Molecular Phylogenetics and Biogeography of the Neocellia Series of Anopheles Mosquitoes in the Oriental Region
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CORE Metadata, citation and similar papers at core.ac.uk Provided by UM Digital Repository Molecular Phylogenetics and Evolution 52 (2009) 588–601 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogenetics and biogeography of the Neocellia Series of Anopheles mosquitoes in the Oriental Region Katy Morgan a, Samantha M. O’Loughlin a,b, Fong Mun-Yik a,c, Yvonne-Marie Linton d Pradya Somboon e, Sein Min f, Pe Than Htun f, Simone Nambanya g, Indira Weerasinghe h Tho Sochantha i, Anil Prakash j, Catherine Walton a,* a Faculty of Life Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, UK b NERC Centre for Population Biology, Imperial College, London, UK c University of Malaya, Kuala Lumpur, Malaysia d Department of Entomology, The Natural History Museum, London, UK e Department of Parasitology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand f Department of Medical Research, Yangon, Myanmar g Centre of Malariology, Parasitology and Entomology, Vientiane, Laos h Institute of Medical Research, Colombo, Sri Lanka i National Centre for Malaria Control, Parasitology and Entomology, Phnom Penh, Cambodia j Regional Medical Research Centre, Dibrugarh, Assam, India article info abstract Article history: Molecular studies of population divergence and speciation across the Oriental Region are sparse, despite Received 29 July 2008 the region’s high biodiversity and extensive Pliocene and Pleistocene environmental change. A molecular Revised 28 January 2009 phylogenetic study of the Neocellia Series of Anopheles mosquitoes was undertaken to identify patterns of Accepted 29 January 2009 diversification across the Oriental Region and to infer the role of Pleistocene and Pliocene climatic change. Available online 6 February 2009 A robust phylogeny was constructed using CO2 and ND5 mitochondrial genes and ITS2 and D3 nuclear ribosomal markers. Bayesian analysis of mitochondrial genes was used to date divergence events. The Keywords: repeated contraction and expansion of forest habitat resulting from Pleistocene climatic fluctuations Anopheles appears to have had a substantial impact on intraspecific diversification, but has not driven speciation Southeast Asia Phylogeography within this group. Primarily early to mid Pliocene speciation was detected within the Annularis Group, Biogeography whereas speciation within the Maculatus and Jamesii Groups occurred during the mid and late Pliocene. Pleistocene climatic change Both allopatric divergence driven by late Pliocene environmental changes and ecological adaptation, Allopatric speciation involving altitudinal replacement and seasonality, are likely to have influenced speciation in the Macul- Ecological speciation atus Group. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction Region, which shares similar flora and fauna to the Southeast Asian hotspots. Research on Oriental biodiversity has been neglected rel- Southeast Asia is an important region in terms of global biodi- ative to that of other regions, and consequently little is understood versity, containing four of the 25 global biodiversity hotspots de- of the processes underlying the generation of diversity across the scribed by Myers et al. (2000). These are the island regions of region (Sodhi et al., 2004). The mosquito genus Anopheles is species Sundaland, Wallacea and the Philippines, and the mainland region rich within the Oriental Region, containing multiple sibling species of Indo-Burma. Together these regions contain an estimated 9.7% complexes that occupy a wide variety of ecological niches (Reid, of the world’s known endemic plant species and 8.3% of the known 1968; Collins and Paskewitz, 1996; Foley et al., 2007a). The genus endemic vertebrate species, the majority of which are concen- Anopheles is therefore a good model for studying the distribution of trated within tropical forest habitat (Taylor et al., 1999; Myers biodiversity and the factors influencing population divergence and et al., 2000; Brook et al., 2003). Sri Lanka and the Western Ghats speciation across the region. of India represent an additional biodiversity hotspot in the Oriental Numerous hypotheses have been put forward to explain the species richness of the tropics, a phenomenon that has been dem- onstrated in mosquitoes (Foley et al., 2007a), as well as numerous * Corresponding author. Address: Michael Smith Building, Faculty of Life other taxa (for reviews see Gaston, 2000; Hill and Hill, 2005; Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, UK. Fax: +44 0161 275 5082. Mittlebach et al., 2007). One of the oldest and most debated of E-mail address: [email