoor feeding behavior,An. punctulatus, like An. koliensis, was readily controlled by IRS and ITN. But unlike An. koliensis,An. punctulatus can still be found (7, 62). However, recent surveys on Santa Isabel, where An.punctulatus was previously found to be common, have failed to find this species (30). The preferredlarval habitats of An. punctulatus are small, shallow, exposed pools devoid of other flora and fauna; itchooses these sites to the exclusion of all other members of the group (41, 45). On Santa Isabel thesetypes of sites were common along the vast network of logging roads, but all of these sites surveyedcontained An. hinesorum (30). It is possible that in the Solomon Islands An. punctulatus populationshave been under competitive pressure from An. hinesorum as well as being exposed to insecticide.

An. rennellensis has been found on only one remote island in the Solomons: Specimens have notbeen analyzed using molecular diagnostic tools, and until this is done its existence as a member ofthe group is questionable (72).

The islands of Buka and Bougainville (geographically part of the Solomon Archipelago) havea species composition similar to that on the Solomon Islands in that An. koliensis appears to havebeen eliminated, and An. hinesorum is common, but as in the Solomon Islands it is zoophilic,leaving An. punctulatus and An. farauti as the main malaria vectors. Both of these can be reliablyseparated by proboscis morphology (45, 93). In the Solomon Islands a number of the main islandgroups are yet to be comprehensively surveyed, including Choiseul, New Georgia, San Cristobal,and Malaita, which is the last known location of An. koliensis in the Solomon Islands (84).

Papua New Guinea

On the island of New Guinea the situation is more complex. Species richness increases with 11 ofthe 13 members of the An. punctulatus group occurring there. Of these, several species are unlikelyto play any role in malaria or filariasis transmission because of their scarcity, limited distribution,and lack of contact with humans. These species include An. clowi, An. torresiensis, Anopheles spp.near punctulatus, and An. farauti 5 (48, 50).

In PNG, south of the Central Range, the four most abundant species are An. farauti,An. hinesorum, An. koliensis, and An. punctulatus (49, 50). An. farauti is again restricted to thecoast (usually within one kilometer of saline or brackish water). Unlike the zoophilic genotypesin the Solomon Islands, An. hinesorum in PNG is anthropophilic and is capable of transmittingmalaria (48). It is predominantly found in inland, lowland areas [87.6% of collection sites (n =324) are more than one kilometer from the coast (50), and it has also been found with An. faraution the coast, although this is not common]. Like An. hinesorum, An. koliensis is a species of inland,

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lowland areas, and the two species can occur sympatrically. An. hinesorum only rarely displaysan An. koliensis–type proboscis, and An. koliensis can display an An. farauti–type proboscis—butthis occurs in only 12% of specimens (50). An. punctulatus and An. koliensis rarely share the sameproboscis type. Thus separation of the members of the group south of the Central Range in PNGusing proboscis morphology may not be problematic.

Malaria is unstable in the highlands of New Guinea, occurring there in epidemics (6, 75,79). The two common members of the group that occur in these areas are An. farauti 6 andAn. punctulatus (50). An. farauti 6 is a large mosquito, larger than any of the other members ofthe An. farauti complex (50, 70). In this region species identification using proboscis morphologyshould not be an issue, with An. punctulatus being reliably separated from An. farauti 6.

On the north side of the Central Range in PNG five members of the group are present: An.farauti, An. hinesorum, An. farauti 4, An. koliensis, and An. punctulatus. As in other parts of itsrange An. farauti is restricted to the coast. The other four species are uncommon along the coastand are primarily found in inland, lowland areas. Of 324 sites identified for An. hinesorum only12.4% were coastal; of 43 sites surveyed for An. farauti 4, only 6.9% were coastal (50). Of all themembers of the group An. punctulatus can most reliably be identified by proboscis morphology: Astudy of 676 specimens identified as An. punctulatus using this marker found that 97% were indeedAn. punctulatus as identified by PCR-RFLP (50).

Where An. hinesorum, An. farauti 4, and An. koliensis occur sympatrically, problems may beencountered in separating species using traditional proboscis morphology. An. farauti 4 can bequite polymorphic, with 56% displaying an An. koliensis–type proboscis, 16% an An. punctulatus–type proboscis, and 28% an An. farauti–type proboscis (18, 50).

