[en] Leopoldamys neilli is a threatened murine rodent species endemic to limestone karsts of Thailand. We have studied the phylogeography of L. neilli using two mitochondrial markers (cytb, COI) and one nuclear fragment (bfibr), in order to assess the influence of its endemicity to karst habitat. One hundred fifteen individuals of L. neilli were collected in 20 localities throughout the geographic range of this species in Thailand. Our study revealed strong geographic structure of the mtDNA genetic diversity: six highly differentiated, allopatric genetic lineages were observed in our dataset. They exhibit a very high degree of genetic divergence, low gene flow among lineages and low levels of haplotype and nucleotide diversities within lineages.
Our results suggest that L. neilli’s populations are highly fragmented due to the scattered distribution of its karst habitat. The most divergent lineage includes the populations from western Thailand, which have been separated from the other genetic lineages since at least the Early Pleistocene. The other lineages are more closely related and have diverged since the Middle Pleistocene. This study revealed an unexpected high level of genetic differentiation within L. neilli and highlighted the high endemicity of this species to limestone karsts. Our results enhance the importance of protecting limestone habitats to preserve not only the species but also intraspecific diversity.
Disciplines :
Zoology Genetics & genetic processes
Author, co-author :
Latinne, Alice ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Waengsothorn, Surachit; Thailand Institute of Scientific and Technological Research (TISTR), Bangkok, Thailand
Herbreteau, Vincent; CIRAD, UR AGIRs (Animal et Gestion Inte´gre´e des Risques), France
Michaux, Johan ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Language :
English
Title :
Evidence of complex phylogeographic structure for the threatened rodent Leopoldamys neilli, in Southeast Asia
Achard F, Eva HD, Stibig HJ, Mayaux P, Gallego J, Richards T, Malingreau JP (2002) Determination of deforestation rates of the World's humid tropical forests. Science 297: 999-1002.
Aguilar JP, Michaux J (1996) The beginning of the age of Murinae (Mammalia: Rodentia) in southern France. Acta Zool Cracov 39: 35-45.
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge.
Baker RH, DeSalle R (1997) Multiple sources of character information and the phylogeny of Hawaiian Drosophila. Syst Biol 46: 654-673.
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37-48.
Beheregaray LB (2008) Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Mol Ecol 17: 3754-3774.
Bradley R, Baker R (2001) A test of the genetic species concepts: cytochrome-b sequences and mammals. J Mammal 82: 960-973.
Cabe PR, Page RB, Hanlon TJ, Aldrich ME, Connors L, Marsh DM (2007) Fine-scale population differentiation and gene flow in a terrestrial salamander (Plethodon cinereus) living in a continuous habitat. Heredity 98: 53-60.
Campbell P, Schneider CJ, Adnan AM, Zubaid A, Kunz TH (2004) Phylogeny and phylogeography of Old World fruit bats in the Cynopterus brachyotis complex. Mol Phylogenet Evol 33: 764-781.
Campbell P, Putnam A, Bonney C, Bilgin R, Morales JC, Kunz TH, Ruedas LA (2007) Contrasting patterns of genetic differentiation between endemic and widespread species of fruit bats (Chiroptera: Pteropodidae) in Sulawesi, Indonesia. Mol Phylogenet Evol 44: 474-482.
Clark AG (1990) Inference of haplotypes from PCR-amplified samples of diploid populations. Mol Biol Evol 7: 111-122.
Clements R, Sodhi NS, Schilthuizen M, Ng PKL (2006) Limestone karsts of Southeast Asia: imperiled arks of biodiversity. Bioscience 56: 733-742.
Clements R, Ng PKL, Lu XX, Ambu S, Schilthuizen M, Bradshaw CJA (2008) Using biogeographical patterns of endemic land snails to improve conservation planning of limestone karsts. Biol Conserv 141: 2751-2764.
Corbet G, Hill J (1992) The mammals of the Indomalayan region: a systematic review. Oxford University Press, Oxford.
Day MJ, Urich PB (2000) An assessment of protected karst landscapes in Southeast Asia. Cave Karst Sci 27: 61-70.
Dheeradilok P (1995) Quaternary coastal morphology and deposition in Thailand. Quat Int 26: 49-54.
Dheeradilok P, Kaewyana W (1983) On the quaternary deposits of Thailand. In: Conference on Geology and mineral resources of Thailand, Bangkok, pp 127-135.
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22: 1185-1192.
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. Public Libr Sci Biol 4: 699-710.
Eldridge MDB, King JM, Loupis AK, Spencer PBS, Taylor AC, Pope LC, Hall GP (1999) Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock-wallaby. Conserv Biol 13: 531-541.
Excoffier L, Laval G, Schneider S (2005) Arlequin ver 3. 0: an integrated software package for population genetics data analysis. Evol Biol Online 1: 47-50.
Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78: 311-327.
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge.
Garcia-Paris M, Good DA, Parra-Olea G, Wake DB (2000) Biodiversity of Costa Rican salamanders: implications of high levels of genetic differentiation and phylogeographic structure for species formation. Proc Natl Acad Sci USA 97: 1640-1647.
Gillieson D (2005) Karst in Southeast Asia. In: Gupta A (ed) The physical geography of Southeast Asia. Oxford University Press, Oxford, pp 157-176.
Gorog AJ, Sinaga MH, Engstrom MD (2004) Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biol J Linn Soc 81: 91-109.
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
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.
Hansen MC, Stehman SV, Potapov PV, Loveland TR, Townshend JRG, DeFries RS, Pittman KW, Arunarwati B, Stolle F, Steininger MK, Carroll M, DiMiceli C (2008) Humid tropical forest clearing from 2000 to 2005 quantified by using multitemporal and multiresolution remotely sensed data. Proc Natl Acad Sci USA 105: 9439-9444.
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: 1749-1752.
Heads M (2005) Dating nodes on molecular phylogenies: a critique of molecular biogeography. Cladistics 21: 62-78.
Ho SYW, Larson G (2006) Molecular clocks: when times are a-changin'. Trends Genet 22: 79-83.
Jacobs LL, Downs WR (1994) The evolution of murine rodents in Asia. In: Tomida Y, Li CK, Setoguschi T (eds) Rodent and lagomorph families of Asian origins and their diversification, vol 8. National Science Museum Monograph, Tokyo, pp 149-156.
Jacobs LL, Flynn LJ (2005) Of mice... again: the Siwalik rodent record, murine distribution, and molecular clocks. In: Lieberman D, Smith R, Kelley J (eds) Interpreting the past: essays on human primate and mammal evolution. Brill Academic, Leiden, pp 63-80.
Jacobs LL, Pilbeam D (1980) Of mice and men: fossil-based divergence dates and molecular "Clocks". J Hum Evol 9: 551-555.
Jaeger JJ, Tong H, Denys C (1986) Age de la divergence Mus-Rattus: comparaison des données paléontologiques et moléculaires. C R Acad Sci II 302: 917-922.
Lekagul B, McNeely JA (1988) Mammals of Thailand. White Lotus Press, Bangkok.
Librado P, Rozas J (2009) DnaSP v5: a software or comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
Liu CC, Liu YG, Guo K, Zheng YR, Li GQ, Yu LF, Yang R (2010) Influence of drought intensity on the response of six woody karst species subjected to successive cycles of drought and rewatering. Physiol Plantarum 139: 39-54.
Lunde D, Aplin K (2008) Leopoldamys neilli. In: IUCN 2010 (ed) IUCN Red List of threatened species, version 2010. 1.
Martinez-Solano I, Jockusch EL, Wake DB (2007) Extreme population subdivision throughout a continuous range: phylogeography of Batrachoseps attenuates (Caudata: Plethodontidae) in western North America. Mol Ecol 16: 4335-4355.
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 14: 114-116.
Meijaard E, Groves CP (2006) The geography of mammals and rivers in mainland South-East Asia, chap 11. In: Lehman SM, Fleagle JG (eds) Primate biogeography. Springer, New York, pp 305-329.
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.
Michaux JR, Magnanou E, Paradis E, Nieberding C, Libois R (2003) Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the western Palaearctic region. Mol Ecol 12: 685-697.
Michaux JR, Libois R, Filippucci MG (2005) So close and so different: comparative phylogeography of two small mammal species, the Yellow-necked fieldmouse (Apodemus flavicollis) and the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Heredity 94: 52-63.
Moritz C (1994) Defining 'evolutionarily significant units' for conservation. Trends Ecol Evol 9: 373-375.
Mouline K, Granjon L, Galan M, Tatard C, Doukary A, Solimane AA, Duplantier JM, Cosson JF (2008) Phylogeography of a Sahelian rodents species Mastomys huberti: a Plio-Pleistocene story of emergence and colonization of humid habitats. Mol Ecol 17: 1036-1053.
Musser G, Carleton M (2005) Superfamily Muroidea. In: Wilson DE (ed) Mammal species of the World: a taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore, pp 894-1531.
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
Nieberding C, Morand S, Libois R, Michaux JR (2006) Parasites and the island syndrome: the colonizationof the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). J Biogeogr 33: 1212-1222.
Nijman V (2010) An overview of international wildlife trade from Southeast Asia. Biodiver Conserv 19: 1101-1114.
O'Loughlin SM, Somboon P, Walton C (2007) High levels of population structure caused by habitat islands in the malarial vector Anopheles scanloni. Heredity 99: 31-40.
