[en] Background: Historical biogeography and evolutionary processes of cave taxa have been widely studied in temperate regions. However, Southeast Asian cave ecosystems remain largely unexplored despite their high scientific interest. Here we studied the phylogeography of Leopoldamys neilli, a cave-dwelling murine rodent living in limestone karsts of Thailand, and compared the molecular signature of mitochondrial and nuclear markers.
Methodology/Principal Findings: We used a large sampling (n = 225) from 28 localities in Thailand and a combination of mitochondrial and nuclear markers with various evolutionary rates (two intronic regions and 12 microsatellites). The evolutionary history of L. neilli and the relative role of vicariance and dispersal were investigated using ancestral range reconstruction analysis and Approximate Bayesian computation (ABC). Both mitochondrial and nuclear markers support a large-scale population structure of four main groups (west, centre, north and northeast) and a strong finer structure within each of these groups. A deep genealogical divergence among geographically close lineages is observed and denotes a high population fragmentation. Our findings suggest that the current phylogeographic pattern of this species results from the fragmentation of a widespread ancestral population and that vicariance has played a significant role in the evolutionary history of L. neilli. These deep vicariant events that occurred during Plio-Pleistocene are related to the formation of the Central Plain of Thailand. Consequently, the western, central, northern and northeastern groups of populations were historically isolated and should be considered as four distinct Evolutionarily Significant Units (ESUs).
Conclusions/Significance: Our study confirms the benefit of using several independent genetic markers to obtain a comprehensive and reliable picture of L. neilli evolutionary history at different levels of resolution. The complex genetic structure of Leopoldamys neilli is supported by congruent mitochondrial and nuclear markers and has been influenced by the geological history of Thailand during Plio-Pleistocene.
Disciplines :
Genetics & genetic processes Zoology
Author, co-author :
Latinne, Alice ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Waengsothorn, Surachit
Rojanadilok, Prateep
Eiamampai, Krairat
Sribuarod, Kriangsak
Michaux, Johan ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Language :
English
Title :
Combined Mitochondrial and Nuclear Markers Revealed a Deep Vicariant History for Leopoldamys neilli, a Cave-Dwelling Rodent of Thailand
Publication date :
31 October 2012
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, San Franscisco, United States - California
Volume :
7
Issue :
10
Pages :
e47670
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Holsinger JR (2005) Vicariance and dispersalist biogeography. In: Culver DC, White WB, editors. Encyclopedia of caves. Amsterdam: Elsevier/Academic Press. pp. 591-599.
Juan C, Guzik MT, Jaume D, Cooper SJB, (2010) Evolution in caves: Darwin's 'wrecks of ancient life' in the molecular era. Mol Ecol 19: 3865-3880.
Peck SB, Finston T, (1993) Galapagos islands troglobites: the questions of tropical troglobites, parapatric distributions with eyed-sister-species, and their origin by parapatric speciation. Mem Biospeol 20: 19-37.
Howarth FG, (1980) The zoogeography of specialized cave animals: a bioclimatic model. Evolution 28: 365-389.
Howarth FG, (1987) The evolution of non-relictual tropical troglobites. Int J Speleol 16: 1-16.
Leys R, Watts C, Cooper SJB, Humphreys WF, (2003) Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57: 2819-2834.
Villacorta C, Jaume D, Oromi P, Juan C, (2008) Under the volcano: phylogeography and evolution of the cave-dwelling Palmorchestia hypogaea (Amphipoda, Crustacea) at La Palma (Canary Islands). BMC Biol 6: 7.
Clements R, Sodhi NS, Schilthuizen M, Ng PKL, (2006) Limestone karsts of southeast Asia: Imperiled arks of biodiversity. Bioscience 56: 733-742.
Vermeulen JJ, Whitten T (1999) Biodiversity and Cultural Property in the Management of Limestone Resources-Lessons from East Asia. Washington (DC):World Bank.
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J, (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
Gillieson D (2005) Karsts of Southeast Asia. In: Gupta A, editor. The Physical Geography of Southeast Asia. Oxford: Oxford University Press. pp. 157-176.
Lekagul B, McNeely JA (1988) Mammals of Thailand. Bangkok: White Lotus Press.
Musser GG, Carleton M (2005) Superfamily Muroidea. In: Wilson DE, Reeder DM, editors. Mammal species of the World: a taxonomic and geographic reference. 3rd edition ed. Baltimore: Johns Hopkins University Press. pp. 894-1531.