protected] (C. Walton). these hypotheses is the refuge model, originally proposed by Haffer 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.01.022 K. Morgan et al. / Molecular Phylogenetics and Evolution 52 (2009) 588–601 589 (1969). This states that the repeated expansion and contraction of (see Fig. 1), leading to increased inland aridity (Heaney, 1991). tropical forest in response to climatic fluctuation resulted in allo- Consequently, whereas Pleistocene tropical forest cover across patric divergence and eventual speciation. The Pleistocene, with South America and Africa was primarily affected by temperature its alternating cool, arid glacial periods and warm, moist intergla- and precipitation, sea level fluctuations are thought to have had cial periods, might therefore be expected to generate biodiversity an equal or even greater impact on tropical forest cover across according to the refuge hypothesis. However, since the majority Southeast Asia (Heaney, 1991). Palaeoenvironmental reconstruc- of speciation events in a wide range of tropical vertebrate and tions of the last glacial maximum indicate that the dominant trop- invertebrate taxa pre-date the Pleistocene (Moritz et al., 2000; ical forest habitat of interglacial periods was largely replaced by Burns and Naoki, 2004; Bush, 2005; Hill and Hill, 2005; Perez- grassland and savannah habitat during glacial periods, particularly Eman, 2005), the importance of Pleistocene climatic change in gen- in mainland Southeast Asia (Heaney, 1991; Hope et al., 2004; erating tropical diversity remains unclear. Rather than allopatric White et al., 2004). fragmentation, the importance of environmentally driven adapta- Molecular studies indicate that forest fragmentation in the Sun- tion in generating tropical biodiversity has been highlighted in sev- da Shelf region, encompassing insular and mainland Southeast eral recent studies across South America, Africa and Australia Asia, led to population fragmentation and divergence in both ro- (Smith et al., 1997, 2005; Schneider et al., 1999; Ogden and Thorpe, dent (Gorog et al., 2004) and plant taxa (Cannon and Manos, 2002). Models of ecological speciation that have been proposed in- 2003). Within the insular Sundaic region, speciation within the clude the gradient (reviewed in Moritz et al., 2000) and altitudinal Macaca silensis Group of macaques (Ziegler et al., 2007) and the replacement models (Norman et al., 2007). Pteruthius genus of shrike babblers (Reddy, 2008) is thought to The role of Pleistocene climatic change in driving speciation in have been triggered by the allopatric fragmentation of populations South America and Africa continues to be debated (Moritz et al., on different islands, as rising sea levels submerged land bridges be- 2000; Pennington et al., 2004). It has been suggested that the Pleis- tween them. On the mainland, the interglacial expansion of tropi- tocene refuge model is a particularly implausible explanation for cal forest from refugial regions has been suggested as the cause of the generation of Amazonian biodiversity due to accumulating pal- population expansions in Anopheles mosquito species (Walton aeoecological evidence indicating that this region remained largely et al., 2001; Chen et al., 2004; O’Loughlin et al., 2008) and in Simu- forested during glacial periods (Mayle et al., 2004). In contrast, lium blackfly species (Pramual et al., 2005). However, the question Pleistocene climatic change may have had a particularly strong of whether allopatric divergence associated with habitat fragmen- environmental influence in Southeast Asia. Southeast Asia is un- tation has resulted in speciation within forest taxa within the ique among tropical regions with regard to the dramatic effect of mainland Oriental Region is unanswered and is a question we ad- changes in Pleistocene sea level, which rose and fell during inter- dress here. glacial and glacial periods, respectively (Voris, 2000). This caused The Neocellia Series (Christophers, 1924) of the Anopheles sub- the repeated destruction and formation of land bridges between genus Cellia comprises some 31 currently recognised species (Har- the mainland and island regions, with the large landmass of the bach, 2004; Gad et al., 2006). The majority of species in the Sunda Shelf being exposed during periods of lowered sea level Neocellia Series are found within the Oriental Region; however Fig. 1. Relief map of Southeast Asia indicating the locations of sample sites (see Table 1). The smooth black line indicates the approximate landmass configuration when sea levels were 120 m below their current level, the lowest levels reached during the Pleistocene (data taken from Voris, 2000). 590 K. Morgan et al. / Molecular Phylogenetics and Evolution