Microsatellite analysis reveals low genetic diversity in managed populations of the critically endangered gharial (Gavialis gangeticus) in India
1.
Grigg, G. & Kirshner, D. Biology and Evolution of Crocodylians (CSIRO Publishing, 2015). https://doi.org/10.1071/9781486300679.
Google Scholar
2.
Singh, L. A. K. Ecological studies on the Indian gharial Gavialis gangeticus (Gmelin) (Reptilia, Crocodilia). PhD Thesis, Utkal University, Odisha (1978).
3.
Whitaker, R. The management of crocodilians in India. In Wildlife Management; Crocodiles and Alligators (eds Webb, G. J. W. et al.) 63–72 (Surrey Beatty and Sons, 1987).
Google Scholar
4.
Hussain, S. A. Reproductive success, hatchling survival and rate of increase of gharial Gavialis gangeticus in National Chambal Sanctuary, India. Biol. Conserv. 87, 261–268 (1999).
Article Google Scholar
5.
Bustard, H. R. A future for the Gharial. Cheetal 17, 3–8 (1975).
Google Scholar
6.
Hussain, S. A. Basking site and water depth selection by gharial Gavialis gangeticus Gmelin 1789 (Crocodylia, Reptilia) in National Chambal Sanctuary, India and its implication for river conservation. Aquat. Conserv. Mar. Freshw. Ecosyst. 19, 127–133 (2009).
Article Google Scholar
7.
Lang, J. W., Chowfin, S. & Ross, J. P. Gavialis gangeticus (errata version published in 2019). IUCN Red List Threat. Species 2019 (2019).
8.
Basu, D. Saving the gharial. Indian Wildlifer 1, 7–15 (1981).
Google Scholar
9.
Singh, V. B. The status of the gharial (Gavialis gangeticus) in U.P. and its rehabilitation. J. Bombay Nat. Hist. Soc. 75, 668–683 (1978).
Google Scholar
10.
Stevenson, C. & Whitaker, R. Indian Gharial Gavialis gangeticus. In Crocodiles. Status Survey and Conservation Action Plan (eds Manolis, S. C. & Stevenson, C.) 139–143 (Crocodile Specialist Group, 2010).
Google Scholar
11.
Whitaker, R. & Basu, D. The gharial (Gavialis gangeticus) a review. J. Bombay Nat. Hist. Soc. 79, 531–548 (1982).
Google Scholar
12.
Whitaker, R. The gharial: Going extinct again. Iguana 14, 25–33 (2007).
Google Scholar
13.
Lang, J. W., Jailabdeen, A. & Kumar, P. Gharial ecology project—Update 2018–2019. IUCN-SSC Crocodile Spec. Gr. Newsl. 37, 15–17 (2018).
Google Scholar
14.
IUCN/SSC. Guidelines for Reintroductions and Other Conservation Translocations IUCN. Version 1.0. Gland, Switzerland: IUCN Species Survival Commission viiii + 57 pp. (2013).
15.
Schwartz, M. K. Guidelines on the use of molecular genetics in reintroduction programs. EU LIFE-Nature Proj. to Guidel. reintroduction Threat. species 51–58 (2005).
16.
White, L. C., Moseby, K. E., Thomson, V. A., Donnellan, S. C. & Austin, J. J. Long-term genetic consequences of mammal reintroductions into an Australian conservation reserve. Biol. Conserv. 219, 1–11 (2018).
Article Google Scholar
17.
Weeks, A. R. et al. Assessing the benefits and risks of translocations in changing environments: A genetic perspective. Evol. Appl. 4, 709–725 (2011).
PubMed PubMed Central Article Google Scholar
18.
Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623 (2008).
PubMed Article Google Scholar
19.
Katdare, S. et al. Gharial (Gavialis gangeticus) populations and human influences on habitat on the River Chambal, India. Aquat. Conserv. Mar. Freshw. Ecosyst. 21, 364–371 (2011).
Article Google Scholar
20.
