1. Introduction
1.1. Why study Anopheles diversity: Relevance for malaria control
The need to understand diversity in
This chapter focuses on the need to not only characterise species boundaries, ecology and distributions, but also to understand the potential for divergence and the extent of gene flow within and between species of
2. Diversity of Anopheles species across Southeast Asia
This chapter primarily focuses on the diversity of
The diversity of Anopheline fauna that exists within Southeast Asia is richer than in any other region of the world [14], and at least 19 species, some of which comprise cryptic species complexes, are known to play some role in malaria transmission [15]. Exactly 50% of the 24 currently recognised
Early attempts for a geographical stratification of malaria units [17] were based on the biogeographical realms of Wallace (1876). However, Wallace’s Oriental Realm is largely inappropriate for South Asia and Southeast Asia due to the exceptionally high biodiversity and high heterogeneity of spatial distribution of vectors in this region [14-15]. On a smaller spatial scale there are multiple biogeographical subregions within Southeast Asia, including the biodiversity hotspot regions of IndoBurma, Sundaland, the Philippines and Wallacea ([18]; see figure 1). These hotspots were defined in part on the basis of endemism so it is not surprising that they appear to define the distributions of many malaria vectors, with clear patterns of species turnover apparent at each of the biogeographical boundaries.
The first biogeographical boundary that shows a clear association with species distributions is that separating IndoBurma from southwestern Asia (Figure 1). It should be noted that northeast India, although politically part of India, is biogeographically and ecologically aligned with IndoBurma rather than southwestern Asia. The
The boundary between the biodiversity hotspot regions of IndoBurma and Sundaland (Figure 1) represents a second major biogeographic transition in Southeast Asia, and is characterised by high species turnover in a number of taxonomic groups (e.g. birds, mammals and reptiles [19-21]). This long-recognised biogeographic transition was first noted by Wallace in 1869, and though its exact position along the Thai-Malay Peninsula is debated, with some dispute as to whether the transition occurs at the Isthmus of Kra (10º30’N) or the Kangar-Pattani line (6-7ºN) further south [22], its biogeographical significance is unquestioned. The transition is associated with dramatic climate and phytological changes. IndoBurma has a very seasonal climate in terms of both temperature and rainfall, whereas that of Sundaland is much more stable, with precipitation levels remaining high throughout the year. Whereas mixed moist deciduous forest is the dominant forest habitat type of IndoBurma, that of Sundaland is perhumid evergreen forest [23-24]. Thus it seems unsurprising that this is a region of high species turnover, as the selective pressures on either side of the Isthmus of Kra biogeographic transition would differ considerably, potentially driving rapid adaptive change and subsequent ecological speciation following the dispersal of taxa from one side to the other.
Again, the majority of
The final distinct biodiversity hotspot regions of Southeast Asia are those of Wallacea and the Philippines, each of which harbours a unique assemblage of
In addition to the divisions between the biogeographic regions discussed above, there are some apparent transitions within biogeographic regions. As previously discussed, there is some distinction between the species composition of each of the major Sundaic Islands and the mainland, although several species within the
Although the distributions of the majority of
The distinctiveness of the Anopheline fauna of each of the major biogeographic regions of Southeast Asia, which occurs despite the continuity of landmass between these regions, suggests that ecological factors, such as climate and dominant habitat type, play a key role in defining species distributions. Malaria stratifications based on ecological biomes, such as forest, foothill and urban regions, are therefore especially useful in designating control efforts [16]. The clear ecological similarity between many closely related vector species also suggests a strong conservation of ecological niche. Species within the
3. Processes driving the diversification of the Anopheline fauna of Southeast Asia
3.1. The role of historical environmental change
As discussed in the first section of this chapter, as well as an understanding of extant species distribution and ecology, the characterisation of population dynamics and levels and patterns of gene flow both within and between species is essential, as the effective size and connectivity of populations will influence the speed at which traits relevant to malaria control evolve and spread between them [38]. The release of genetically modified mosquitoes has been proposed for the control of vector populations in Africa [39]; if such approaches were developed for Southeast Asia, population genetic studies would be necessary to determine the number of genetically modified individuals and release sites needed for a successful program [39-40]. The estimation of levels of contemporary gene flow is greatly complicated, however, by the historical genetic structuring of mosquito populations [41-42]. In order to reliably infer patterns of contemporary gene flow, it is therefore essential that we first gain a thorough understanding of the population history of the
As with all organisms, the genetic structuring of
3.1.1. Miocene (23.0 – 5.3 mya): Dispersal of Pyretophorus series and Myzomyia series from Africa to Asia
