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Population genetics of the snow leopards (Panthera uncia) from the Western Himalayas, India

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Abstract

The snow leopard (Panthera uncia), one of the most threatened felids distributed along the high-altitude mountains in the Himalayas, has experienced a steady population decline in most of its distribution range due to the loss of suitable habitats, anthropogenic activities, and retaliatory killings. We undertook the genetic assessment of the snow leopard in the Western Himalaya, India, and identified 18 unique individuals. The snow leopard populations exhibited moderate genetic variability, i.e., effective number of alleles = 3.96 ± 0.004, observed heterozygosity = 0.539 ± 0.038 and no variation at mtDNA. We found the snow leopard populations under panmixia, possibly due to the long-ranging behavior and dispersal patterns. We present the first population genetic account of the snow leopard from the Western Himalayas and discuss the importance of non-invasive genetics in monitoring the snow leopard population in the tough terrain of the trans-Himalayan region of India.

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References

  • Anon (2008) The Project Snow Leopard. Ministry of Environment and Forests, Government of India, New Delhi. http://moef.gov.in/wp-content/uploads/2018/03/Project-Snow-Leopard-2008.pdf

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Bhatnagar YV, Wangchuk R, Mishra C (2006) Decline of the Tibetan gazelle Procapra picticaudata in Ladakh, India. Oryx 40:229–232

    Article  Google Scholar 

  • Bhatnagar YV, Mathur VB, McCarthy T (2001) A regional perspective for snow leopard conservation in the Indian Trans-Himalaya. In: National Workshop on Regional Planning for Wildlife Protected Areas, pp 6–8

  • Bhatnagar YV, Mathur VB, Sathyakumar S, Ghoshal A, Sharma RK, Bijoor A, Lal P (2016) South Asia: India. Snow leopards. Academic Press, London, pp 457–469

    Chapter  Google Scholar 

  • Chetri M, Odden M, Sharma K, Flagstad Ø, Wegge P (2019) Estimating snow leopard density using fecal DNA in a large landscape in north-central Nepal. Glob Ecol Conserv 17:e00548

    Article  Google Scholar 

  • Chundawat RS (1992) Ecological studies of snow leopard and its associated prey species in Hemis High Altitude National Park, Ladakh (J andK). Dissertation, University of Rajasthan, Jaipur, India

  • Da Fonseca RR, Johnson WE, O’Brien SJ, Ramos MJ, Antunes A (2008) The adaptive evolution of the mammalian mitochondrial genome. BMC Genom 9:1–22

    Article  Google Scholar 

  • Dalui S, Khatri H, Singh SK, Basu S, Ghosh A, Mukherjee T, Thakur M (2020) Fine-scale landscape genetics unveiling contemporary asymmetric movement of red panda (Ailurus fulgens) in Kangchenjunga landscape, India. Sci Rep 10:1–12

    Article  Google Scholar 

  • Dhar U, Rawal RS, Samant SS (1997) Structural diversity and representativeness of forest vegetation in a protected area of Kumaun Himalaya, India: implications for conservation. Biodivers Conserv 6:1045–1062

    Article  Google Scholar 

  • Dutta T, Sharma S, Maldonado JE, Wood TC, Panwar HS, Seidensticker J (2013) Fine-scale population genetic structure in a wide-ranging carnivore, the leopard (Panthera pardus fusca) in central India. Divers Distrib 19(7):760–771

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Favre DS (1989) International Trade in Endangered Species: A Guide to CITES. Dordrecht: Martinus Nijhoff, 415 pp.

  • Fox JL, Sinha SP, Chundawat RS, Das PK (1991) Status of the snow leopard Panthera uncia in North-west India. Biological Conserv 55(3):283–298

  • Garner A, Hicks RJL, JF, (2005) Patterns of genetic diversity and its loss in mammalian populations. Conserv Biol 19:1215–1221

    Article  Google Scholar 

  • Gartner MC, Powell DM, Weiss A (2014) Personality structure in the domestic cat (Felissil vestriscatus), Scottish wildcat (Felissil vestrisgrampia), clouded leopard (Neofelisnebulosa), snow leopard (Panthera uncia), and African lion (Panthera leo): a comparative study. J Compar Psychol 128:414

    Article  Google Scholar 

  • Hajkova P, Zemanova B, Roche K, Hajek B (2009) An evaluation of field and noninvasive genetic methods for estimating Eurasian otter population size. Conserv Genet 10(6):1667–1681

    Article  Google Scholar 

  • Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS ONE 7(9):e45170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hassanin A, Ropiquet A, Couloux A, Cruaud C (2009) Evolution of the mitochondrial genome in mammals living at high altitude: new insights from a study of the tribe Caprini (Bovidae, Antilopinae). J Mol Evol 68:293–310