Nair, T., Thorbjarnarson, J. B., Aust, P. & Krishnaswamy, J. Rigorous gharial population estimation in the Chambal: Implications for conservation and management of a globally threatened crocodilian. J. Appl. Ecol. 49, 1046–1054 (2012).
Article Google Scholar
21.
Hussain, S. A. Ecology of gharial (Gavialis gangeticus) in National Chambal Sanctuary. MPhil Thesis, Aligarh Muslim University, Uttar Pradesh (1991).
22.
Sharma, S. P. et al. Mitochondrial DNA analysis reveals extremely low genetic diversity in a managed population of the Critically Endangered Gharial (Gavialis gangeticus, Gmelin 1789). Herpetol. J. 30, 202–206 (2020).
Article Google Scholar
23.
Jogayya, K. N., Meganathan, P. R., Dubey, B. & Haque, I. Novel microsatellite DNA markers for Indian Gharial (Gavialis gangeticus). Conserv. Genet. Resour. 5, 787–790 (2013).
Article Google Scholar
24.
Zhu, H., Wu, X., Xue, H., Wei, L. & Hu, Y. Isolation of polymorphic microsatellite loci from the Chinease alligator (Alligator sinensis). Mol. Ecol. Resour. 9, 892–894 (2009).
CAS PubMed Article PubMed Central Google Scholar
25.
Glenn, T. C. et al. Characterization of microsatellite DNA loci in American alligators. Copeia 3, 591–601 (1998).
Article Google Scholar
26.
Ojeda, G. N., Amavet, P. S., Rueda, E. C., Siroski, P. A. & Larriera, A. Mating system of Caiman yacare (Reptilia: Alligatoridae) described from microsatellite genotypes. J. Hered. 108, 135–141 (2017).
PubMed PubMed Central Google Scholar
27.
Yu, D. et al. Analysis of genetic variation and bottleneck in a captive population of Siamese crocodile using novel microsatellite loci. Conserv. Genet. Resour. 3, 217–220 (2011).
Article Google Scholar
28.
Hinlo, M. R. P. et al. Population genetics implications for the conservation of the Philippine Crocodile Crocodylus mindorensis Schmidt, 1935 (Crocodylia: Crocodylidae). J. Threat. Taxa 6, 5513–5533 (2014).
Article Google Scholar
29.
Mcvay, J. D. et al. Evidence of multiple paternity in Morelet’s Crocodile (Crocodylus moreletii) in Belize, CA, inferred from microsatellite markers. J. Exp. Zool. Part A Ecol. Genet. Physiol. 309, 643–648 (2008).
Article Google Scholar
30.
Dever, J. A., Strauss, R. E., Rainwater, T. R., McMurry, S. T. & Densmore, I. L. D. Genetic diversity, population subdivision, and gene flow in Morelet’s crocodile (Crocodylus moreletii) from Belize, Central America. Copeia 4, 1078–1091 (2002).
Article Google Scholar
31.
Aggarwal, R. K., Lalremruata, A. & Dubey, B. Development of fourteen novel microsatellite markers of Crocodylus palustris, the Indian mugger, and their cross-species transferability in ten other crocodilians. Conserv. Genet. Resour. 7, 197–200 (2014).
Article Google Scholar
32.
Campos, J. C., Mobaraki, A., Abtin, E., Godinho, R. & Brito, J. C. Preliminary assessment of genetic diversity and population connectivity of the Mugger Crocodile in Iran. Amphib. Reptil. 39, 126–131 (2018).
Article Google Scholar
33.
Garner, A., Rachlow, J. L. & Hicks, J. F. Patterns of genetic diversity and its loss in mammalian populations. Conserv. Biol. 19, 1215–1221 (2005).
Article Google Scholar
34.
Rossi, N. A. et al. High levels of population genetic differentiation in the American crocodile (Crocodylus acutus). PLoS ONE 15, e0235288 (2020).
