Biodiversity Science ›› 2014, Vol. 22 ›› Issue (1): 40-50.doi: 10.3724/SP.J.1003.2014.13144

Special Issue: From Genome to Diversity

• Orginal Article • Previous Article     Next Article

Diversification of Southeast Asian mammals during the Quaternary glaciation: insights from the genomic era

Lin Miao, Shu-Jin Luo*()   

  1. College of Life Sciences, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871
  • Received:2013-06-24 Accepted:2013-12-25 Online:2014-02-10
  • Luo Shu-Jin E-mail:luo.shujin@pku.edu.cn

Southeast (SE) Asia refers to the region east to the Philippine islands, west to the Indian subcontinent, north to central China and south to the Sunda islands. This region includes six of the world’s 25 biodiversity hotspots and is of strategic significance in global biodiversity conservation. The complicated geological and climatological history of this region has resulted in extremely high species diversity and endemism. Two classic biogeographic boundaries, the Wallace Line and the Isthmus of Kra, divide SE Asia into the Indochinese province to the north and Sundaic province to the south. Because the Indochinese and Sundaic provinces are connected today through the Malay Peninsula and the Sunda shelf was exposed for the majority of time during the Quaternary glaciation, previous biogeographic studies have proposed that gene flow occurred between mainland and different island populations causing low divergence in the region. However, recent molecular genetic studies have reported that migration of terrestrial mammal populations was not as great as previously thought due to ecological restrictions. Thus, deep vicariant divergence was present in several mammals as early as two million years ago and appeared not to have been affected by gene flow following the formation of land bridges during later glacial periods. Furthermore, the super eruption of the Toba volcano in Sumatra about 73,000 years ago may have intensified divergence. A literature review has indicated three hierarchical levels present in the formation of mammalian diversity in SE Asia. These include populations between the Indochinese and Sundaic provinces which diverged millions of years ago, populations among the Sunda Islands which diverged hundreds of thousands of years ago, and Late Pleistocene biogeographic events causing demographic changes. Most of the previous population genetic studies on SE Asia mammals were based on analyses of mitochondrial or nuclear DNA data. Recent advances in population genomics provide new opportunities to obtain a comprehensive understanding of the demographic history and speciation processes of SE Asian mammals during the Quaternary glaciation.

Key words: Southeast Asia, biogeography, mammal, population genomics, Quaternary

Fig. 1

Major biogeographic divisions and speciation events in Southeast (SE) Asia. The Wallace Line and Isthmus of Kra divide SE Asia into Indochinese and Sundaic provinces (Tougard, 2001). Distribution ranges of the species and boundaries between the congeneric species are shown (data from IUCN, 2013): Manis pentadactyla and M. javanica, Macaca leonine and M. nemestrina, Neofelis nebulosa and N. diardi, and Pardofelis temminckii and P. badia. Ancestral populations of each of these pairs of species retracted into remanent refugia during dramatic geological or geographic events (e.g., glacial periods), leading to subsequent allopatric speciation. When suitable climate and habitats returned (e.g., interglacial periods), such populations (species) expanded out of fragmented refugia in the south and north and converged on current range boundaries, although the exact location of such boundaries varied by species."

Appendix I

Case studies of population genetics and biogeography research of Southeast Asian mammals"