The vectors of malaria and lymphatic filariasis were intensively studied north of the CentralRange during the 1980s. The main study sites were the Madang area, which included coastal andinland villages (31–33, 35, 36, 38–41, 57), and the Maprik area (63–65), where the study villageswere situated in inland river valleys. In these study sites, An. farauti, An. hinesorum, An. farauti 4,An. koliensis, and An. punctulatus have been found, in some cases sympatrically. However, despitethe presence of overlapping morphological characters among some of these species, the resultsof these earlier studies should not be dismissed without carefully examining the locations of thestudies and the probable mix of species sharing key diagnostic morphological characteristics in agiven area. Along the coast, An. farauti is the dominant species (18, 19, 39, 50), and in surveysconducted in coastal villages, where An. hinesorum and An. farauti 4 are uncommon, proboscismorphology would reliably separate An. farauti from An. koliensis and An. punctulatus. In a numberof inland study sites, An. punctulatus was the dominant species: In Buksak, an inland village southof Madang where malaria and filariasis transmission has been studied, the dominant species is An.punctulatus, which was 99.9% of collections (32, 37). Similarly in the Maprik area where filariasistransmission was studied, An. punctulatus was the only anopheline collected in four of the six studyvillages (21). Problems with the use of proboscis morphology may arise in villages where An.farauti 4 makes up a sizable component of the anopheline fauna.

Although distribution of the members of the group on the main island of PNG is now wellknown, the major islands of the Bismarck Archipelago have been poorly studied to date. An. farautihas been recorded on Manus Island. But, surprisingly, New Britain and New Ireland have yet tobe surveyed.

Northern Australia

Three members of the group—An. farauti, An. hinesorum, and An. torresiensis—occur in northernAustralia, where the annual rainfall is >1,200 mm (46, 100). Although malaria no longer occurs on

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the mainland (the last outbreak was in 1962; 20), it still occurs in the Torres Strait Islands (broughtacross from PNG), and there have been outbreaks in northern Queensland due to imported cases(58). An. farauti s.l. was incriminated as a vector during a vivax epidemic in Cairns in 1942 (20),but given that all three species occur sympatrically in the Cairns area, exactly which species wasinvolved is uncertain. An. farauti and An. hinesorum have wide distributions outside of Australia,but An. torresiensis is only found outside of Australia in the southern plains of PNG, where thedrier monsoonal climate typical of northern Australia occurs (8).

West Papua and Papua Provinces: Indonesia

Historically An. farauti, An. koliensis, and An. punctulatus have been recorded from the Indonesianside of the island of New Guinea, but there have been very few recent studies where specimenscollected have been identified using molecular techniques. Thus, most studies in this region arelikely to combine cryptic species (74, 90, 103). An. farauti 4 has not yet been confirmed in thisregion; however, as the environment is analogous to PNG there is no reason to doubt its presence,particularly in the inland river valleys on the northern side of the Central Range, where both specieshave been found to be abundant.

Modeling Species’ Distribution

In light of the extensive distribution data now available, several papers on species’ distributionalmodeling (using bioclimatic ecological niche modeling) are available that try to extrapolate iden-tified species’ spatial structure through areas where surveys are lacking. These can also provideinsight into the environmental parameters that may be driving species’ distributions. One ex-ample includes the CLIMEX modeling of An. farauti in Australia that showed a future climatechange scenario range expansion for the species (26); two years after this study was published, thedistribution of An. farauti was found to extend beyond the hypothesized future climate changedistribution (104), highlighting issues involved in modeling the distribution of the species ratherthan the distribution of the entomologist.

The boosted regression tree correlative modeling of the An. farauti complex throughout theSWP (which saw six species modeled together; 88) was not overly helpful, as the resulting dis-tributional hypotheses are being driven by a variety of different species’ traits. For example,the following were modeled together: An. farauti, a coastally restricted species with a broaddistribution and strong tendencies for brackish water; An. hinesorum, a freshwater-only specieswith a broad distribution throughout coastal and inland regions, showing elevational tendenciesand utilizing a variety of larval habitats; and An. torresiensis, which is highly restricted to themonsoon climate region of northern Australia and southern New Guinea. Thus, it is unlikelythat combining multiple species such as these into a single analysis will be overly informative.Single-species distribution modeling has been performed and includes a boosted regression treestudy of An. koliensis in the SWP (88), although it has been suggested that this species con-tains three intraspecific rDNA genotypes (18). Nonetheless, this distributional hypothesis ex-trapolates across almost all of New Guinea, including the New Guinea highlands, and east toGuadalcanal in the Solomon Islands. With some insight on An. koliensis’s biology, one wouldquestion the high probability of encountering An. koliensis in the PNG highlands that is sug-gested by the model, as only one specimen has ever been found at high elevation (over 1,000 m)(50).