    Article  CAS  PubMed  Google Scholar 

  • Jackson R, Mallon D, Mccarthy T (2008) Panthera unica. The IUCN Red List of Threatened Species. http://www.iucnredlist.org/details/15957/0

  • Janečka JE, Jackson R, Yuquang Z, Diqiang L, Munkhtsog B, Buckley-Beason V, Murphy WJ (2008) Population monitoring of snow leopards using noninvasive collection of scat samples: a pilot study. Anim Conserv 11:401–411

    Article  Google Scholar 

  • Janečka JE, Munkhtsog B, Jackson RM, Naranbaatar G, Mallon DP, Murphy WJ (2011) Comparison of noninvasive genetic and camera-trap** techniques for surveying snow leopards. J Mam 92:771–783

    Article  Google Scholar 

  • Janecka JE, Zhang Y, Li D, Munkhtsog B, Bayaraa M, Galsandorj N, Jackson R (2017) Range-wide snow leopard phylogeography supports three subspecies. J Hered 108:597–607

    Article  PubMed  Google Scholar 

  • Janecka JE, Janecka MJ, Helgen KM, Murphy WJ (2018) The validity of three snow leopard subspecies: response to Senn et al. Heredity 120(6):586–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janjua S, Peters JL, Weckworth B, Abbas FI, Bahn V, Johansson O, Rooney TP (2020) Improving our conservation genetic toolkit: ddRAD-seq for SNPs in snow leopards. Conserv Gen Res 12:257–261

    Article  Google Scholar 

  • Johnson PCD, Haydon DT (2007) Maximum-likelihood estimation of allelic dropout and false allele error rates from microsatellite genotypes in the absence of reference data. Genetics 175:827–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalinowski ST, Wagner AP, Taper ML (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579

    Article  CAS  Google Scholar 

  • Karmacharya DB, Thapa K, Shrestha R, Dhakal M, Janecka JE (2011) Noninvasive genetic population survey of snow leopards (Panthera uncia) in Kangchenjunga conservation area, Shey Phoksundo National Park and surrounding buffer zones of Nepal. BMC Res Notes 4:1–9

    Article  Google Scholar 

  • Li J, Dajun W, Hang Y, Duojie Z, Zhala J, George BS, Charudutt M (2014) Role of Tibetan Buddhist monasteries in snow leopard conservation. Conserv Biol 28:87–94

    Article  PubMed  Google Scholar 

  • Lovari S, Boesi R, Minder I, Mucci N, Randi E, Dematteis A, Ale SB (2009) Restoring a keystone predator may endanger a prey species in a human-altered ecosystem: the return of the snow leopard to Sagarmatha National Park. Anim Conserv 12:559–570

    Article  Google Scholar 

  • Luo SJ, Kim JH, Johnson WE, Van DWJ, Martenson J, O’Brien YN (2004) Phylogeography and genetic ancestry of tigers (Panthera tigris). PLoS Biol 12:e442

    Article  Google Scholar 

  • McCarthy TM, Chapron G (2003) Snow leopard survival strategy. International Snow Leopard Trust and Snow Leopard Network, Seattle, p 105

    Google Scholar 

  • McCarthy MI, Abecasis GR, Cardon LR, Goldstein DB, Little J, Ioannidis JP, Hirschhorn JN (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Gen 9:356–369

    Article  CAS  Google Scholar 

  • McCarthy T, Mallon D, Jackson R, Zahler P, McCarthy K (2017) Panthera uncia. The IUCN Red List of Threatened Species 2017:e.T22732A50664030.10.2305/IUCN.UK.2017-2.RLTS.T22732A50664030.en

  • Menotti-Raymond M, David VA, Lyons LA, Schäffer AA, Tomlin JF, Hutton MK, Brien SJ (1999) A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57:9–23

    Article  CAS  PubMed  Google Scholar 

  • Mishra C, Allen P, McCarthy TOM, Madhusudan MD, Bayarjargal A, Prins HH (2003) The role of incentive programs in conserving the snow leopard. Conserv Biol 17:1512–1520

    Article  Google Scholar 

  • Mishra S, Singh SK, Munjal AK, Aspi J, Goyal SP (2014) Panel of polymorphic heterologous microsatellite loci to genotype critically endangered Bengal tiger: a pilot study. Spring plus 3:1–10

    Article  Google Scholar 

  • Mukesh KVP, Sharma LK, Shukla M, Sathyakumar S (2015a) Pragmatic perspective on conservation genetics and demographic history of the last surviving population of Kashmir red deer (Cervus elaphushanglu) in India. PLoS ONE 10:e0117069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukesh T, Sharma LK, Charoo SA, Sathyakumar S (2015b) Conflict bear translocation: investigating population genetics and fate of bear translocation in Dachigam National Park, Jammu and Kashmir, India. PLoS ONE 10:e0132005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nyhus PJ, Mccarthy T, Mallon D (2016) Snow leopards: biodiversity of the world: conservation from genes to landscapes. Academic Press, London

