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Standardization and Validation of a Panel of Cross-Species Microsatellites To bioRxiv preprint doi: https://doi.org/10.1101/447201; this version posted October 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Standardization and validation of a panel of cross-species microsatellites to 2 individually identify the Asiatic wild dog (Cuon alpinus): implications in 3 population estimation and dynamics 4 * * *# 5 Shrushti Modi , Bilal Habib , Pallavi Ghaskadbi, Parag Nigam, Samrat Mondol 6 7 Email: 8 [email protected] 9 [email protected] 10 [email protected] 11 [email protected] 12 [email protected] 13 14 Affiliation: Wildlife Institute of India, Chandrabani, Dehradun, Uttarakhand, India 248001 15 *Equal contribution 16 17 #Corresponding author: Samrat Mondol, Animal Ecology and Conservation Biology 18 Department, Wildlife Institute of India, Chandrabani, Dehradun, Uttarakhand, India 248001 19 Email: [email protected] 20 21 22 23 24 25 Keywords: Dhole, individual identification, non-invasive sampling, genetic connectivity, 26 population parameters, Maharashtra tiger landscape 1 bioRxiv preprint doi: https://doi.org/10.1101/447201; this version posted October 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 27 Abstract 28 Background 29 The Asiatic wild dog or dhole (Cuon alpinus) is a highly elusive, monophyletic, forest 30 dwelling, social canid distributed across south and Southeast Asia. Severe pressures from 31 habitat loss, prey depletion, disease, human persecution and interspecific competition resulted 32 in global population decline in dholes. Despite a declining population trend, detailed 33 information on population size, ecology, demography and genetics is lacking. Generating 34 reliable information and landscape level for dholes is challenging due to their secretive 35 behaviour and monomorphic physical features. Recent advances in non-invasive DNA-based 36 tools can be used to monitor populations and individuals across large landscapes. In this 37 paper, we describe standardization and validation of faecal DNA-based methods for 38 individual identification of dholes. We tested this method on field-collected dhole faeces in 39 four tiger reserves of the central Indian landscape in the state of Maharashtra, India. Further, 40 we conducted preliminary analyses of dhole population structure and demography in the 41 study area. 42 Results 43 We tested a total of 18 cross-species markers and developed a panel of 12 markers for 44 unambiguous individual identification of dholes. This marker panel identified 101 unique 45 individuals from faecal samples collected across our pilot field study area. These loci showed 46 varied level of amplification success (57-88%), polymorphism (3-9 alleles), heterozygosity 47 (0.23-0.63) and produced a cumulative probability of identity (unbiased) and probability of -10 -4 48 identity (sibs) value of 4.7x10 and 1.5x10 , respectively. Our preliminary analyses of 49 population structure indicated four genetic subpopulations in dholes. Qualitative analyses of 50 population demography show signal of population decline. 2 bioRxiv preprint doi: https://doi.org/10.1101/447201; this version posted October 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 51 Conclusion 52 Our results demonstrated that the selected panel of 12 microsatellite loci can conclusively 53 identify dholes from poor quality, non-invasive biological samples and help in exploring 54 various population parameters. Our methods can be used to estimate dhole populations and 55 assess population trends for this elusive, social carnivore. 56 3 bioRxiv preprint doi: https://doi.org/10.1101/447201; this version posted October 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 57 Introduction 58 The Asiatic wild dog or dhole (Cuon alpinus) is a highly elusive, endangered, social canid 59 distributed in south and southeast Asia [1, 2] occupying a range of habitat types including 60 alpine, temperate, sub-tropical and tropical forests [2]. Driven by habitat loss, prey depletion, 61 disease transmission from domestic dog, human persecution and interspecific competition [3, 62 4], dholes are currently found in about 75% of their historical global range [2, 4]. Global 63 dhole population is roughly estimated to be about 4500-10500 with only 949-2215 mature 64 individuals, but accurate estimates and population trends are not available from any part of its 65 range [4]. They are considered as ‘Endangered’ by IUCN under criteria C2a(i) and Appendix 66 II of the Convention on International Trade in Endangered