Understanding the diversification pattern of three subspecies of swamp deer (Rucervus duvaucelii) during the Pleistocene–Holocene based on mitochondrial and Y chromosome markers

Mammalian Biology (2021)Cite this article

Abstract

The Quaternary period played a vital role in the creation of new ecological and vegetation zones, which shaped the diversification and distribution of species. The present study aimed to document, for the first time, phylogeography of three reported subspecies/populations of swamp deer, Rucervus duvaucelii duvaucelii (northern), R. d. ranjitsinhi (eastern) and R. d. branderi (central), using a fragment of the mitochondrial cyt b gene and the Y chromosome DBY-7. Inferred phylogenetic relationships revealed the presence of three genetically distinct lineages using both historic and contemporary samples. Sequence divergence between the northern and eastern populations was less (1.5%) than between the northern and central populations (1.8%). Molecular dating based on the cyt b gene suggests that swamp deer split into two (northern-eastern and central) major clades from the common ancestor before 1.3 Million years ago. Demography based on Bayesian skyline plot suggested a slight decline in one population (R. d. duvaucelii) but a stable population size in the other two populations (R. d. ranjitsinhi and R. d. branderi). The observed shallow split of the northern population into the Jhilmil Tal Wildlife Conservation Reserve and Dudhwa National Park subpopulations may have been due to extreme climatic fluctuations during the Quaternary period (Holocene) and the subsequent increased human footprint. We also review and discuss the significance of past climatic and vegetation changes due to human settlement and of paleoenvironmental and biogeographic events that may have facilitated the diversification and distribution of habitat-specific swamp deer into small patches across the Indian subcontinent and of the congeneric species, R. schomburgki, from the southeastern area in Thailand with related conservation implications.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Availability of data and material

All required information is available within the manuscript. Sequence data submitted to GenBank (CYTB–MW279546-MW279582; DBY7–MW263300-MW263303).

Code availability

Not applicable.

References

  1. Balakrishnan NC, Monfort SL, Gaur A, Singh L, Sorenson MD (2003) Phylogeography and conservation genetics of Eld’s deer (Cervus eldi). Mol Ecol 12:1–10

    CAS  PubMed  Article  Google Scholar 

  2. Bart SVFZS (1876) On Cervus schomburgki (Blyth). Proc Sci Meet Zool Soc Lond 44(1):304–308. https://doi.org/10.1111/j.1096-3642.1876.tb02568.x

    Article  Google Scholar 

  3. Berger A (1984) Accuracy and frequency stability of the Earth’s orbital elements during the Quaternary. In: Berger A, Imbrie J, Hays JGK, Saltzmann B (eds) Milankovitch and climate, part 1. Reidel, Dordrecht

    Google Scholar 

  4. Blanford WT (1880) The Fauna of British India including Ceylon and Burma, Mammalia. Taylor & Francis, London

    Google Scholar 

  5. Blinkhorn J, Parker AG, Ditchfield P, Haslam M, Petraglia M (2012) Uncovering a landscape buried by the super-eruption of Toba, 74,000 years ago: a multi-proxy environmental reconstruction of landscape heterogeneity in the Jurreru Valley, south India. Quat Int 258:135–147

    Article  Google Scholar 

  6. Bouckaert R, Heled J, Khnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Comput Biol 10:1–6

    Article  CAS  Google Scholar 

  7. Brown WM, Matthew George J, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971

    CAS  PubMed  Article  Google Scholar 

  8. Cerling TE, Ehleringer JR, Harris JM (1998) Carbon dioxide starvation, the development of C4 ecosystems, and mammalian evolution. Philos Trans R Soc Lond B Biol Sci 353:159–170

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Chan Y-C, Roos C, Inoue-Murayama M, Inoue E, Shih C-C, Vigilant L (2012) A comparative analysis of Y chromosome and mtDNA phylogenies of the Hylobates gibbons. BMC Evol Biol 12:150

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. Choudhury A (1997) Checklist of the mammals of Assam, 2nd edn. Gibbon Books & Assam Science Technology & Environment Council, Guwahati

    Google Scholar 

  11. Choudhury A (2003) The mammals of Arunachal Pradesh. Regency Publications, New Delhi

    Google Scholar 

  12. Choudhury A (2004) Kaziranga: wildlife in Assam. Rupa & Co., New Delhi

    Google Scholar 

  13. Clift P, Plumb R (2008) The Asian monsoon: causes, history and effects. Cambridge University Press, Cambridge

    Google Scholar 

  14. Cuvier G (1823) Recherches sur les ossemens fossiles de quadrupèdes. Nouvelle é: Dufour & d’Ocagne, Amsterdam

    Google Scholar 

  15. Duckworth JW, Kumar NS, Pokharel CP, Sagar Baral H, Timmins R (2015) Rucervus duvaucelii. The IUCN Red List of Threatened Species. e.T4257A22167675