The collisions of the Indian, African and Australian plates with Eurasia all had substantial impacts on the landscape and fauna of Southeast Asia. India initially collided with Southeast Asia approximately 50 million years ago (mya), and the subsequent northwards push of the Indian plate resulted in the formation and uplift of the Himalayas [44], forming a geographical barrier between Southeast Asia and the rest of the Asian continent. The second major period of tectonic activity, which involved the uplift of the Himalayas approximately 25mya, coincided with the collision of the African and Eurasian plates. This latter event resulted in the closure of the Tethys Sea and so created a land connection between the continents of Africa and Asia [48]. Although this region is now characterised by arid desert habitat, a corridor of tropical forest is thought to have persisted during the humid periods of the early and mid-Miocene [48]. Combined with low sea-levels, this allowed forest taxa such as the ancestors of the Oriental Myzomyia and Pyretophorus Series to disperse from their African origins into Southeast Asia [49-50]. Increasingly arid conditions and the consequent desertification of East Asia during the late Miocene (6.2 – 5mya) restricted this exchange [48, 51], effectively isolating the forest fauna of Asia and Africa. The Oriental and African taxa within the Myzomyia and Pyretophorus Series form monophyletic groups in both cases (with the exception of the placement of the African species
3.1.2. Late Miocene and Pliocene (6 – 2mya): Forest fragmentation drives allopatric speciation
The increasingly cool and arid climate responsible for extensive desertification across East Asia during the late Miocene also resulted in the expansion of grassland and savannah habitat across Southeast Asia [52]. The consequent reduction in available
3.1.3. Pleistocene (1.8 mya – 11,000 ya): Changes in landmass configuration drive dispersal and divergence within species
During the Pleistocene, the ongoing fluctuations in the extent of forest cover across Southeast Asia were exacerbated by the dramatic impact of glacio-eustatic sea level change on the region’s climate [45-46]. These sea-level fluctuations, which involved drops of between 50 and 200 meters during each of the Pleistocene glaciations [56], had a more dramatic effect on the climate and habitats of Southeast Asia than those of any other tropical region [46]. Sea level regressions of 60 meters or more result in the exposure of the Gulf of Thailand, and dramatically reduce the surface area of the South China Sea [45] (Figure 7). This reduction in the surface area of ocean across Southeast Asia would have reduced evaporation from the ocean’s surface, and consequently the levels of moisture carried across the mainland by the monsoon rains. Due to the coincidence of periods of reduced sea level with glacial maxima, the reduction in the monsoon moisture content would have been exacerbated by the cool temperature and consequently reduced moisture-carrying capacity of the air [46]. The distribution of forest across Southeast Asia was in turn affected by the reduced precipitation levels, as regions with sufficient moisture to support them shrank [47, 57]. Reconstructions of the dominant habitat types across Southeast Asia during the Last Glacial Maximum (LGM), which are based on palynonlogical and sedimentological data, indicate that tropical forest became restricted to small and isolated pockets, often at intermediate altitudes and at the base of mountains, where precipitation run-off ensured moisture levels remained high enough to support it [58-59]. Substantial areas of forest habitat were replaced by grassland and savannah, although larger areas of forest are thought to have persisted in insular relative to mainland Southeast Asia [47, 57].
The reduction of forest habitat to small and isolated patches would have resulted in the fragmentation of forest-associated
The evidence for allopatric speciation associated with Pleistocene environmental change is especially strong between the cryptic sister species
Although the above examples provide exceptions, the majority of speciation events within the Anopheline fauna of Southeast Asia are estimated to pre-date the Pleistocene [25, 30, 49], and the environmental fluctuations of the Pleistocene appear to have been much more influential in driving divergence and shaping population structure within, rather than between,
Such an influence of Pleistocene climatic change might be expected to be shared across multiple forest-dependent taxa. This hypothesis has been statistically evaluated in several
Besides driving divergence between isolated populations, the restriction of populations to refugial regions is also likely to have influenced patterns of genetic diversity across the landscape. The long-term persistence of populations within refugial regions leads to the accumulation of high genetic diversity and population structure. Since only a fraction of the gene pool is generally involved in range expansion, regions that are repeatedly re-colonised following local extinction are expected to harbour substantially lower genetic diversity [70-71]. These predicted patterns can be used to identify potential refugial regions, and in Southeast Asia have led to the identification of the mountainous regions of northeastern India, northern Myanmar, northern Thailand, southern China and northern Vietnam as potential Pleistocene glacial refugia for
Although the majority of main
3.1.4. The formation of land-bridges and consequent creation and destruction of dispersal routes during the Pleistocene