中文名 拉丁名 分布区域 研究概况 参考文献
马来貘 Tapirus indicus 缅甸、泰国、马来半岛、苏门答腊岛 目前无亚种划分。另外3种貘均分布于美洲, 与马来貘分化时间超过20 Ma。 Lynam et al., 2008; Steiner & Ryder, 2011
苏门答腊犀牛 Dicerorhinus sumatrensis 历史上曾经分布于印度半岛、中南半岛和巽他群岛, 目前仅分布于婆罗洲、苏门答腊岛和马来半岛南部 共3个亚种, D. s. lasiotis分布于印度半岛和缅甸, D. s. sumatrensis分布于泰国、马来半岛和苏门答腊岛, D. s. harrissoni分布于婆罗洲。 van Strien et al., 2008b
爪哇犀牛 Rhinoceros sondaicus 历史上曾经分布于印度半岛、中南半岛和巽他群岛, 目前仅分布于越南和爪哇岛 共3个亚种, R. s. inermis分布于印度半岛和缅甸, R. s. annamiticus分布于越南、老挝、柬埔寨和泰国东部, R. s. sondaicus分布于泰国、马来半岛、苏门答腊岛和爪哇岛。 van Strien et al., 2008a
Capricornis milneedwardsii
Capricornis sumatraensis
C. milneedwardsii分布于中国南部及克拉地峡以北的中南半岛; C. sumatraensis分布于克拉地峡以南的马来半岛及苏门答腊岛 Capricornis的分类尚不是很清楚, 目前分为6个种, 此处列出的2个种分布于印支区和巽他区, 并且其物种的分布以克拉地峡为分界线。 Duckworth et al., 2008a, b
Rusa unicolor 印度半岛、斯里兰卡、中国南部、中南半岛、巽他群岛 Rusa unicolor分为7个亚种, 其中R. u. unicolor分布于印度半岛与斯里兰卡, R. u. cambojensis分布于中南半岛, R. u. equina分布于苏门答腊岛, R. u. brookei分布于婆罗洲。 Timmins et al., 2008b; Leslie, 2011
印度野牛 Bos gaurus 印度半岛、中南半岛 传统上分为3个亚种, B. g. gaurus分布于印度半岛, B. g. readei分布于克拉地峡以北的中南半岛, B. g. hubbacki分布于克拉地峡以南的马来半岛。基于形态学的最新研究认为B. g. readeiB. g. hubbacki应合并为1个亚种B. g. laosiensis, 基于核基因估算亚种间分化时间约为1.85 Ma。 Duckworth et al., 2008d; Hassanin et al., 2012
爪哇野牛 Bos javanicus 中南半岛、巽他群岛 传统上分为3个亚种, B. j. javanicus分布于爪哇岛和巴厘岛, B. j. lowi分布于婆罗洲, B. j. birmanicus分布于中南半岛, 但B. j. lowi亚种的存在受到质疑。染色体研究发现B. j. birmanicus 2n=56, B. j. birmanicus 2n=60, 基于核基因估算亚种间分化时间约为0.75 Ma。 Ropiquet et al., 2008; Timmins et al., 2008a; Hassanin et al., 2012
Maxomys surifer 中南半岛和巽他群岛 通过线粒体控制区与细胞色素B基因建树, 印支区种群为一支、克拉地峡以南的马来半岛与苏门答腊岛种群为一支、婆罗洲种群为一支, 估算其分化时间为数百万年(使用不同的突变速率结果差异较大)。 Gorog et al., 2004
Maxomys whiteheadi 巽他群岛和克拉地峡以南的马来半岛 通过线粒体控制区与细胞色素B基因建树, 克拉地峡以南的马来半岛与苏门答腊岛种群为一支、婆罗洲种群为一支, 估算其分化时间为数十万年到数百万年(使用不同的突变速率结果差异较大)。 Gorog et al., 2004
Leopoldamys sabanus 中南半岛和巽他群岛 通过线粒体控制区与细胞色素B基因建树, 印支区种群为一支、克拉地峡以南的马来半岛与苏门答腊岛种群为一支、婆罗洲种群为一支, 估算其分化时间为数百万年(使用不同的突变速率结果差异较大)。 Gorog et al., 2004
亚洲象 Elephas maximus 印度半岛、斯里兰卡、中南半岛和巽他群岛 存在两组线粒体单倍型, 巽他区仅分布β单倍型组, 其他地区α和β两组单倍型均有分布, α组和β组分化时间约1.88 Ma。 Fernando et al., 2000; Fleischer et al., 2001; Vidya et al., 2009
巽他鼯猴 Galeopterus variegatus 中南半岛和巽他群岛 线粒体与核基因分析显示马来半岛和爪哇岛的鼯猴分化时间分别为约5.4 Ma和约3.9 Ma。 Janecka et al., 2008
小毛猬 Hylomys suillus 中南半岛和巽他群岛 使用细胞色素B基因建树, 印支区和巽他区的单倍型分为两组, 巽他区的苏门答腊岛和马来半岛分在一起, 爪哇岛和婆罗洲分在一起。印支区和巽他区单倍型分化时间为数百万年(不同校准点结果不同, 分别为3.9 Ma、5.0 Ma、18.1 Ma)。 Ruedi & Fumagalli, 1996
中国穿山甲
马来穿山甲
Manis pentadactyla
Manis javanica
中国穿山甲分布于中国南部地区, 马来穿山甲分布于中南半岛和巽他群岛 已知不同物种。 IUCN, 2013
北方豚尾猕猴
南方豚尾猕猴
Macaca leonine
Macaca nemestrina
北方豚尾猕猴分布于印支区, 南方豚尾猕猴分布于巽他区 两种豚尾猕猴原先为M. nemestrina的2个亚种, 后分为2个独立的种, 两种豚尾猕猴在素叻他尼–甲米(Surat Thani-Krabi)区带内同域分布并且有杂交, 两种豚尾猕猴具有明显的形态学差异, 使用线粒体与核基因多位点序列估算分化时间大于1 Ma。 Fabre et al., 2009; Malaivijitnond et al., 2012
食蟹猴
普通猕猴
Macaca fascicularis
Macaca mulatta
普通猕猴分布于中国南部、中南半岛北部、印度半岛北部, 食蟹猴分布于中南半岛、巽他群岛和菲律宾群岛 两种猕猴在中南半岛北部同域分布, Y染色体和线粒体遗传标记显示两种猕猴存在基因交流, 尽管使用线粒体与核基因多位点序列估算分化时间约2 Ma, 但结果很可能受到个体来源的影响。食蟹猴本身至少存在10个亚种, 使用线粒体D-loop区建树, 食蟹猴按样品来源分为中南半岛、巽他群岛和菲律宾群岛三组。 Tosi et al., 2002; Smith et al., 2007; Street et al., 2007; Shiina et al., 2010
戴帽长臂猿
白掌长臂猿
Hylobates pileatus
Hylobates lar
戴帽长臂猿主要分布于泰国东南及柬埔寨西部, 白掌长臂猿主要分布于泰国中西部、缅甸东部和整个马来半岛及苏门答腊岛北部 在泰国中部两物种同域分布并存在杂交, 线粒体基因组估算两物种分化时间约2.9 Ma。白掌长臂猿根据形态差异划分为5个亚种, 但需要进一步的研究。 Brockelman & Geissmann, 2008; Brockelman et al., 2008; Chan et al., 2010
苏门答腊红毛猩猩
婆罗洲红毛猩猩
Pongo abelii