  16. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Article  Google Scholar 

  17. Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Biol 27:401–410

    Article  Google Scholar 

  18. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. Gilbert C, Ropiquet A, Hassanin A (2006) Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology and biogeography. Mol Phylogenet Evol 40:101–117

    CAS  PubMed  Article  Google Scholar 

  21. Groves C (1982) Geographic variation in the barasingha or swamp deer (Cervus duvaucelii). J Bombay Nat Hist Soc 79:620–629

    Google Scholar 

  22. Gupta AK, Anderson DM, Pandey DN, Singhvi AK (2006) Adaptation and human migration, and evidence of agriculture coincident with changes in the Indian summer monsoon during the Holocene. Curr Sci 90:1082–1090

    Google Scholar 

  23. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  24. Hellborg L, Ellegren H (2003) Y chromosome conserved anchored tagged sequences (YCATS) for the analysis of mammalian male-specific. Mol Ecol 12:283–291

    CAS  PubMed  Article  Google Scholar 

  25. Hensaw J (1994) The swamp deer in suklaphanta wildlife reserve. Nepal Oryx 28:199–206

    Article  Google Scholar 

  26. Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Huffman (2006) Rucervus duvaucelii, Barasingha, Swamp deer. http://www.ultimateungulate.com/Artiodactyla/Rucervus_duvaucelii.html. Accessed 20 Nov 2006

  28. Ikeda S, Osawa K, Akamatsu Y (2009) Sediment and nutrients transport in watershed and their impact on coastal environment. Proc Jpn Acad Ser B Phys Biol Sci 85:374–390

    PubMed  PubMed Central  Article  Google Scholar 

  29. Janis CM, Scott KM (1987) The interrelationships of higher ruminant families with special emphasis on the members of the cervoidea. Am Mus Novit 2893:1–85

  30. Johns GC, Avise JC (1998) A Comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Phylogenet Evol 15:1481–1490

    CAS  Article  Google Scholar 

  31. Kale V, Joshi V, Hire P (2004) Palaeohy-drological reconstructions based on analysis of a palaeochannel and Toba-ash associated alluvial sediments in the Deccan Trap region, India. J Geol Soc 64:481–489

    Google Scholar 

  32. Kangas V-M, Rytkönen S, Kvist L, Käpylä T, Nygrén T, Aspi J (2016) Geographic cline in the shape of the moose mandible: indications of an adaptive trend. J Mamm Evol 24:233–241. https://doi.org/10.1007/s10914-016-9344-y

    Article  Google Scholar 

  33. Karanth KP (2003) Evolution of disjunct distributions among wet-zone species of the Indian subcontinent: testing various hypotheses using a phylogenetic approach. Curr Sci 85:1276–1283

    Google Scholar 

  34. Kuroki Y, Toyoda A, Noguchi H, Taylor TD, Itoh T, Kim DS, Kim DW, Choi SH, Kim IC, Choi HH et al (2006) Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nat Genet 38:158–167

    CAS  PubMed  Article  Google Scholar 

  35. Kurup GU (1974) Mammals of Assam and the Mammal-Geography of India. In: Mani MS (ed) Ecology and Biogeography in India. Monographiae Biologicae, vol 23. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-2331-3_18

    Google Scholar 

  36. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. Lovejoy NR, De Araújo MLG (2000) Molecular systematics, biogeography and population structure of Neotropical freshwater needle shes of the genus Potamorrhaphis. Mol Ecol 9:259–268

    CAS  PubMed  Article  Google Scholar 

  38. Ludt CJ, Schroeder W, Rottmann O, Kuehn R (2004) Mitochondrial DNA phylogeography of red deer (Cervus elaphus). Mol Phylogenet Evol 31:1064–1083

    CAS  PubMed  Article  Google Scholar 

  39. Lydekker R (1890) The new natural history. Printed by order of the Trustees of the British Museum (Natural History) London

  40. Lydekker R (1907) The game animals of India, Burma, Malaya, and Tibet, being a new and revised edition of ‘The great and small game of India, Burma, and Tibet. Rowland Ward, Limited, London

    Google Scholar 

  41. Martin C (1977) Status and ecology of the Barasingha (Cervus duvauceli branderi) in Kanha National Park (India). J Bombay Nat Hist Soc 74:60–132

    Google Scholar 

  42. Massicot P (2005) Animla Info-Barasingha. http://www.animalinfo.org/species/artiperi/cervduva. Accessed 20 Nov 2006

  43. McDevitt AD, Edwards CJ, O’Toole P, O’Sullivan P, O’Reilly C, Carden RF (2009) Genetic structure of, and hybridisation between, red (Cervus elaphus) and sika (Cervus nippon) deer in Ireland. Mamm Biol 74:263–273