Besides substantially influencing climatic conditions across Southeast Asia, the alterations in landmass configuration during the Pleistocene also had a considerable effect on the availability of migration routes across Southeast Asia. The Sunda Shelf is thought to have been dominated by grassland and savannah habitats during periods of exposure, and thus was important in allowing the exchange of open-habitat species such as early hominins and hoofed mammals between the mainland and the Sundaic Islands [56, 74]. Although the open habitat is thought to have acted as a barrier to dispersal of forest-associated taxa between Borneo and Sumatra, the persistence of gallery forests along the major river systems of the Sunda Shelf is thought to have provided narrow dispersal corridors for such taxa [74]. The repeated exposure and submergence of the Sunda Shelf is thought to have promoted allopatric speciation in a number of Sundaic taxa, with periods of dispersal facilitated by the exposure of the Sundaland bridge being followed by the isolation of populations on different landmasses as sea levels rose, e.g. [26, 75]. Although as previously mentioned, there is some species turnover within
Inferred speciation events within the
3.2. Ecological factors
The rich diversity of habitat types and host species available within Southeast Asia is likely to have driven differential local adaptation leading to divergence between ecologically isolated populations and consequent ecological speciation [43]. Characterisation of the bionomics, habitat and feeding preferences of vector species, and of interspecific and intraspecific variation in these traits, is an important step in defining appropriate vector control strategies. Additionally, through the relation of species biology and ecology to phylogenetic relationships we may infer the ecological adaptations that are likely to have driven divergence and speciation, and given rise to the most effective malaria vectors within Southeast Asia. This may also give an indication of the characters that are evolutionarily labile and those that show niche conservatism, which may allow the prediction of how species may respond to anthropogenic change such as urbanisation and an expansion of agriculture. The Leucosphyrus Group provides one example of ecological differentiation between closely related species. This group includes several important vectors of both human and simian malaria, and due to its medical importance, has been well characterised in terms of taxonomy, phylogeny and ecology ([76]; reviewed in [33] and [32]). The mapping of species feeding preferences onto a phylogenetic tree supported two independent host-switching events, each leading to the evolution of anthropophilic taxa from their zoophilic ancestors, which fed on non-human primates in the forest canopy [64]. This switch in host preference is likely to have involved a change in behaviour, from feeding in the forest canopy to feeding on the forest floor, as well as changes in host detection. This host switch was estimated to have occurred during the late Pliocene/early Pleistocene, which has important implications for human evolution, suggesting that hominins were present within Southeast Asia as early as 2.2 million years ago (mya), and that their arrival shaped the evolution of malaria vectors [64].
As well as the change in host preference, several other ecological adaptations are likely to have driven divergence within the Leucosphyrus Group. The distribution of the group overlaps the biogeographical transition zone that lies between IndoBurma and Sundaland (figure 1;[21]), with the majority of species being limited in distribution to the region either south, or north, of this divide. All basal species are limited in distribution to insular Southeast Asia, suggesting that this region represents the group’s ancestral origin [64]. Despite the existence of several species within peninsular Malaysia only two northwards dispersal events into IndoBurma were supported, suggesting that this dispersal required some kind of ecological adaptation. It has been suggested that this may have involved an adaptation specific to the more seasonal climate of Southeast Asia, such as the increased resistance of larvae to desiccation observed in
All species within the Leucosphyrus Group show a strong association with tropical forest habitat and are remarkably similar in terms of habitat preference; however
The likely involvement of ecological variation in species divergence has also been assessed within the Maculatus Group, within which the phylogenetic mapping of species’ altitudinal distribution supported a scenario of ecological speciation through altitudinal replacement[25]. This is a phenomenon in which the distribution of one species replaces that of its sister species along an altitudinal gradient, as populations become adapted to the environmental conditions within their altitudinal zone [77-78]. Species within the Maculatus Group typically lay their eggs within streams or the rock pools associated with them. Various characteristics of these typical larval habitats, such as the water temperature and the speed of water flow, are likely to vary with altitude. Adaptation to these specific larval habitats may therefore have played a role in the ecological divergence of populations at higher altitudes [25].
Whilst ecological differences between species may provide clues as to the factors driving past speciation events, investigation of intraspecific ecological variation within a species range may give an indication of the processes involved in the early stages of ecological divergence and speciation. Variation in traits such as anthropophilic vs. zoophilic, or exophagic vs. endophagic feeding preferences have the potential to greatly influence vector status, and there are several species in which vector status is reported to vary across the range.
