Management implications of genetic studies for ex situ populations of three critically endangered Asian Gyps vultures

Animal Conservation

Volumn 18, Issue 3, 2015, Pages 259-270

  Ishtiaq, F ^a,f   Prakash, V ^b   Green, R E ^c,d   Johnson, J ^e  

^a WILDLIFE INSTITUTE OF INDIA   (India)

^b BOMBAY NATURAL HISTORY SOCIETY   (India)

^c RSPB CENTRE FOR CONSERVATION SCIENCE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF NORTH TEXAS   (United States)

^f INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Captive breeding; bottleneck; ex situ; genetic diversity; Heterozygosity; India; Population management; Relatedness

Indexed keywords

BIRD; BREEDING POPULATION; CAPTIVE BREEDING; CONSERVATION MANAGEMENT; DEMOGRAPHY; ENDANGERED SPECIES; POPULATION BOTTLENECK; POPULATION GENETICS; RELATEDNESS; SPECIES CONSERVATION;

INDIA; PAKISTAN;

AVES; GYPS; GYPS BENGALENSIS;

EID: 84930389683     PISSN: 13679430     EISSN: 14691795     Source Type: Journal    
DOI: 10.1111/acv.12166     Document Type: Article

References (90)

1. Aguilar, A., Roemer, G., Debenham, S., Binns, M., Garcelon, D. & Wayne, R.K. (2004). High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc. Natl. Acad. Sci. USA 101, 3490-3494.
2. Arshad, M., Pedall, I., Gonzalez, J. & Wink, M. (2009). Genetic variation of four Gyps species (Gyps bengalensis, G.africanus, G.indicus and G.fulvus) based on microsatellite analysis. J. Raptor. Res. 43, 227-236.
3. Ballou, J.D. & Lacy, R.C. (1995). Identifying genetically important individuals for management of genetic diversity in pedigreed populations. In Population management for survival and recovery. Analytical methods and strategies in small population conservation: 76-111. Ballou, J.D., Gilpin, M. & Foose, T.J. (Eds). New York: Columbia University Press.
4. Balmford, A., Mace, G.M. & Leader-Williams, N. (1996). Designing the ark: setting priorities for captive breeding. Conserv. Biol. 10, 719-727.
5. Baral, H.S., Giri, J.B. & Virani, M.Z. (2004). On the decline of oriental white-backed vultures Gyps bengalensis in lowland Nepal. In Raptors worldwide: 215-219. Chancellor, R.D. & Meyburg, B.-U. (Eds). Berlin: WWGBP/MME (BirdLife Hungary).
6. BirdLife International (2010). Gyps bengalensis. IUCN Red List of Threatened Species 2011. Version 2011.2. IUCN. http://www.iucnredlist.org (accessed on 4 January 2012).
7. Blouin, M.S., Parsons, M., Lacaille, V. & Lotz, S. (1996). Use of microsatellite loci to classify individuals by relatedness. Mol. Ecol. 5, 393-401.
8. Bouman, J. (1977). The future of Przewalski horses (Equus przewalskii) in captivity. Int. Zoo Yb. 17, 62-68.
9. Bourke, B.P., Frantz, A.C., Lavers, C.P., Davison, A., Dawson, D.A. & Burke, T.A. (2010). Genetic signatures of population decline in the British golden eagle (Aquila chrysaetos). Conserv. Genet. 11, 1837-1846.
10. Bowkett, A.E. (2009). Recent captive-breeding proposals and the return of the ark concept to global species conservation. Conserv. Biol. 23, 773-776.
11. Clements, T., Gilbert, M., Rainey, H.J., Cuthbert, R., Eames, J.C., Bunnat, P., Teak, S., Chansocheat, S. & Setha, T. (2013). Vultures in Cambodia: population, threats and conservation. Bird Conserv. Int. 23, 7-24.
12. Cornuet, J.M. & Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001-2014.
13. Cuthbert, R.J., Dave, R., Chakrabortya, S.S., Kumar, S., Prakash, S., Ranade, S.P. & Prakash, V. (2011a). Assessing the ongoing threat from veterinary non-steroidal anti-inflammatory drugs to critically endangered Gyps vultures in India. Oryx 45, 420-426.