Pongo pygmaeus
苏门答腊猩猩分布于苏门答腊岛, 婆罗洲猩猩分布于婆罗洲 两种猩猩原先为P. pygmaeus的2个亚种, 后分为2个独立的种, 全基因组DNA序列估算两种猩猩分化时间约为40 Ma。 Zhi et al., 1996; Locke et al., 2011; Mailund et al., 2011
云豹
巽他云豹
Neofelis nebulosa
Neofelis diardi
云豹分布于喜马拉雅山南麓、中国南部、中南半岛; 巽他云豹分布于苏门答腊岛和婆罗洲 两种云豹原先为N. nebulosa的2个亚种, 后分为2个独立的种, 基于线粒体、核基因和微卫星遗传学标记的研究显示两种云豹存在较大遗传差异, 估算分化时间为1.41 Ma。对巽他云豹的进一步研究显示苏门答腊岛和婆罗洲的种群存在明显的形态学和遗传学差异, 并分为2个亚种, 估算分化时间为120-400 ka。 Buckley-Beason et al., 2006; Kitchener et al., 2006; Wilting et al., 2007, 2011
Panthera tigris 虎历史上曾经广泛分布于亚洲, 现分布于东南亚的有3个亚种: 印支虎(P. t. corbetti, 分布于印支区)、马来虎(P. t. jacksoni, 分布于克拉地峡以南的马来半岛)和苏门答腊虎(P. t. sumatrae, 分布于苏门答腊岛) 线粒体基因估算所有现存亚种最近共同祖先的时间为72-108 ka, 东南亚分布的不同亚种间体现出明显的遗传学差异。 Luo et al., 2004
Panthera pardus 广泛分布于旧大陆 豹没有体现出从印支区到巽他区明显的遗传差异。 Uphyrkina et al., 2001
渔猫 Prionailurus viverrinus 印度半岛、斯里兰卡、中南半岛、巽他群岛 地理分布呈不连续性, 马来半岛上无分布, 可能体现了南北种群的历史隔离。
亚洲金猫
婆罗洲金猫
Pardofelis temminckii
Pardofelis badia
亚洲金猫分布于中国南部、中南半岛、苏门答腊岛; 婆罗洲金猫分布于婆罗洲 婆罗洲金猫被认为是金猫在婆罗洲的特化种, 二者分化时间大约4.3 Ma。 Johnson et al., 2006
Cuon alpinus 印度半岛、中南半岛、巽他群岛 基于线粒体序列的系统发生分析显示, 印度恒河以南的单倍型聚为一支, 印度恒河以北以及缅甸、泰国、马来西亚的单倍型聚为一支, 苏门答腊岛和爪哇岛的单倍型聚为一支。 Iyengar et al., 2005; Durbin et al., 2008
马来熊 Helarctos malayanus 印度半岛北部、中南半岛及巽他群岛 基于形态学的研究发现婆罗洲的个体与其他分布区的差异较大, 故分为2个亚种, H. m. euryspilus(婆罗洲)与H. m. malayanus(其他地区)。 Meijaard, 2004; Fredriksson et al., 2008
果子狸 Paguma larvata 喜马拉雅山脉南麓、中国南部、中南半岛、巽他群岛、日本 基于线粒体控制区和细胞色素B的序列分析表明果子狸遗传多样性较低, 但可以大致分为3个单倍型组: 中国组、印支组和巽他组。 Duckworth et al., 2008c; Patou et al., 2009
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