Although several examples of species-specific differences in ecology can be found, there does seem to be considerable ecological similarity between species within each of the major groups, as was discussed earlier in this chapter. All species within the Leucosphyrus Group, for example, show an extremely strong association with forest habitat, laying their eggs within temporary forest pools [31-32]. Although species vary in their feeding preferences, and
4. Gene flow within and between species
The absence or presence of gene flow between populations and species has a considerable impact on the dynamics of malaria transmission, and on the measures used for vector control. In the absence of gene flow, genetic drift and local adaptation result in the genetic differentiation of populations, and potentially in divergence at ecological traits likely to influence malaria transmission [38, 43]. The presence of gene flow, on the other hand, homogenises genetic variation and may lead to the exchange of adaptive and potentially medically relevant alleles between populations. Although the accumulation of reproductive barriers generally restricts gene flow between species, gene flow may still continue across certain genomic regions, creating patterns of differential divergence and introgression across the genome [7, 87-89]. Numerous cases of mitochondrial introgression between
The dynamic demographic histories of the major malaria vector species, as discussed previously in this chapter, complicate the inference of contemporary gene flow. For example, population bottlenecks and subsequent expansions, which appear to be common in the Anopheline fauna of Southeast Asia (e.g. [29, 42]), can homogenise genetic variation and thus eliminate accumulated genetic diversity between isolated populations, giving false signal of ongoing gene flow [94]. Knowledge of the historical patterns of divergence, range restriction and expansion in
5. Future directions
Despite the wealth of knowledge of
Secondly, the investigation of patterns of population structure at a genomic level remains to be performed in the
Besides gene flow between populations within a species, the possibility of contemporary interspecific gene flow should also be considered. The identification and characterisation of such contemporary gene flow between species will be vitally important in determining whether medically important traits may spread between them. Again, this issue will benefit from a genome-wide approach, as patterns of introgression and divergence will vary across the genome due to the differential influence of selection [7, 87-89]. Genomic studies have been invaluable in characterising divergence and introgression across the genome, and identifying the targets of selection within the genomes of
The possibility of ongoing gene flow or historic introgression between species is also important for the reliable delineation of species boundaries, particularly within complexes of closely related and morphologically identical
References
- 1.
Fantini B. Anophelism without malaria: an ecological and epidemiological puzzle. Parassitologica 1994; 36: 83-106. - 2.
Hackett L.W. and Missiroli A. The natural disappearance of malaria in certain parts of Europe. American Journal of Epidemiology 1931; 13: 57-78. - 3.
Collins F.H. and Paskewitz S.M. A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Molecular Biology 1996; 5: 1-9. - 4.
Coluzzi M., Sabatini A., Petrarca V., and Di Deco M.A. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae Complex. Transactions of the Royal Society of Tropical Medicine and Hygiene 1979; 73: 483-497. - 5.
Besansky N.J., Krzywinski J., Lehmann T. , et al. Semipermeable species boundaries betweenAnopheles gambiae andAnopheles arabiensis : Evidence from multilocus DNA sequence variation. Proceedings of the National Academy of Sciences 2003; 100: 10818-10823. - 6.
Lehmann T. and Diabate A. The molecular forms of Anopheles gambiae : A phenotypic perspective. Infection, Genetics and Evolution 2008; 8: 737-746. - 7.
Neafsey D.E., Lawniczak M.K.N., Park D.J. , et al. SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 2010; 330: 514-517. - 8.
Lawniczak M.K.N., Emrich S.J., Holloway A.K. , et al. Widespread divergence between incipientAnopheles gambiae species revealed by whole genome sequences. Science 2010; 330: 512-514. - 9.
Torre A.d., Fanello C., Akogbeto M. , et al. Molecular evidence of incipient speciation withinAnopheles gambiae s.s. in West Africa. Insect Molecular Biology 2001; 10: 9-18. - 10.
Favia G., della Torre A., Bagayoko M. , et al. Molecular identification of sympatric chromosomal forms ofAnopheles gambiae and further evidence of their reproductive isolation. Insect Molecular Biology 1997; 6: 377-383. - 11.
Appawu M.A., Baffoe-Wilmot A., Afari E.A., Nkrumah F.K., and Petrarca V. Species composition and inversion polymorphism of the Anopheles gambiae Complex in some sites of Ghana, West Africa. Acta Tropica 1994; 56: 15-23. - 12.
Chareonviriyaphap T., Bangs M.J., and Ratanatham S. Status of malaria in Thailand. Southeast Asian Journal of Tropical Medical Public Health 2000; 31: 225-237. - 13.
Trung H.D., Van Bortel W., Sochantha T. , et al. Malaria transmission and major malaria vectors in different geographical areas of Southeast Asia. Tropical Medicine & International Health 2004; 9: 230-237. - 14.
Manguin S. and Boëte C. Global impact of mosquito biodiversity, human vector-borne diseases and environmental change. In: J.L. Pujol (eds), The Importance of Biological Interactions in the Study of Biodiversity. InTech: Winchester, UK.2011 27-50. - 15.