    Article  Google Scholar 

  44. Meijaard E, Groves C (2004) Morphometrical relationships between Southeast Asian deer (Cervidae, tribe Cervini): evolutionary and biogeographic implications. J Zool 263:179–196

    Article  Google Scholar 

  45. Meyer A (1993) Evolution of mitochondrial DNA in fishes. In: Hochachka M (ed) Biochemistry and molecular biology of fishes. Elsevier, Amsterdam

    Google Scholar 

  46. Milá B, Girman DJ, Kimura M, Smith TB (2000) Genetic evidence for the effect of a postglacial population expansion on the phylogeography of a North American songbird. Proc Biol Sci 267:1033–1040

    PubMed  PubMed Central  Article  Google Scholar 

  47. Morgan ME, Kingston JD, Marino BD (1994) Carbon isotopic evidence for the emergence of C4 plants in the neogene from Pakistan and Kenya. Nature 367:162–165

    CAS  Article  Google Scholar 

  48. Morrison-Scott TCS (1951) Checklist of palaeractic and Indian mammals. British Museum, London

    Google Scholar 

  49. Nishida S, Goto M, Pastene LA, Kanda N, Koike H (2007) Phylogenetic relationships among CetaceansRevealed by Y-chromosome sequences. Zool Sci 24:723–732. https://doi.org/10.2108/zsj.24.723

    CAS  Article  Google Scholar 

  50. Nylander JAA (2004) Mr Modeltest v2. Program Distributed by the Author Evolutionary Biology Centre. Uppsala University, Uppsala

    Google Scholar 

  51. Pandey AK, Pandey P, Singh GD, Juya N (2014) Climate footprints in the late quaternary-holocene landforms of Dun valley, NW Himalaya, India. Curr Sci 106:245–253

    Google Scholar 

  52. Perez-Espona S, Perez-Barberıa F, Goodall-Copestake W, Jiggins C, Gordon I, Pemberton J (2009) Genetic diversity and population structure of Scottish Highland red deer (Cervus elaphus) populations: a mitochondrial survey. Heredity 102:199–210

    CAS  PubMed  Article  Google Scholar 

  53. Pitra C, Fickel J, Meijaard E, Groves PC (2004) Evolution and phylogeny of old world deer. Mol Phylogenet Evol 33:880–895

    CAS  PubMed  Article  Google Scholar 

  54. Pocock R (1943) The larger deer of British India. J Bombay Nat Hist Soc 43:553–572

    Google Scholar 

  55. Prakash RK, Nayak RK, Pandey R, Shukla U et al (2012) Habitat viability analysis for the proposed reintroduction site for the hard-ground Barasingha (Cervus duvauceli branderi) in the Bori Wildlife Sanctuary, Satpura Tiger Reserve (Madhya Pradesh). Report by State Forest Research Institute, Jabalpur (M.P.), India

  56. Prater S (1948) The book of Indian animals, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  57. Qureshi Q, Sawarkar VB, Mathur PK (1995) Ecology and Management of swamp deer (Cervus duvauceli) in Dudhwa Tiger Reserve UP (India). Wildlife Institute of Indian, Dehradun

    Google Scholar 

  58. Qureshi Q, Sawarkar V, Rahmani A, Mathur P (2004) Swamp Deer or Barasingha (Cervus duvauceli Cuvier, 1823). Wildlife Institute of Indian, Dehradun

    Google Scholar 

  59. Rambaut A (2009) FigTree, ver. 1.3.1. [Online]. Institute of Evolutionary Biology. University of Edinburgh. http://tree.bio.ed.ac.uk/. Accessed Oct 2014

  60. Rambaut A, Drummond A (2014) Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer/. Accessed Oct 2014

  61. Ramos-onsins SE, Rozas J (2020) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100. https://doi.org/10.1093/molbev/msl052

    Article  Google Scholar 

  62. Randi E, Pierpaoli M, Danilkin A (1998) Mitochondrial DNA polymorphism in populations of Siberian and European roe deer (Capreolus pygargus and C. capreolus). Heredity 80:429–437

    CAS  PubMed  Article  Google Scholar 

  63. Rocha-Olivares A, Rosenblatt RH, Vetter RD (1999) Molecular evolution, systematics, and zoogeography of the rockfish subgenus Sebastomus (Sebastes, Scorpaenidae) based on mitochondrial cytochrome b and control region sequences. Mol Phylogenet Evol 11:441–458