Pagès M, Chaval Y, Waengsothorn S, Cosson JF, Hugot JP, Morand S, Michaux J (2010) Refining the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evol Biol. doi: 10. 1186/1471-2148-10-184.
Patou ML, Chen J, Cosson L, Andersen DH, Cruaud C, Couloux A, Randi E, Zhang S, Veron G (2009) Low genetic diversity in the masked palm civet Paguma larvata (Viverridae). J Zool 278: 218-230.
Patou ML, Wilting A, Gaubert P, Esselstyn JA, Cruaud C, Jennings A, Fickel J, G Veron (2010) Evolutionary history of the Paradoxurus palm civets-a new model for Asian biogeography. J Biogeogr. doi: 10. 1111/j. 1365-2699. 2010. 02364. x.
Peh KSH (2010) Invasive species in Southeast Asia: the knowledge so far. Biodiver Conserv 19: 1083-1099.
Penny D (2001) A 40, 000 year palynological record from north-east Thailand; implications for biogeography and palaeo-environmental reconstruction. Palaeogeogr Palaeoclimatol Palaeoecol 171: 97-128.
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality test against population growth. Mol Biol Evol 19: 2092-2100.
Rivière-Dobigny T, Herbreteau V, Khamsavath K, Douangboupha B, Morand S, Michaux JR, Hugot JP (2011) Preliminary assessment of the genetic population structure of the enigmatic species Laonastes aenigmamus (Rodentia: Diatomyidae). J Mammal 92: 620-628.
Robins J, Hingston M, Matisoo-Smith E, Ross H (2007) Identifying Rattus species using mitochondrial DNA. Mol Ecol Notes 7: 717-729.
Rosenberg NA, Feldman MW (2002) The relationship between coalescence times and population divergence times. In: Slatkin M, Veuille M (eds) Modern developments in theoretical population genetics. Oxford University Press, New York, pp 130-164.
Schilthuizen M, Liew TS, Bin Elahan B, Lackman-Ancrenaz I (2005) Effects of karst forest degradation on pulmonate and prosobranch land snail communities in Sabah, Malaysian Borneo. Conserv Biol 19: 949-954.
Schipper J, Chanson JS, Chiozza F, Cox NA, Hoffmann M, Katariya V, Lamoreux J et al (2008) The status of the world's land and marine mammals: diversity, threats and knowledge. Science 322: 225-230.
Seddon JM, Santucci F, Reeve NJ, Hewitt GM (2001) DNA footprints of European hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene refugia, postglacial expansion and colonization routes. Mol Ecol 10: 2187-2198.
Simms MJ (2005) Sedimentary processes, karsts and palaeokarst. In: Selley RC, Cocks LRM, Plimer IR (eds) Encyclopedia of geology. Elsevier, Oxford, pp 678-687.
Sinsakul S (2000) Late Quaternary geology of the Lower Central Plain, Thailand. J Asian Earth Sci 18: 415-426.
Sodhi NS, Koh LP, Brook BW, Ng PKL (2004) Southeast Asian biodiversity: an impending disaster. Trends Ecol Evol 19: 654-660.
Sodhi NS, Posa MRC, Lee TM, Bickford D, Koh LP, Brook BW (2010) The state and conservation of Southeast Asian biodiversity. Biodiver Conserv 19: 317-328.
Sorenson MD, Franzosa EA (2007) TreeRot, version 3. Boston University, Boston.
Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony, (*and other methods), version 4. Sinauer Associates, Sunderland.
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.
Taylor D (2010) Biomass burning, humans and climate change in Southeast Asia. Biodiver Conserv 19: 1025-1042.
Vermeulen J, Whitten T (1999) Biodiversity and cultural property in the management of limestone resources-lessons from East Asia. World Bank, Washington.
Verneau O, Catzeflis F, Furano AV (1998) Determining and dating recent rodent speciation events by using L1 (LINE-1) retrotransposons. Proc Natl Acad Sci USA 95: 11284-11289.
Waengsothorn S, Nabhitabhata J, Moochan T (2007) The ecological distribution of Thai endemic rodents with a new distributional range of Niviventer hinpoon. Thailand 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.
Welch JJ, Bromham L (2005) Molecular dating when rates vary. Trends Ecol Evol 20: 320-327.
White JC, Penny D, Kealhofer L, Maloney B (2004) Vegetation changes from the late Pleistocene through the Holocene from three areas of archaeological significance in Thailand. Quat Int 113: 111-132.
Wiles GJ (1981) Abundance and habitat preferences of small mammals in southwestern Thailand. Nat Hist Bull Siam Soc 29: 44-54.
World Bank (2004) Thailand Environment Monitor 2004, Biodiversity conservation. World Bank Report. http://go. worldbank. org/VPRE208MZ0.
Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92: 371-373.