Sinka M., Bangs M., Manguin S. , et al. The dominantAnopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic precis. Parasites & Vectors 2011; 4: 89. - 16.
Schapira A. and Boutsika K. Chapter 3 - Malaria Ecotypes and Stratification. In: D. Rollinson and S.I. Hay (eds), Advances in Parasitology. Academic Press.2012 97-167. - 17.
Macdonald G. Local features of malaria. (eds), The Epidemiology and Control of Malaria. Oxford University Press: London.1957 63-99. - 18.
Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B., and Kent J. Biodiversity hotspots for conservation priorities. Nature 2000; 403: 853-858. - 19.
Hughes A.C., Satasook C., Bates P.J.J., Bumrungsri S., and Jones G. Explaining the causes of the zoogeographic transition around the Isthmus of Kra: using bats as a case study. Journal of Biogeography 2011; 38: 2362-2372. - 20.
Round P.D., Hughes J.B., and Woodruff D.S. Latitudinal range limits of resident forest birds in Thailand and the Indochinese–Sundaic zoogeographic transition. Natural History Bulletin of the Siam Society 2003; 51: 69-96. - 21.
Woodruff D.S. and Turner L.M. The Indochinese - Sundaic zoogeographic transition: a description and analysis of terrestrial mammal species distributions. Journal of Biogeography 2009; 30: 569-580. - 22.
Woodruff D. Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity. Biodiversity and Conservation 2010; 19: 919-941. - 23.
Hughes J.B., Round P.D., and Woodruff D.S. The Indochinese-Sundaic faunal transition at the Isthmus of Kra: an analysis of resident forest bird species distributions. Journal of Biogeography 2003; 30: 569-580. - 24.
Woodruff D.S. Neogene marine transgressions, palaeogeography and biogeographic transitions on the Thai-Malay Peninsula. Journal of Biogeography 2003; 30: 551-567. - 25.
Morgan K., O'Loughlin S.M., Mun-Yik F. , et al. Molecular phylogenetics and biogeography of the Neocellia Series ofAnopheles mosquitoes in the Oriental Region. Molecular Phylogenetics and Evolution 2009; 52: 588-601. - 26.
Reddy S. Systematics and biogeography of the shrike-babblers ( Pteruthius ): Species limits, molecular phylogenetics, and diversification patterns across southern Asia. Molecular Phylogenetics and Evolution 2008; 47: 54-72. - 27.
Abegg C. and Thierry B. Macaque evolution and dispersal in insular south-east Asia. Biological Journal of the Linnean Society 2002; 75: 555-576. - 28.
Singh S., Prakash A., Yadav R.N.S. , et al. Anopheles (Cellia)maculatus group: Its spatial distribution and molecular characterization of member species in north-east India. Acta Tropica 2012; 124: 62-70. - 29.
Morgan K., O’Loughlin S.M., Chen B. , et al. Comparative phylogeography reveals a shared impact of Pleistocene environmental change in shaping genetic diversity within nineAnopheles mosquito species across the Indo-Burma biodiversity hotspot. Molecular Ecology 2011; 20: 4533-4549. - 30.
Zarowiecki M., Walton C., Torres E. , et al. Pleistocene genetic connectivity in a widespread, open-habitat-adapted mosquito in the Indo-Oriental region. Journal of Biogeography 2011; 38: 1422-1432. - 31.
Reid J.A. Anopheline mosquitoes of Malaya and Borneo. Malaysia, Government of Malaysia 1968 - 32.
Obsomer V., Defourny P., and Coosemans M. The Anopheles dirus Complex: spatial distribution and environmental drivers. Malaria Journal 2007; 6: (26). - 33.
Manguin S., Garros C., Dusfour I., Harbach R.E., and Coosemans M. Bionomics, taxonomy, and distribution of the major malaria vector taxa of Anopheles subgenusCellia in Southeast Asia: An updated review. Infection, Genetics and Evolution 2008; 8: 489-503. - 34.
Foley D.H., Rueda L.M., Peterson A.T., and Wilkerson R.C. Potential distribution of two species in the medically important Anopheles minimus Complex (Diptera: Culicidae). Journal of Medical Entomology 2008; 45: 852-860. - 35.
Brandling-Bennett A.D., Doberstyn E.B., and Pinichpongse S. Current epidemiology of malaria in Southeast Asia. Southeast Asian J Trop Med Public Health 1981; 12: 289-297. - 36.
Das M.K., Adak T., and Sharma V.P. Genetic analysis of a larval colour mutant, yellow larva, in Anopheles sundaicus . Journal of the American Mosquito Control Association 1997; 13: 203-204. - 37.