Distribution models for single species of the Australian members of the An. punctulatus groupprovide some insight into the mosquitoes’ biology (98, 99). In this, An. farauti and An. torresiensis

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were reasonably described across northern Australia through a combination of ecological nichemodeling using Genetic Algorithm for Rule-Set Production (GARP; 96) and data mining proce-dures (98), although outputs appeared to be less satisfactory in terms of explaining the environ-mental factors associated with the distribution of An. hinesorum (98). An. farauti and An. hinesorumhave two genetically distinct populations across northern Australia (in Queensland and the North-ern Territory) that could obscure the analyses, as they may have evolved slightly different traitsin isolation; so, it may be valuable to also analyze these genetically (and geographically) distinctpopulations in isolation. Nonetheless, atmospheric moisture was a critical variable for each ofthe three Australian species, and elevation appeared to be a critical variable for An. farauti (98,99). Given that this species is found in both fresh and brackish water and that the reason for itscoastal distribution is not fully understood, its ecological niche seems to be influenced by higheratmospheric moisture near the sea as well as by steep elevation gradients immediately inland fromthe coast (98, 99), perhaps driving the hydrology of its coastal breeding sites.

MALARIA VECTOR CONTROL

Strategies Targeting Vectors Indoors

IRS with dichlorodiphenyltrichloroethane (DDT) and dieldrin started in PNG and eastern In-donesia in the 1950s (78, 89, 90), with the An. punctulatus group displaying high levels of suscepti-bility to DDT throughout PNG and the Solomon Islands (4, 95). Not surprisingly, IRS with DDTwas highly effective in initially controlling malaria in PNG and the Solomon Islands. However,in this area, unlike other geographic areas where DDT was used, An. farauti maintained its phys-iological susceptibility to the insecticide but rapidly shifted its behavior to feed more frequentlyoutdoors and earlier in the evening, thereby minimizing its contact with the insecticide deployedin IRS (101).

In the late 1980s, ITNs were implemented in PNG (56), followed by the Solomon Islands (62).The demonstrated efficacy of ITNs in reducing the incidence of Plasmodium falciparum infectionin children up to four years old in PNG (40, 56) and in significantly reducing human infectionrates and densities of An. farauti in the Solomon Islands (62) led to their widespread distributionthroughout the geographic range of the An. punctulatus group. The development of insecticidalnets capable of maintaining their insecticidal properties after up to 20 washes subsequently ledto the replacement of ITNs with long-lasting insecticide-treated nets (LLINs). However, theeffectiveness of IRS, ITNs, and LLINs depends on humans being inside houses late at night toattract vectors inside, where they come into contact with the insecticide either when attempting totake a blood meal or when resting on walls after feeding. Documentation of increasingly early andoutdoor biting by members of the An. punctulatus group (30, 101), and in particular An. farauti,has raised concerns about the future efficacy of IRS and LLINs for either control or eradicationof malaria (83).

Strategies Targeting Vectors Outside of Houses

The Solomon Islands is often cited as an example of effective programs that target sources oflarvae. This approach used pipes to maintain salinity levels in coastal lagoons at concentrationsgreater than An. farauti can tolerate (67). However, this strategy has only been studied for impactson larvae (28), and it has never been evaluated with regard to cases of malaria in humans or impactson the biting density of adult An. farauti. In Vanuatu, larvivorous fish were a component in thesuccessful malaria elimination strategy on Aneityum (66). However, the impact of the fish was

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ultimately believed to be marginal because of the failure to identify all larval habitats and theincompleteness of fish predation on larvae.

Strategies for Control or Elimination

The effectiveness of IRS and LLINs will depend on not only where and when a mosquito seeks ablood meal on a human but also the number of blood meals taken during the extrinsic incubationperiod (the feeding cycle length has been estimated as 48 h; 80, 94) as well as the proportion ofpeople inside houses and the proportion of these who sleep under an LLIN or the proportion ofhouses treated with IRS.