14. Cuthbert, R., Taggart, M.A., Prakash, V., Saini, M., Swarup, D., Upreti, S., Mateo, R., Chakraborty, S.S., Deori, P. & Green, R.E. (2011b). Effectiveness of action in India to reduce exposure of Gyps vultures to the toxic veterinary drug diclofenac. PLoS ONE 6, e19069.
15. Edmands, S. (2007). Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol. Ecol. 16, 463-475.
16. Eimes, J.A., Bollmer, J.L., Whittingham, L.A., Johnson, J.A., Van Oosterhout, C. & Dunn, P.O. (2011). Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation. J. Evol. Biol. 24, 1847-1856.
17. Ejsmond, M. & Radwan, J. (2011). MHC diversity in bottlenecked populations: a simulation model. Conserv. Genet. 12, 129-137.
18. 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.
19. Excoffier, L., Laval, G. & Schneider, S. (2005). Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47-50.
20. Foose, T.J. & Ballou, J.D. (1988). Population management: theory and practice. Int. Zoo Yb. 27, 26-41.
21. Foose, T., Lande, N.R., Flesness, G., Rabb, G. & Read, B. (1986). Propagation plans. Zoo Biol. 5, 139-146.
22. Frankham, R. (2008). Genetic adaptation to captivity in species conservation programs. Mol. Ecol. 17, 325-333.
23. Frankham, R., Ballou, J.D. & Briscoe, D.A. (2002). Introduction to conservation genetics: Cambridge: Cambridge University Press.
24. Frankham, R., Ballou, J.D., Eldridge, M.D.B., Lacy, R.C., Ralls, K., Dudash, M.R. & Fenster, C.B. (2011). Predicting the probability of outbreeding depression. Conserv. Biol. 25, 465-475.
25. Garza, J.C. & Williamson, E.G. (2001). Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10, 305-318.
26. Gautschi, B., Tenzer, I., Müller, J.P. & Schmid, B. (2000). Isolation and characterization of microsatellite loci in the bearded vulture (Gypaetus barbatus) and cross-amplification in three old world vulture species. Mol. Ecol. 9, 2193-2195.
27. Gautschi, B., Jacob, G., Negro, J.J., Godoy, J.A., Müller, J. & Schmid, B. (2003). Analysis of relatedness and determination of the source of founders in the captive bearded vulture, Gypaetus barbatus, population. Conserv. Genet. 4, 479-490.
28. Gilbert, M., Watson, R.T., Ahmed, S., Asim, M. & Johnson, J.A. (2007). Vulture restaurants and their role in reducing diclofenac exposure in Asian vultures. Bird Conserv. Int. 17, 63-77.
29. Gilbert, M.J., Oaks, L., Virani, M.Z., Watson, R.T., Ahmed, S., Chaudhry, M.J.I., Arshad, M., Mahmood, S., Ali, A., Khattak, R.M. & Khan, A.A. (2004). The status and decline of vultures in the provinces of Punjab and Sind, Pakistan: a 2003 update. In Raptors worldwide: 221-234. Chancellor, R.C. & Meyburg, B.-U. (Eds). Berlin: World Working Group on Birds of Prey/MME-BirdLife Hungary.
30. Gonçalves da Silva, A. & Russello, M.A. (2009). iRel v1.0: an online tool for estimating relatedness. http://www.gentools.ecgl.ok.ubc.ca:8080/webMathematica/irel/irel.html (accessed on 27 August 2011).
31. Goudet, J. (2001). Fstat, a computer program to estimate and test gene diversities and fixation indices. Version 2.9.3.2. http://www2.unil.ch/popgen/softwares/fstat.htm (accessed on September 2011).
32. Green, R.E., Newton, I., Shultz, S., Cunningham, A.A., Gilbert, M., Pain, D.J. & Prakash, V. (2004). Diclofenac poisoning as a cause of vulture population declines across the Indian subcontinent. J. Appl. Ecol. 41, 793-800.