Dusfour I., Linton Y.-M., Cohuet A. , et al. Molecular Evidence of Speciation Between Island and Continental Populations ofAnopheles (Cellia )sundaicus (Diptera: Culicidae), a principal malaria vector taxon in Southeast Asia. Journal of Medical Entomology 2004; 41: 287-295. - 38.
Hartl D.L. and Clark A.G. Principals of population genetics. Sunderland, U.S.A., Sinauer Associates, Inc. 2007. - 39.
Riehle M.A., Srinivasan P., Moreira C.K., and Jacobs-Lorena M. Towards genetic manipulation of wild mosquito populations to combat malaria: advances and challenges. Journal of Experimental Biology 2003; 206: 3809-3816. - 40.
Hay B.A., Chen C.-H., Ward C.M. , et al. Engineering the genomes of wild insect populations: Challenges, and opportunities provided by synthetic Medea selfish genetic elements. Journal of Insect Physiology 2010; 56: 1402-1413. - 41.
Zellmer A.J. and Knowles L.L. Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence. Molecular Ecology 2009; 18: 3593-3602. - 42.
O'Loughlin S.M., Okabayashi T., Honda M. , et al. Complex population history of twoAnopheles dirus mosquito species in Southeast Asia suggests the influence of Pleistocene climate change rather than human-mediated effects. Journal of Evolutionary Biology 2008; 21: 1555-1569. - 43.
Coyne J.A. and Orr H.A. Speciation.Sunderland, MA, Sinauer Associates 2004. - 44.
Hall R., The plate tectonics of the Cenozoic SE Asia and the distribution of land and sea. 1998, Leiden: Backhuys Publishers. p. 133 - 163. - 45.
Voris H.K. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography 2000; 27: 1153-1167. - 46.
Heaney L.R. A synopsis of climatic and vegetational change in Southeast Asia. Climatic Change 1991; 19: 53-61. - 47.
White J.C., Penny D., Kealhofer L., and Maloney B. Vegetation changes from the late Pleistocene through the Holocene from three areas of archaeological significance in Thailand. Quaternary International : The record of Human /Climate interaction in Lake Sediments 2004; 113: 111-132. - 48.
Janis C.M. Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review of Ecology and Systematics 1993; 24: 467-500. - 49.
Garros C., Harbach R.E., and Manguin S. Systematics and biogeographical implications of the phylogenetic relationships between members of the Funestus and Minimus Groups of Anopheles (Diptera: Culicidae). Journal of Medical Entomology 2005; 42: 7-18. - 50.
Zarowiecki M. Speciation and species delineation in the Pyretophorus Series of Anopheles mosquitoes. University of Manchester PhD thesis 2009. - 51.
Guo Z., Peng S., Hao Q. , et al. Late Miocene–Pliocene development of Asian aridification as recorded in the Red-Earth Formation in northern China. Global and Planetary Change 2004; 41: 135-145. - 52.
Haffer J. Speciation in Amazonian forest birds. Science 1969; 165: 131-137. - 53.
Chandler M., Rind D., and Thompson R. Joint investigations of the middle Pliocene climate II: GISS GCM Northern Hemisphere results. Global and Planetary Change 1994; 9: 197-219. - 54.
Cronin T.M., Kitamura A., Tkeya N. , et al. Late Pliocene climate change 3.4-2.3 Ma: paleoceanographic record from the Yabuta Formation, Sea of Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 1994; 108: 437-455. - 55.
Ravelo A.C., Andreasen D.H., Lyle M., Lyle A.O., and Wara M.W. Regional climate shifts caused by gradual global cooling in the Pliocene epoch. Nature 2004; 429: 263-267. - 56.
Tougard C. Biogeography and migration routes of large mammal faunas in South–East Asia during the Late Middle Pleistocene: focus on the fossil and extant faunas from Thailand. Palaeogeography, Palaeoclimatology, Palaeoecology 2001; 168: 337-358. - 57.
Hope G., Kershaw A.P., van der Kaars S. , et al. History of vegetation and habitat change in the Austral-Asian region. Quaternary International 2004; 118-119: 103-126. - 58.
Brandon-Jones D. The Asian Colobinae (Mammalia: Cercopithecidae) as indicators of Quaternary climatic change. Biological Journal of the Linnean Society 1996; 59: 327-350. - 59.
Gathorne-Hardy F.J., Syaukani, Davies R.G., Eggleton P., and Jones D.T. Quaternary rainforest refugia in south-east Asia: Using termites (Isoptera) as indicators. Biological Journal of the Linnean Society 2002; 75: 453-466. - 60.