    CAS  PubMed  Article  Google Scholar 

  64. Roos C, Zinner D, Kubatko LS, Schwarz C, Yang M, Meyer D, Nash SD, Xing J, Batzer M, Brameier M et al (2011) Nuclear versus mitochondrial DNA: evidence for hybridization in colobine monkeys. BMC Evol Biol 11:77

    PubMed  PubMed Central  Article  Google Scholar 

  65. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  66. Sankaran R (1989) Status of the swamp deer (Cervus duvauceli duvauceli) in the Dudwa National Park, Uttar Pradesh, India. J Bombay Nat Hist Soc 87:250–259

    Google Scholar 

  67. Schaff D (1978) Population size and structure and habitat relations of the Barasingha (Cervus d. duvauceli) in Suklaphanta wildlife reserve. Michigan, USA

  68. Schaller G (1967) The deer and the tiger. University of Chicago Press, Chicago

    Google Scholar 

  69. Singh CP, Chauhan JS, Parihar JS, Singh RP, Shukla R (2015) Using environmental niche modeling to find suitable habitats for the Hard-ground Barasingha in Madhya Pradesh, India. JoTT 7(11):7761–7769. https://doi.org/10.11609/JoTT.o3899.7761-9

    Article  Google Scholar 

  70. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 595:585–595

    Article  Google Scholar 

  71. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  72. Tobe SS, Kitchener AC, Linacre AMT (2010) Reconstructing mammalian phylogenies: a detailed comparison of the cytochrome b and cytochrome oxidase subunit i mitochondrial genes. PLoS One 5:e14156. https://doi.org/10.1371/journal.pone.0014156

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:907–3930

    Article  CAS  Google Scholar 

  74. Valdiya KS (2002) Emergence and evolution of Himalaya: reconstructing history in the light of recent studies. Prog Phys Geogr 26:360–399

    Article  Google Scholar 

  75. Verma S, Singh L (2003) Novel universal primers establish identity of an enormous number of animal species for forensic application. Mol Ecol Notes 3:28–31

    CAS  Article  Google Scholar 

  76. Xue D, Wang H, Zhang T, Liu J (2014) Population genetic structure and demographic history of atrina pectinata based on mitochondrial DNA and microsatellite markers. PLoS One 9(5):e95436. https://doi.org/10.1371/journal.pone.0095436

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Director, Dean and Research Coordinator of the Wildlife Institute of India, Dehradun, for strong support and facilitation. Our sincere thanks are due to the Bombay Natural History Society, Mumbai, India for providing historical samples. The authors acknowledge the support provided by the Nodal Officer and all the researchers and staff of the Wildlife Forensic Cell of the Wildlife Institute of India for conducting this study.

Funding

This was a grant-in-aid project of the Wildlife Institute of India.

Author information

Author notes

  1. Ved Prakash Kumar, Bheem Dutt Joshi, Reeta Sharma contributed equally.

Affiliations

  1. Wildlife Institute of India, Chandrabani, Dehradun, Uttarakhand, 248001, India

    Ved Prakash Kumar, Bheem Dutt Joshi, Reeta Sharma, Animesh Talukdar, Parag Nigam & Surendra Prakash Goyal

  2. Maaty Biodiversity Conservation and Societal Research Organization, Dehradun, 248001, India

    Ved Prakash Kumar & Ankita Rajpoot

  3. Veer Kunwar Singh University, Arrah, Bihar, 802301, India

    Ved Prakash Kumar & Dhyanendra Kumar

Authors
  1. Ved Prakash Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bheem Dutt Joshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Reeta Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ankita Rajpoot
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Animesh Talukdar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Parag Nigam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dhyanendra Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Surendra Prakash Goyal
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

VPK conceived the idea, generated data, performed the data analysis and wrote the manuscript; BDJ and SPG conceived the idea and wrote the manuscript; BDJ performed the data analysis; RS and AR edited the manuscript; and PN and AT curated data.

Corresponding authors

Correspondence to Bheem Dutt Joshi or Surendra Prakash Goyal.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Ethics approval

All samples were collected non-invasively from the repository of the Wildlife Institute of India from which ethical permission was procured. No animal or human participation was involved in this study.

Consent to participate

All authors approved this manuscript and no data have been used for which copyright is needed.

Consent for publication

All authors give consent to publish this manuscript and no data have been used for which copyright is needed.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations

Handling editor: Pamela Burger.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCM 106 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kumar, V.P., Joshi, B.D., Sharma, R. et al. Understanding the diversification pattern of three subspecies of swamp deer (Rucervus duvaucelii) during the Pleistocene–Holocene based on mitochondrial and Y chromosome markers. Mamm Biol (2021). https://doi.org/10.1007/s42991-021-00104-7

Download citation

Keywords

  • Subspecies
  • mtDNA
  • Genetic diversity
  • Divergence time
  • Reintroduction
  • Conservation