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Wen, W, Falush D (2004) Documentation for structure software: version 2. Department of Human Genetics, University of Chicago, Chicago. http://pritch.bsd.uchicago.edu/structure.htm

  • Raymond M, Rousset F (1995) GENEPOP (V. 4): Population genetics software for exact tests and ecumenicism. J Heredity 86:248-249 

  • Rodgers TW, Janečka JE (2013) Applications and techniques for non-invasive faecal genetics research in felid conservation. Eur J Wild Res 59:1–16

    Article  Google Scholar 

  • Rodgers WA, Panwar HS (1988) Biogeographical classification of India. Wildlife Institute of India, New Forest, Dehra Dun, India

  • Senn H, Murray-Dickson G, Kitchener AC, Riordan P, Mallon D (2018) Response to Janecka et al. 2017. Heredity 120:581–585

    Article  CAS  PubMed  Google Scholar 

  • Shrestha B, Kindlmann P (2020) Implications of landscape genetics and connectivity of snow leopard in the Nepalese Himalayas for its conservation. Sci Rep 10:1–11

    Article  Google Scholar 

  • Singh SK, Mishra S, Aspi J, Kvist L, Nigam P, Pandey P, Goyal SP (2015) Tigers of Sundarbans in India: is the population a separate conservation unit? PLoS ONE 10(4):e0118846

    Article  PubMed  PubMed Central  Google Scholar 

  • Suryawanshi KR, Bhatnagar YV, Redpath S, Mishra C (2013) People, predators and perceptions: patterns of livestock depredation by snow leopards and wolves. J Appl Ecol 50:550–560

    Article  Google Scholar 

  • Taberlet P, Bouvet J (1994) Mitochondrial DNA polymorphism, phylogeography, and conservation genetics of the brown bear Ursus arctos in Europe. Proc R Soc Lond Ser B 255(1344):195–200

    Article  CAS  Google Scholar 

  • Thakur M, Fernandes M, Sathyakumar S, Singh SK, Vijh RK, Han J, et al (2018) Understanding the cryptic introgression and mixed ancestry of Red Junglefowl in India. PLoS ONE 13(10):e0204351. https://doi.org/10.1371/journal.pone.0204351

  • Toews DP, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930

    Article  CAS  PubMed  Google Scholar 

  • Uphyrkina O, Johnson WE, Quigley H, Miquelle D, Marker L, Bush M, O’Brien SJ (2001) Phylogenetics, genome diversity and origin of modern leopard, Panthera pardus. Mol Eco 10:2617–2633

    Article  CAS  Google Scholar 

  • Valière N, Bonenfant C, Toigo C, Luikart G, Gaillard JM, Klein F (2007) Importance of a pilot study for non-invasive genetic sampling: genoty** errors and population size estimation in red deer. Conserv Genet 81:69–78

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genoty** errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J Wildl Manag 69:1419–1433

    Article  Google Scholar 

  • Watts SM, McCarthy TM, Namgail T (2019) Modelling potential habitat for snow leopards (Panthera uncia) in Ladakh, India. PLoS ONE 14:e0211509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge the support and permission received from the State Forest Department of Himachal Pradesh (letter no. WL/Research Study/WLM/2291). Authors thank to the funded by the National Mission on Himalayan Studies, Ministry of Environment, Forest and Climate Change (MoEf&CC) for funding the project. 

Funding

The research is funded by National Mission for Himalayan Studies, Ministry of Environment, Forest and Climate Change (MoEF&CC), New Delhi, India (Grant No. NMHS/2017–18/LG09/02/476).

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  1. Sujeet Kumar Singh

    Present address: Amity Institute of Forestry and Wildlife, Amity University, Noida, India

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  1. Zoological Survey of India, New Alipore, Kolkata, West Bengal, 700053, India

    Vinaya Kumar Singh, Sujeet Kumar Singh, Bheem Dutt Joshi, Kailash Chandra, Lalit Kumar Sharma & Mukesh Thakur

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Data collection and fieldwork were carried out after obtaining research permission from the State forest department of Himachal Pradesh (letter no. WL/Research Study/WLM/2291).

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Singh, V.K., Singh, S.K., Joshi, B.D. et al. Population genetics of the snow leopards (Panthera uncia) from the Western Himalayas, India. Mamm Biol 102, 263–269 (2022). https://doi.org/10.1007/s42991-021-00196-1

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