Colinvaux P.A., De Oliveira P.E., and Bush M.B. Amazonian and neotropical plant communities on glacial time-scales: The failure of the aridity and refuge hypotheses. Quaternary Science Reviews 2000; 19: 141-169. - 61.
Colinvaux P.A., Irion G., Raesaenen M.E., and Bush M.B. Geological and paleoecological data falsify the Haffer & Prance refuge hypothesis of Amazonian speciation. Amazoniana 2001; 16: 609-646. - 62.
Mayle F.E., Beerling D.J., Gosling W.D., and Bush M.B. Responses of Amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philosophical Transactions of the Royal Society B 2004; 359: 499–514. - 63.
Morgan K., Linton Y.-M., Somboon P. , et al. Inter-specific gene flow dynamics during the Pleistocene-dated speciation of forest-dependent mosquitoes in Southeast Asia. Molecular Ecology 2010; 19: 2269 - 2285. - 64.
Morgan K. Determining the processes generating biodiversity in Southeast Asia using Anopheles mosquitoes. University of Manchester PhD thesis 2009. - 65.
Dusfour I., Michaux J.R., Harbach R.E., and Manguin S. Speciation and phylogeography of the Southeast Asian Anopheles sundaicus complex. Infection, Genetics and Evolution 2007; 7: 484-493. - 66.
Sathiamurthy E. and Voris H.K. Maps of holocene sea level transgression and submerged lakes on the Sunda Shelf. The Natural History Journal of Chulalongkorn University 2006; Supplement 2: 1-43. - 67.
Walton C., Handley J.M., Collins F.H. , et al. Population Structure and Population History ofAnopheles dirus Mosquitoes in Southeast Asia. Molecular Biology and Evolution 2000; 17: 962-974. - 68.
Chen B., Pedro P.M., Harbach R.E. , et al. Mitochondrial DNA variation in the malaria vectorAnopheles minimus across China, Thailand and Vietnam: evolutionary hypothesis, population structure and population history. Heredity 2011; 106: 241–252. - 69.
Currat M., Ray N., and Excoffier L. SPLATCHE: a program to simulate genetic diversity taking into account environmental heterogeneity. Molecular Ecology Notes 2004; 4: 139-142. - 70.
Hewitt G.M. Genetic consequences of climatic oscillations in the Quaternary. Philosofical Transactions of the Royal Society of London, Series B, biological Sciences 2004; 359: 183-195. - 71.
Hewitt G.M. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 1996; 58: 247-276. - 72.
Chen B., Harbach R.E., and Butlin R.K. Genetic variation and population structure of the mosquito Anopheles jeyporiensis in southern China. Molecular Ecology 2004; 13: 3051-3056. - 73.
Amerasinghe P.H., Amerasinghe F.P., Konradsen F., Fonseka K.T., and Wirtz R.A. Malaria vectors in a traditional dry zone village in Sri Lanka. The American Journal of Tropical Medicine and Hygiene 1999; 60: 421-9. - 74.
Bird M.I., Taylor D., and Hunt C. Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Science Reviews 2005; 24: 2228-2242 - 75.
Ziegler T., Abegg C., Meijaard E. , et al. Molecular phylogeny and evolutionary history of Southeast Asian macaques forming theM. silenus group Molecular Phylogenetics and Evolution 2007; 42: 807-816. - 76.
Sallum M.A.M., Foster P.G., Li C., Sithiprasasna R., and Wilkerson R.C. Phylogeny of the Leucosphyrus Group of Anopheles (Cellia ) (Diptera: Culicidae) based on mitochondrial gene sequences. Annals of the Entomological Society of America 2007; 100: 27-35. - 77.
Moritz C., Patton J.L., Schneider C.J., and Smith T.B. Diversification of rainforest faunas: an integrated molecular approach. Annual Review of Ecology and Systematics 2000; 31: 533–563. - 78.
Norman J.A., Rheindt F.E., Rowe D.L., and Christidis L. Speciation dynamics in the Australo-Papuan Meliphaga honeyeaters Molecular Phylogenetics and Evolution 2007; 42: 80-91. - 79.
Trung H.D., Bortel W.V., Sochantha T. , et al. Behavioural heterogeneity ofAnopheles species in ecologically different localities in Southeast Asia: a challenge for vector control. Tropical Medicine & International Health 2005; 10: 251-262. - 80.
Scanlon J.E., Reid J.A., and Cheong W.H. Ecology of Anopheles vectors of malaria in the Oriental region. Ent. med., 1968; 6: 237 - 246. - 81.
Walton C., Sharpe R.G., Pritchard S.J., Thelwell N.J., and Butlin R.K. Molecular identification of mosquito species. Biological Journal of the Linnean Society 1999; 68: 241-256. - 82.
