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Range-Wide Mtdna Phylogeography Yields Insights Into the Origins of Asian Elephants T Proc. R. Soc. B doi:10.1098/rspb.2008.1494 Published online Range-wide mtDNA phylogeography yields insights into the origins of Asian elephants T. N. C. Vidya1,2,*, Raman Sukumar1 and Don J. Melnick3 1Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India 2Evolutionary and Organismal Biology Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore 560 064, India 3Department of Ecology, Evolution and Environmental Biology, Columbia University, 1200 Amsterdam Avenue, New York, NY 10027, USA Recent phylogeographic studies of the endangered Asian elephant (Elephas maximus) reveal two highly divergent mitochondrial DNA (mtDNA) lineages, an elucidation of which is central to understanding the species’s evolution. Previous explanations for the divergent clades include introgression of mtDNA haplotypes between ancestral species, allopatric divergence of the clades between Sri Lanka or the Sunda region and the mainland, historical trade of elephants, and retention of divergent lineages due to large population sizes. However, these studies lacked data from India and Myanmar, which host approximately 70 per cent of all extant Asian elephants. In this paper, we analyse mtDNA sequence data from 534 Asian elephants across the species’s range to explain the current distribution of the two divergent clades. Based on phylogenetic reconstructions, estimates of times of origin of clades, probable ancestral areas of origin inferred from dispersal–vicariance analyses and the available fossil record, we believe both clades originated from Elephas hysudricus. This probably occurred allopatrically in different glacial refugia, the a clade in the Myanmar region and the b clade possibly in southern India–Sri Lanka, 1.6–2.1 Myr ago. Results from nested clade and dispersal–vicariance analyses indicate a subsequent isolation and independent diversification of the b clade in both Sri Lanka and the Sunda region, followed by northward expansion of the clade. We also find more recent population expansions in both clades based on mismatch distributions. We therefore suggest a contraction–expansion scenario during severe climatic oscillations of the Quaternary, with range expansions from different refugia during warmer interglacials leading to the varying geographical overlaps of the two mtDNA clades. We also demonstrate that trade in Asian elephants has not substantially altered the species’s mtDNA population genetic structure. Keywords: phylogeography; divergent mitochondrial clades; Pleistocene refugia; elephant trade; Elephas fossils 1. INTRODUCTION the differentiation of the genus Loxodonta and was present The Asian elephant (Elephas maximus) is endangered, with duringthe Early Pliocene (Maglio 1973). A recent molecular a wild population of 41 000–52 000 individuals in 6 per study by Rohland et al.(2007)has estimated that Loxodonta cent of the range occupied 4000 years ago (Sukumar and the Mammuthus–Elephas lineage diverged 7.6 (95% 2003). It is the sole surviving species of the Proboscidea in CI 6.6–8.8) million years ago (Myr ago). The fossil record Asia. Studies of its evolutionary history and phylogeo- alone suggests that this split is more recent (ca 5.5 Myr ago) graphy are recent enough that their results have not (see electronic supplementary material 1). A derivative of the been integrated into conservation action, although the early Elephas ekorensis–Elephas recki complex colonized flagship role of the elephant for broader conservation in Asia and is thought to have given rise to Elephas planifrons Asia has been recognized (Duckworth & Hedges 1998; and Elephashysudricus (Maglio 1973). The earliest records of Sukumar 2003). Fossils and molecular analyses are both species were found in the Siwalik Hills in the northern valuable in reconstructing evolutionary history, so while Indian subcontinent, E. planifrons appearing ca 3.6 Myr ago fossil data for the Elephantidae are limited in Asia, and E. hysudricus ca 2.7 Myr ago (see Nanda 2002). Late in increasing molecular data and new ways of evaluating the Early Pleistocene, Elephas namadicus, another derivative them are providing a clearer picture of the species’ of E. recki, colonized Asia and displaced the earlier Elephas phylogeography (Fernando et al. 2000, 2003; Fleischer species across a considerable part of their ranges (Maglio et al. 2001; Vidya et al. 2005). 1973) before disappearing in the Late Pleistocene. However, The largest study of fossil elephantid morphology E. hysudricus, which was widespread, is considered (based indicated that the genus Elephas originated in Africa after on dental and cranial evidence) to have given rise to E. maximus in southern Asia ca 0.25 Myr ago (Maglio * Author and address for correspondence: Evolutionary and Orga- nismal Biology Unit, Jawaharlal Nehru Centre for Advanced Scientific 1973)andtoElephas hysudrindicus, a Javan species, ca Research, Bangalore 560 064, India ([email protected]). 