Species (CITES). The Indian 67 subcontinent currently retains majority of the remaining dhole populations [4], where the 68 species has faced about 60% decline in their historical distribution [5]. The Western Ghats 69 and central Indian forests of the subcontinent still holds majority of the remaining dhole 70 population in India[6], whereas small populations are found in the Eastern Ghats [6], 71 northeast India [7, 8] and Himalayan region [9]. Given the current anthropogenic disturbance 72 scenario across its range, the future survival of this monotypic genus depends on integrated 73 conservation measures involving detailed, accurate information on ecology, demography and 74 genetics. 75 However, generating reliable information for this elusive, forest-dwelling and pack-living 76 canid at landscape scale is challenging. Traditional ecological techniques such as regular 77 photographic capture approach is ineffective for dholes due to absence of unique coat 78 patterns and their monomorphic forms, and physical tagging methods are impractical at 79 landscape scales due to logistical difficulties, high costs and small numbers of captures 80 possible. In this context, genetic tools have tremendous potential to generate critical 81 information (for example, population size estimation [10], phylogeography [11, 12], pack 4 bioRxiv preprint doi: https://doi.org/10.1101/447201; this version posted October 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 82 dynamics and reproductive fitness [13, 14], dispersal patterns [15, 16] etc.) for elusive 83 species conservation across large landscapes [17]. The ability to identify individuals from 84 non-invasive samples collected over large space provide a feasible option to generate detailed 85 information on elusive, forest-dwelling dholes as they cannot be identified using other 86 approaches. 87 In this study, we addressed key methodological issues related to selection and standardization 88 of a set of molecular markers for individual identification of dholes. Subsequently, we tested 89 these markers on field-collected dhole samples from three tiger reserves of the central Indian 90 landscape in the state of Maharashtra, India for individual identification and conducted 91 preliminary analyses of population parameters this this landscape. In addition to the utility of 92 these markers in dhole population estimation at landscape level, we believe that this approach 93 has wider relevance in non-invasive, fecal DNA based population assessments of many other 94 low density, elusive, wide-ranging species. 95 Methods 96 Research permits and ethical considerations 97 All required permissions for fieldwork and sampling were provided by the Maharashtra 98 Forest Department (Permit No. 09/2016). The entire study was non-invasive through field- 99 collected faecal samples, and thus did not require any ethical clearance from the institute. 100 Study Area 101 The study was focused in five protected areas Melghat Tiger Reserve (MTR), Pench Tiger 102 Reserve (PTR), Navegaon-Nagzira Tiger Reserve (NNTR), Tadoba-Andhari Tiger Reserve 103 (TATR) and Umred-Karandhla Wildlife Sanctuary (UKWLS) of the central Indian landscape 104 in the state of Maharashtra, India. The entire area is a complex of forested areas (core zone) 105 with different levels of connectivity. NNTR and PTR are geographically closer as compared 106 to MTR-NNTR and MTR-PTR. MTR and PTR are part of the Satpura-Maikal-Pench corridor 5 bioRxiv preprint doi: https://doi.org/10.1101/447201; this version posted October 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 107 in the Satpura-Maikal landscape. The forest type is of dry deciduous to moist deciduous 108 nature with major vegetation consisting Tectona grandis, Anogeissus latifolia, Lagerstroemia 109 parviflora, Terminalia spp., Heteropogon contortus, Themeda quadrivalvis, Cynodon 110 dactylon etc. 111 Field Sampling 112 Dholes prefer dense forested habitats [18] where the social groups defecate in communal 113 latrine sites [1]. Their elusive nature and highly social behaviour presents unique challenges 114 in scat sampling for individual identification. In this study, sampling was conducted through 115 intensive foot and vehicle surveys covering the entire study area to identify dhole latrine 116 sites. Once the site is found, one bolus from each fresh scat was collected considering from 117 one individual. Separate gloves were used to collect each sample. All samples were collected 118 directly in wax paper and stored in separate ziplock bags.
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