The survival of An. farauti has been estimated as 0.7 per feeding cycle (from an area in PNGwith neither ITNs nor IRS; 34). This means that 16.8% of vectors would be estimated to survivefor the duration of the extrinsic incubation period (allowing for a 10-day extrinsic incubationperiod with 5 feeding cycles of 48 h each) in the absence of both LLINs and IRS. In Guadalcanal,part of the Solomon Islands, An. farauti feeds predominantly outdoors (74%) and early in theevening (65% of biting occurs between 6:30 and 10 PM) (29). The World Health Organizationstates that LLIN coverage is 100% in the Solomon Islands and malaria incidence is dropping(91, 105). Thus, despite the exophilic and early biting behavior of the Solomon Islands’ dominantvector, An. farauti, IRS and LLINs can exert a significant effect in controlling malaria providedthat people use LLINs or sleep in an IRS-treated house. However, if An. farauti should seek bloodmeals earlier and more often outdoors, the effectiveness of LLINs and IRS will diminish. NeitherIRS nor LLINs would be capable of eliminating malaria transmission.

Malaria elimination where the members of the An. punctulatus group are the dominant vectorswill require more than an intervention that attacks the vectors inside houses. Intervention strategiesto complement LLINs and IRS that reduce the transmission component occurring outside ofhouses are required. This is further reflected in the Solomon Islands Malaria Program Review,which recognized that “LLINs and IRS are insufficient intervention tools to further reduce malariatransmission, and that other innovative vector control tools, including personal protection, larvalcontrol and treated barriers, should be evaluated” (76).

CONCLUSION

Malaria remains the most important vector-borne disease in the SWP region, with easternIndonesian, PNG, and the Solomon Islands enduring some of the highest attack rates in theworld outside Africa (105). As can be seen from this review much remains to be learned about themembers of the An. punctulatus group that are the primary malaria vectors of this region. Basicparameters such as distribution and ecology are still unknown for many areas, especially Indonesiabut also a number of the islands of PNG and the Solomon Islands. Studies on the behavior andbiology of the members with regards to their role in transmission have only been conducted in afew areas on the north coast of PNG and in parts of the Solomon Islands, but throughout muchof the range of these species these characteristics are largely unknown. Independently evolvingpopulations have been revealed within a number of the member taxa, but this has not been ex-tensively studied in all the members and little is known of the behavior of the currently identifiedintraspecific genetic groups with regard to their role in transmission. Control strategies such asIRS and ITNs, which only target adults entering houses to feed, have struggled to make a seriousimpact on malaria transmission where the vector feeds early in the night and outdoors, as in thecase of the main coastal vector An. farauti. Additional control measures that act against other stagesof the life cycle and against adults while they are outdoors are required. The SWP region has a

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complex and rich biogeography that presents one of the most challenging (and exciting) places tostudy the vector biology of the An. punctulatus group.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

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Annual Review ofEntomology

Volume 60, 2015Contents

Breaking Good: A Chemist Wanders into EntomologyJohn H. Law � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Multiorganismal Insects: Diversity and Function ofResident MicroorganismsAngela E. Douglas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �17

Crop Domestication and Its Impact on Naturally SelectedTrophic InteractionsYolanda H. Chen, Rieta Gols, and Betty Benrey � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �35

Insect Heat Shock Proteins During Stress and DiapauseAllison M. King and Thomas H. MacRae � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �59

Termites as Targets and Models for BiotechnologyMichael E. Scharf � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �77

Small Is Beautiful: Features of the Smallest Insects andLimits to MiniaturizationAlexey A. Polilov � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 103

Insects in Fluctuating Thermal EnvironmentsHerve Colinet, Brent J. Sinclair, Philippe Vernon, and David Renault � � � � � � � � � � � � � � � � � 123

Developmental Mechanisms of Body Size and Wing-BodyScaling in InsectsH. Frederik Nijhout and Viviane Callier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 141

Evolutionary Biology of Harvestmen (Arachnida, Opiliones)Gonzalo Giribet and Prashant P. Sharma � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 157

Chorion Genes: A Landscape of Their Evolution, Structure,and RegulationArgyris Papantonis, Luc Swevers, and Kostas Iatrou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 177