0.8–1.0 Myr ago (Maglio 1973; Van den Bergh et al. 1996). Electronic supplementary material is available at http://dx.doi.org/10. Molecular phylogeographic analyses are often based on 1098/rspb.2008.1494 or via http://journals.royalsociety.org. mitochondrial DNA (mtDNA) markers. As mtDNA is Received 14 October 2008 Accepted 28 October 2008 1 This journal is q 2008 The Royal Society 2 T. N. C. Vidya et al. Asian elephant phylogeography Bhutan (13) NE India (63) Lao PDR (14) AC 0.538 AC 0.619 AB 0.143 AE 0.385 AH 0.349 AD 0.286 BL 0.077 BL 0.032 AE 0.500 Nepal H 0.603±0.0885 H 0.479±0.0435 BQ 0.071 p Vietnam (25) 0.007±0.0043 p 0.003±0.0020 H 0.692±0.0942 N India (6) p 0.005±0.0033 AA 0.040 AC 1.000 AB 0.280 H,p 0 AD 0.120 China C India (12) AJ 0.200 BC 0.250 AK 0.280 BL 0.750 BO 0.080 Bangladesh ± H 0.409±0.1333 H 0.813 0.0389 ± p 0.001±0.0008 Myanmar (24) p 0.006 0.0037 AF 0.083 Cambodia (1) Sri Lanka (82) Thailand Nilgiris (159) S India AH 0.125 AB 1.000 BN 1.000 AE 0.232 AI 0.042 Borneo (20) H,p 0 AF 0.012 BH 0.292 AG 0.098 BL 0.292 BD 1.000 Anamalai- BQ 0.125 H,p 0 Periyar (67) BH 0.061 BI 0.037 BW 0.042 Peninsular Malaysia (14) BA 0.060 BJ 0.037 H 0.823±0.0458 BP 0.071 BB 0.015 BK 0.012 p 0.014±0.0074 BQ 0.786 BF 0.896 BL 0.244 BP 0.059 BU 0.071 BL 0.030 BR 0.176 0.196±0.0637 BM 0.012 BV 0.071 H ± p <0.000 BN 0.024 BS 0.176 H 0.396 0.1588 BO 0.122 BT 0.441 p 0.003±0.0021 BP 0.110 BU 0.147 H 0.853±0.0190 H 0.740±0.0522 p 0.016±0.0083 p 0.004±0.0025 Sumatra (34) Figure 1. Present Asian elephant distribution (grey) based on Sukumar (2003) and (for India) Vidya et al. (2005), and the number of individuals sampled (within parentheses), proportions of different haplotypes, and Hˆ and p (expressed as average G 1.96 s.e.) tabled against different populations. Haplotypes beginning with the letter A belong to the a clade and those beginning with the letter B to the b clade. (See electronic supplementary material 2 for more details about figure 1.) maternally inherited, stochastic extinctions of mito- are geographically separated. More specifically, these chondrial lineages through the absence of female offspring hypotheses include: (i) the introgression of mtDNA from are usually the norm unless sufficiently large populations E. namadicus or an alternative species of Elephas to of females exist. The coexistence of divergent lineages of E. maximus (Fernando et al.2000); (ii) allopatric divergence mtDNA within a species is therefore rare and requires an of populations on the mainland giving rise to the a clade and elucidation of the evolutionary and population processes on Sri Lanka giving rise to the b clade, followed by secondary that led to it (Melnick et al. 1993). The Asian elephant has contact and admixture (Fernando et al. 2000); (iii) two such divergent lineages of mtDNA haplotypes or introgression of mtDNA from E. hysudrindicus (in the clades, the ‘a’ (Fernando et al. 2000, 2003) or ‘B’ clade Sunda region), which gave rise to the b clade, into (Hartl et al. 1996; Fleischer et al. 2001) and the ‘b’ or ‘A’ E. maximus, which carried the a clade, followed by extensive clade (we use the a and b terminology here), with a trade in elephants bringing the b clade to Sri Lanka and sequence divergence of approximately 3 per cent. southern India (Fleischer et al. 2001); and (iv) incomplete Haplotypes from these two clades coexist within popu- lineage sorting, or the retention of divergent lineages simply lations, sometimes within small geographical areas owing to large population size (Fleischer et al.2001). (Fernando et al. 2000; Fleischer et al. 2001), unlike Importantly, these hypotheses were based on only four to six other mammalian species, in which divergent clades are samples from India, which hosts approximately 60 per cent usually geographically separate (e.g. Taberlet & Bouvet of the entire Asian elephant population (Sukumar 2003), 1994; Jensen-Seaman & Kidd 2001). Therefore, under- and zero tofive samples from Myanmar, which hosts another standing the coexistence and distribution of the two clades 10 per cent. is vital to understanding Asian elephant evolution. Here, we expand our phylogeographic analysis by Hypotheses to explain the distribution of the two Asian examining mtDNA from 534 Asian elephants across the elephant clades have invoked introgression of mitochondrial species’s range (figure 1), including larger sample sizes haplotypes from another species through hybridization, from India (nZ244) and Myanmar (nZ24).
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