Waengsothorn S, Nabhitabhata J, Moochan T, (2007) The ecological distribution of Thai endemic rodents with a new distributional range of Niviventer hinpoon. Thail Nat Hist Mus J 2: 31-42.
Waengsothorn S, Kenthao A, Latinne A, Hugot JP, (2009) Rodents within the Centre for Thai National Reference Collections (CTNRC), past, present and future. Kasetsart J Nat Sci 43: 118-124.
Sket B, (2008) Can we agree on an ecological classification of subterranean animals? J Nat Hist 42: 1549-1563.
Culver DC, Pipan T (2009) The Biology of Caves and Other Subterranean Habitats. Oxford: Oxford University Press.
Lunde DP, Aplin K (2008) Leopoldamys neilli. In: IUCN, editor. IUCN Red List of Threatened Species. Version 2011.2. . Accessed 2012 Oct 4.
Pages M, Chaval Y, Herbreteau V, Waengsothorn S, Cosson JF, et al. (2010) Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evol Biol 10: 184.
Latinne A, Waengsothorn S, Herbreteau V, Michaux J, (2011) Evidence of complex phylogeographic structure for the threatened rodent Leopoldamys neilli, in Southeast Asia. Conserv Genet 12: 1495-1511.
Ballard JWO, Whitlock MC, (2004) The incomplete natural history of mitochondria. Mol Ecol 13: 729-744.
Balloux F, (2010) The worm in the fruit of the mitochondrial DNA tree. Heredity 104: 419-420.
Galtier N, Nabholz B, Glémin S, Hurst GDD, (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18: 4541-4550.
Corbet G, Hill J (1992) The mammals of the Indomalayan region: a systematic review. Oxford: Oxford University Press.
Hare MP, Palumbi SR, (1999) The accuracy of heterozygous base calling from diploid sequence and resolution of haplotypes using allele-specific sequencing. Mol Ecol 8: 1750-1752.
Latinne A, Waengsothorn S, Risterucci AM, Michaux JR, (2011) Isolation, characterization and PCR multiplexing of polymorphic microsatellite markers in the threatened murine rodent, Leopoldamys neilli. Conserv Genet Resour 3: 511-513.
Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
Excoffier L, Laval G, Schneider S, (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1: 47-50.
Stephens M, Smith NJ, Donnelly P, (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68: 978-989.
Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW, (2006) Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23: 1891-1901.
Delport W, Poon AFY, Frost SDW, Pond SLK, (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26: 2455-2457.
Posada D, Crandall KA, (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Syst Biol 59: 307-321.
Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony, (*and other methods), version 4. 4. Sunderland: Sinauer Associates.
Bandelt HJ, Forster P, Rohl A, (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37-48.
Rousset F, (2008) GENEPOP '007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8: 103-106.
Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
Rosenberg NA, Feldman MW (2002) The relationship between coalescence times and population divergence times. In: Slatkin M, Veuille M, editors. Modern Developments in Theoretical Population Genetics. New York: Oxford University Press. pp. 130-164.
Drummond AJ, Rambaut A, (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
Jacobs LL, Flynn LJ (2005) Of mice again: the Siwalik rodent record, murine distribution, and molecular clocks. In: Lieberman D, Smith R, Kelley J, editors. Interpreting the past: essays on human, primate and mammal evolution. Leiden: Brill Academic. pp. 63-80.
Steppan SJ, Adkins RM, Anderson J, (2004) Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53: 533-553.
Pagès M, Chevret P, Gros-Balthazard M, Hughes S, Alcover JA, et al. (2012) Paleogenetic Analyses Reveal Unsuspected Phylogenetic Affinities between Mice and the Extinct Malpaisomys insularis, an Endemic Rodent of the Canaries. PLoS ONE 7: e31123.
Aguilar JP, Michaux J, (1996) The beginning of the age of Murinae (Mammalia: Rodentia) in southern France. Acta Zool Cracov 39: 35-45.
Michaux J, Aguilar JP, Montuire S, Wolff A, Legendre S, (1997) Les Murinae (Rodentia, Mammalia) neogenes du Sud de la France: Evolution et paleoenvironnements. Geobios 30: 379-385.
Winkler AJ, (2002) Neogene paleobiogeography and East African paleoenvironments: contributions from the Tugen Hills rodents and lagomorphs. J Hum Evol 42: 237-256.
Suchard MA, Weiss RE, Sinsheimer JS, (2001) Bayesian selection of continuous-time Markov chain evolutionary models. Mol Biol Evol 18: 1001-1013.