Walton C., Somboon P., O'Loughlin S.M. , et al. Genetic diversity and molecular identification of mosquito species in theAnopheles maculatus group using the ITS2 region of rDNA. Infection, Genetics and Evolution 2007; 7: 93-102. - 83.
Walton C., Somboon P., Harbach R.E. , et al. , Molecular identification of mosquito species in theAnopheles annularis group in southern Asia. Medical and Veterinary Entomology 2007; 21: 30-35. - 84.
Phuc H.K., Ball A.J., Son L. , et al. Multiplex PCR assay for malaria vectorAnopheles minimus and four related species in the Myzomyia Series from Southeast Asia. Medical and Veterinary Entomology 2003; 17: 423-428. - 85.
Sharpe R.G., Hims M.M., Harbach R.E., and Butlin R.K. PCR-based methods for identification of species of the Anopheles minimus group: allele-specific amplification and single-strand conformation polymorphism. Medical and Veterinary Entomology 1999; 13: 265-273. - 86.
Walton C., Handley J.M., Kuvangkadilok C. , et al. Identification of five species of theAnopheles dirus complex from Thailand, using allele-specific polymerase chain reaction. Medical and Veterinary Entomology 1999; 13: 24-32. - 87.
Wu C.-I. and Ting C.-T. Genes and speciation. Nature Reviews Genetics 2000; 5: 114-122. - 88.
Emelianov I., Marec F., and Mallet J. Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proceedings of the Royal Society of London. Series B: Biological Sciences 2004; 271: 97-105. - 89.
Via S. Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2012; 367: 451-460. - 90.
Gray E.M., Rocca K.A., Costantini C., and Besansky N.J. Inversion 2La is associated with enhanced desiccation resistance in Anopheles gambiae . Malaria journal 2009; 8: 215. - 91.
Torre A.D., Merzagora L., Powell J.R., and Coluzzi M. Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae Complex. Genetics 1997; 146: 239–244. - 92.
Reidenbach K.R., Neafsey D.E., Costantini C. , et al. Patterns of genomic differentiation between ecologically differentiated M and S forms ofAnopheles gambiae in West and Central Africa. Genome Biology and Evolution 2012; 4: 1202-1212. - 93.
Weetman D., Wilding C.S., Steen K., Pinto J., and Donnelly M.J. Gene flow–dependent genomic divergence between Anopheles gambiae M and S forms. Molecular Biology and Evolution 2012; 29: 279-291. - 94.
Marko P.B. and Hart M.W. The complex analytical landscape of gene flow inference. Trends in Ecology & Evolution 2011; 26: 448-456. - 95.
Balkenhol N., Gugerli F., Cushman S. , et al. Identifying future research needs in landscape genetics: where to from here? Landscape Ecology 2009; 24: 455-463. - 96.
Storfer A., Murphy M.A., Spear S.F., Holderegger R., and Waits L.P. Landscape genetics: where are we now? Molecular Ecology 2010; 19: 3496-3514. - 97.
Emaresi G., Pellet J., Dubey S., Hirzel A., and Fumagalli L. Landscape genetics of the Alpine newt ( Mesotriton alpestris ) inferred from a strip-based approach. Conservation Genetics 2011; 12: 41-50. - 98.
Galpern P., Manseau M., and Wilson P. Grains of connectivity: analysis at multiple spatial scales in landscape genetics. Molecular Ecology 2012; 21: 3996-4009. - 99.
Hancock A.M., Brachi B., Faure N. , et al. Adaptation to climate across theArabidopsis thaliana genome. Science 2011; 334: 83-86. - 100.
Hohenlohe P.A., Bassham S., Etter P.D. , et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 2010; 6: e1000862. - 101.
Herrera C.M. and Bazaga P. Population-genomic approach reveals adaptive floral divergence in discrete populations of a hawk moth-pollinated violet. Molecular Ecology 2008; 17: 5378-5390. - 102.
Holt R.A., Subramanian G.M., Halpern A. , et al. The genome sequence of the malaria mosquitoAnopheles gambiae . Science 2002; 298: 129-149. - 103.
Broad Institute. Genome analysis of vectorial capacity in major Anopheles vectors of malaria parasites. http://www.broadinstitute.org/annotation/genome/anopheles.1/Info.html (accessed 4 January 2013). - 104.
Weill M., Chandre F., Brengues C. , et al. The kdr mutation occurs in the Mopti form ofAnopheles gambiae s.s. through introgression. Insect Molecular Biology 2000; 9: 451-455. - 105.
Petit R.J. and Excoffier L. Gene flow and species delimitation. Trends in Ecology and Evolution 2009; 24: 386-393.