CAS PubMed PubMed Central Article Google Scholar
35.
van Asch, B. et al. Phylogeography, genetic diversity, and population structure of Nile crocodile populations at the fringes of the southern African distribution. PLoS ONE 14, 1–20 (2019).
Google Scholar
36.
Luck, N. L. et al. Mitochondrial DNA analyses of the saltwater crocodile (Crocodylus porosus) from the Northern Territory of Australia. Aust. J. Zool. 60, 18–25 (2012).
Article Google Scholar
37.
Russello, M. A., Brazaitis, P., Gratten, J., Watkins-Colwell, G. J. & Caccone, A. Molecular assessment of the genetic integrity, distinctiveness and phylogeographic context of the Saltwater crocodile (Crocodylus porosus) on Palau. Conserv. Genet. 8, 777–787 (2007).
CAS Article Google Scholar
38.
Ray, D. A. et al. Low levels of nucleotide diversity in Crocodylus moreletiiand evidence of hybridization with C. acutus. Conserv. Genet. 5, 449–462 (2004).
CAS Article Google Scholar
39.
Eckert, C. G., Samis, K. E. & Lougheed, S. C. Genetic variation across species’ geographical ranges: The central-marginal hypothesis and beyond. Mol. Ecol. 17, 1170–1188 (2008).
CAS PubMed Article PubMed Central Google Scholar
40.
Ellegren, H. & Galtier, N. Determinants of genetic diversity. Nat. Rev. Genet. 17, 422–433 (2016).
CAS PubMed Article Google Scholar
41.
Romiguier, J. et al. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515, 261–263 (2014).
ADS CAS PubMed Article Google Scholar
42.
Allendorf, F. W. & Luikart, G. Conservation and the Genetics of Populations (Blackwell Publishing, 2007).
Google Scholar
43.
Guries, R. P. & Ledig, F. T. Genetic structure of populations and differentiation in forest trees. in Conkle, MT (tech. coord.) Proceedings of the symposium on isozymes of North American forest trees and forest insects. USDA For. Serv. Gen. Tech. Rep. PSW-48 42–47 (1979).
44.
Biebach, I. & Keller, L. F. Inbreeding in reintroduced populations: The effects of early reintroduction history and contemporary processes. Conserv. Genet. 11, 527–538 (2010).
Article Google Scholar
45.
Wang, J. Estimating pairwise relatedness in a small sample of individuals. Heredity (Edinb). 119, 302–313 (2017).
CAS PubMed PubMed Central Article Google Scholar
46.
Degiorgio, M. & Rosenberg, N. A. An unbiased estimator of gene diversity in samples containing related individuals p. Mol. Biol. Evol. 26, 501–512 (2008).
PubMed PubMed Central Article CAS Google Scholar
47.
Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94 (2010).
PubMed PubMed Central Article Google Scholar
48.
Girod, C., Vitalis, R., Leblois, R. & Fréville, H. Inferring population decline and expansion from microsatellite data: A simulation-based evaluation of the msvar method. Genetics 188, 165–179 (2011).
PubMed PubMed Central Article Google Scholar
49.
Luikart, G. & Cornuet, J. M. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12, 228–237 (1998).
Article Google Scholar
50.
Keller, L. F. et al. Immigration and the ephemerality of a natural population bottleneck: Evidence from molecular markers. Proc. R Soc. London. Ser. B Biol. Sci. 268, 1387–1394 (2001).
CAS Article Google Scholar
51.
Cristescu, R., Sherwin, W. B., Handasyde, K., Cahill, V. & Cooper, D. W. Detecting bottlenecks using BOTTLENECK 1.2.02 in wild populations: The importance of the microsatellite structure. Conserv. Genet. 11, 1043–1049 (2010).
Article Google Scholar
52.
Peery, M. Z. et al. Reliability of genetic bottleneck tests for detecting recent population declines. Mol. Ecol. 21, 3403–3418 (2012).
PubMed Article PubMed Central Google Scholar
53.
Hoban, S. M., Gaggiotti, O. E. & Bertorelle, G. The number of markers and samples needed for detecting bottlenecks under realistic scenarios, with and without recovery: A simulation-based study. Mol. Ecol. 22, 3444–3450 (2013).