Rambaut A, Drummond AJ (2007) Tracer v1.4. Available: http://beast.bio.ed.ac.uk/Tracer. Accessed 2012 Oct 4.
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995). Available: http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 2012 Oct 4.
Chapuis MP, Estoup A, (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24: 621-631.
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535-538.
Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
Jakobsson M, Rosenberg NA, (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806.
Guillot G, Santos F, Estoup A, (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24: 1406-1407.
Rosenberg NA, (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4: 137-138.
Hardy OJ, Vekemans X, (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2: 618-620.
Arias JS, Szumik CA, Goloboff PA, (2011) Spatial analysis of vicariance: A method for using direct geographical information in historical biogeography. Cladistics 27: 617-628.
Ree RH, Smith SA, (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol 57: 4-14.
Ree RH, Moore BR, Webb CO, Donoghue MJ, (2005) A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution 59: 2299-2311.
Cornuet JM, Ravigne V, Estoup A, (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11: 401.
Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, et al. (2008) Inferring population history with DIY ABC: A user-friendly approach to approximate Bayesian computation. Bioinformatics 24: 2713-2719.
Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
Riviere-Dobigny T, Herbreteau V, Khamsavath K, Douangboupha B, Morand S, et al. (2011) Preliminary assessment of the genetic population structure of the enigmatic species Laonastes aenigmamus (Rodentia: Diatomyidae). J Mammal 92: 620-628.
Krystufek B, Buzan EV, Hutchinson WF, Hanfling B, (2007) Phylogeography of the rare Balkan endemic Martino's vole, Dinaromys bogdanovi, reveals strong differentiation within the western Balkan Peninsula. Mol Ecol 16: 1221-1232.
Buzan EV, Krystufek B, Bryja J, (2010) Microsatellite markers confirm extensive population fragmentation of the endangered Balkan palaeoendemic Martino's vole (Dinaromys bogdanovi). Conserv Genet 11: 1783-1794.
Castleberry SB, King TL, Wood PB, Ford WM, (2002) Microsatellite DNA analysis of population structure in allegheny woodrats (Neotoma magister). J Mammal 83: 1058-1070.
Ho SYW, Larson G, (2006) Molecular clocks: when times are a-changin'. Trends Genet 22: 79-83.
Pulquerio MJF, Nichols RA, (2007) Dates from the molecular clock: how wrong can we be? Trends Ecol Evol 22: 180-184.
Chaimanee Y, (1998) Plio-Pleistocene rodents of Thailand. Thai Stud Biodivers 3.
Zheng S (1993) Quaternary rodents of Sichuan-Guizhou area, China. Beijing: Science Press.
Latinne A, Waengsothorn S, Herbreteau V, Michaux JR (2011) Thai limestone karsts: an impending biodiversity crisis. Proceedings of the 1st EnvironmentAsia International Conference on "Environmental Supporting in Food and Energy Security: Crisis and Opportunity". Bangkok, Thailand. pp. 176-187.
Howarth FG, Hoch H (2005) Adaptive shifts. In: Culver DC, White WB, editors. Encyclopedia of caves. Amsterdam: Elsevier/Academic Press. pp. 17-24.
Nutalaya P, Vella P, Bunopas S, Kaewyana W (1986) Quaternary processes in Thailand. Proceedings of the Workshop on Economic Geology, Tectonics, Sedimentary Processes and Environment of the Quaternary in Southeast Asia, Haad Yai, Thailand. pp. 35-44.
Dheeradilok P, (1995) Quaternary coastal morpholgy and deposition in Thailand. Quat Int 26: 49-54.
Thiramongkol N (1983) Quaternary stratrigraphy of Thailand. Workshop on stratrigraphic correlation of Thailand and Malaysia. Haad Yai, Thailand. pp. 188-203.
Sinsakul S, (2000) Late quaternary geology of the Lower Central Plain, Thailand. J Asian Earth Sci 18: 415-426.
Moritz C, (1994) Defining 'Evolutionarily Significants Units' for conservation. Trends Ecol Evol 9: 373-375.
ESCAP, Economic and Social Commission for Asia and the Pacific (2001) Atlas of Mineral resources of the ESCAP region, Volume 16, Mineral Resources of Thailand. New-York: United Nations.
World Bank (2004) Thailand Environment Monitor 2004, Biodiversity conservation. Washington D.C.: World Bank.