Encyrtid Parasitoids of Soft Scale Insects: Biology, Behavior, and TheirUse in Biological ControlApostolos Kapranas and Alejandro Tena � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 195

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Extrafloral Nectar at the Plant-Insect Interface: A Spotlight on ChemicalEcology, Phenotypic Plasticity, and Food WebsMartin Heil � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 213

Insect Response to Plant Defensive Protease InhibitorsKeyan Zhu-Salzman and Rensen Zeng � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 233

Origin, Development, and Evolution of Butterfly EyespotsAntonia Monteiro � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 253

Whitefly Parasitoids: Distribution, Life History,Bionomics, and UtilizationTong-Xian Liu, Philip A. Stansly, and Dan Gerling � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 273

Recent Advances in the Integrative Nutrition of ArthropodsStephen J. Simpson, Fiona J. Clissold, Mathieu Lihoreau, Fleur Ponton,

Shawn M. Wilder, and David Raubenheimer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 293

Biology, Ecology, and Control of Elaterid Beetles in Agricultural LandMichael Traugott, Carly M. Benefer, Rod P. Blackshaw,

Willem G. van Herk, and Robert S. Vernon � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 313

Anopheles punctulatus Group: Evolution, Distribution, and ControlNigel W. Beebe, Tanya Russell, Thomas R. Burkot, and Robert D. Cooper � � � � � � � � � � � � � � 335

Adenotrophic Viviparity in Tsetse Flies: Potential for Population Controland as an Insect Model for LactationJoshua B. Benoit, Geoffrey M. Attardo, Aaron A. Baumann,

Veronika Michalkova, and Serap Aksoy � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 351

Bionomics of Temperate and Tropical Culicoides Midges: KnowledgeGaps and Consequences for Transmission of Culicoides-Borne VirusesB.V. Purse, S. Carpenter, G.J. Venter, G. Bellis, and B.A. Mullens � � � � � � � � � � � � � � � � � � � � 373

Mirid (Hemiptera: Heteroptera) Specialists of Sticky Plants: Adaptations,Interactions, and Ecological ImplicationsAlfred G. Wheeler Jr. and Billy A. Krimmel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 393

Honey Bee ToxicologyReed M. Johnson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 415

DNA Methylation in Social Insects: How Epigenetics Can ControlBehavior and LongevityHua Yan, Roberto Bonasio, Daniel F. Simola, Jurgen Liebig,

Shelley L. Berger, and Danny Reinberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 435

Exaggerated Trait Growth in InsectsLaura Lavine, Hiroki Gotoh, Colin S. Brent, Ian Dworkin,

and Douglas J. Emlen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 453

viii Contents

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Physiology of Environmental Adaptations and Resource Acquisitionin CockroachesDonald E. Mullins � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 473

Plant Responses to Insect Egg DepositionMonika Hilker and Nina E. Fatouros � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 493

Root-Feeding Insects and Their Interactions with Organismsin the RhizosphereScott N. Johnson and Sergio Rasmann � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 517

Insecticide Resistance in Mosquitoes: Impact, Mechanisms, and ResearchDirectionsNannan Liu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 537

Vector Ecology of Equine PiroplasmosisGlen A. Scoles and Massaro W. Ueti � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 561

Trail Pheromones: An Integrative View of Their Role in Social InsectColony OrganizationTomer J. Czaczkes, Christoph Gruter, and Francis L.W. Ratnieks � � � � � � � � � � � � � � � � � � � � � � 581

Sirex Woodwasp: A Model for Evolving Management Paradigms ofInvasive Forest PestsBernard Slippers, Brett P. Hurley, and Michael J. Wingfield � � � � � � � � � � � � � � � � � � � � � � � � � � � � 601

Economic Value of Biological Control in Integrated Pest Management ofManaged Plant SystemsSteven E. Naranjo, Peter C. Ellsworth, and George B. Frisvold � � � � � � � � � � � � � � � � � � � � � � � � � 621

Indexes

Cumulative Index of Contributing Authors, Volumes 51–60 � � � � � � � � � � � � � � � � � � � � � � � � � � � 647

Cumulative Index of Article Titles, Volumes 51–60 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 652

Errata

An online log of corrections to Annual Review of Entomology articles may be found athttp://www.annualreviews.org/errata/ento

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50. D

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