PubMed Article PubMed Central Google Scholar
54.
Cornuet, J. M. & Luikart, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014 (1996).
CAS PubMed PubMed Central Article Google Scholar
55.
Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 1989).
Google Scholar
56.
Miquel, C. et al. Quality indexes to assess the reliability of genotypes in studies using noninvasive sampling and multiple-tube approach. Mol. Ecol. Notes 6, 985–988 (2006).
Article Google Scholar
57.
Oaks, J. R. A time-calibrated species tree of Crocodylia reveals a recent radiation of the true crocodiles. Evolution (N.Y.) 65, 3285–3297 (2011).
Google Scholar
58.
Broquet, T. & Petit, E. Quantifying genotyping errors in noninvasive population genetics. Mol. Ecol. 13, 3601–3608 (2004).
CAS PubMed Article Google Scholar
59.
Chapuis, M. P. & Estoup, A. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621–631 (2007).
CAS PubMed Article Google Scholar
60.
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M. & Shipley, P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538 (2004).
Article CAS Google Scholar
61.
Valière, N. GIMLET: A computer program for analysing genetic individual identification data. Mol. Ecol. Notes 2, 377–379 (2002).
Google Scholar
62.
Peakall, R. & Smouse, P. E. GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537–2539 (2012).
CAS PubMed PubMed Central Article Google Scholar
63.
Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106 (2007).
PubMed Article PubMed Central Google Scholar
64.
Kalinowski, S. T. HP-RARE 1.0—A computer program for performing rarefaction on measures of allelic richness.pdf. Mol. Ecol. Notes 5, 187–189 (2005).
CAS Article Google Scholar
65.
Weir, B. S. & Cockerham, C. Estimating F-statistics for the analysis of population structure. Evolution (N. Y.). 38, 1358–1370 (1984).
CAS Google Scholar
66.
Hedrick, P. W. A standardized genetic differentiation measure. Evolution (N. Y.). 59, 1633–1638 (2005).
CAS Google Scholar
67.
Jost, L. GST and its relatives do not measure differentiation. Mol. Ecol. 17, 4015–4026 (2008).
PubMed Article PubMed Central Google Scholar
68.
Archer, F. I., Adams, P. E. & Schneiders, B. B. stratag: An r package for manipulating, summarizing and analysing population genetic data. Mol. Ecol. Resour. 17, 5–11 (2017).
CAS PubMed Article PubMed Central Google Scholar
69.
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data: Dominant markers and null alleles. Genetics 155, 945–959 (2000).
CAS PubMed PubMed Central Google Scholar
70.
Hubisz, M. J., Falush, D., Stephens, M. & Pritchard, J. K. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9, 1322–1332 (2009).
PubMed PubMed Central Article Google Scholar
71.
Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620 (2005).
CAS PubMed Article Google Scholar
72.
Earl, D. A. & VonHoldt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012).
Article Google Scholar
73.
Rosenberg, N. A. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138 (2004).
Article Google Scholar
74.
Wilson, G. A. & Rannala, B. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163, 1177–1191 (2003).
PubMed PubMed Central Google Scholar
75.
Excoffier, L., Laval, G. & Schneider, S. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinforma. Online. 1, 47–50 (2005).
CAS Google Scholar
76.
Piry, S., Luikart, G. & Cornuet, J. M. BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90, 502–503 (1999).
Article Google Scholar
77.
Garza, J. C. & Williamson, E. G. Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10, 305–318 (2001).
CAS PubMed Article Google Scholar
78.
Di Rienzo, A. et al. Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. USA 91, 3166–3170 (1994).
ADS PubMed Article Google Scholar
79.
Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).
CAS PubMed PubMed Central Article Google Scholar
80.
Hall, T. A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp. Ser. 41, 95–98 (1999).
CAS Google Scholar
81.
Librado, P. & Rozas, J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452 (2009).
CAS Article Google Scholar More