33. Green, R.E., Taggart, M.A., Das, D., Pain, D.J., Kumar, S., Cunningham, A.A. & Cuthbert, R. (2006). Collapse of Asian vulture populations: risk of mortality from residues of the veterinary drug diclofenac in carcasses of treated cattle. J. Appl. Ecol. 43, 949-956.
34. Hailer, F., Helander, B., Folkestad, A.O., Ganusevich, S.A., Garstad, S., Hauff, P., Koren, C., Nygård, T., Volke, V., Vilà, C. & Ellegren, H. (2006). Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol. Lett. 2, 316-319.
35. Hammerly, S.C., Morrow, M.E. & Johnson, J.A. (2013). A comparison of pedigree- and DNA-based measures for identifying inbreeding depression in the critically endangered Attwater's Prairie-chicken. Mol. Ecol. 22, 5313-5328.
36. Hedrick, P.W. (2001). Conservation genetics: where are we now? Trends Ecol. Evol. 16, 629-636.
37. Hedrick, P.W. & Miller, P. (1992). Conservation genetics: theory and management of captive populations. In Conservation of biodiversity for sustainable development: 70-87. Sandlund, O.T., Hindar, K. & Brown, A.H.D. (Eds). Oslo: Scandinavian University Press.
38. Hoban, S.M., Gaggiotti, O.E. & Bertorelle, G. (2013). 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.
39. Houston, D.C. (1985). Indian white-backed vulture (Gyps bengalensis). In Conservation studies on raptors, technical publication no. 5: 465-466. Newton, I. & Chancellor, R. (Eds). Cambridge: International Council for Bird Preservation.
40. Ivy, J.A. & Lacy, R.C. (2012). A comparison of strategies for selecting breeding pairs to maximize genetic diversity retention in managed populations. J. Hered. 103, 186-196.
41. Ivy, J.A., Miller, A., Lacy, R.C. & DeWoody, J.A. (2009). Methods and prospects for using molecular data in captive breeding programs: an empirical example using parma wallabies (Macropus parma). J. Hered. 100, 441-454.
42. Johnson, J.A., Gilbert, M., Virani, M.Z., Asim, M. & Mindell, D.P. (2008). Temporal genetic analysis of the critically endangered oriental white-backed vulture in Pakistan. Biol. Conserv. 141, 2403-2409.
43. Kennedy, E.S., Grueber, C.E., Duncan, R.P. & Jamieson, I.G. (2014). Severe inbreeding depression and no evidence of purging in an extremely inbred wild species - the Chatham Island black robin. Evolution 68, 987-995.
44. Lacy, R.C. (1987). Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv. Biol. 1, 143-158.
45. Lacy, R.C. (1989). Analysis of founder representation in pedigrees: founder equivalents and founder genome equivalents. Zoo Biol. 8, 111-123.
46. Lacy, R.C. (1994). Managing genetic diversity in captive populations of animals. In Restoration and recovery of endangered plants and animals: 63-89. Bowles, M.L. & Whelan, C.J. (Eds). Cambridge: Cambridge University Press.
47. Landguth, E.L., Cushman, S.A., Schwartz, M.K., McKelvey, K.S., Murphy, M. & Luikart, G. (2010). Quantifying the lat time to detect barriers in landscape genetics. Mol. Ecol. 19, 4179-4191.
48. Lawrence, H.A., Taylor, G.A., Millar, C.D. & Lambert, D.M. (2008). High mitochondrial and nuclear genetic diversity in one of the world's most endangered seabirds, the Chatham Island Taiko (Pterodroma magentae). Conserv. Genet. 9, 1293-1301.
49. Leberg, P.L. (2002). Estimating allelic richness: effects of sample size and bottlenecks. Mol. Ecol. 11, 2445-2449.
50. Leberg, P.L. & Firmin, B.D. (2008). Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol. Ecol. 17, 334-343.
51. Lewis, P.O. & Zaykin, D. (2001). Genetic data analysis: computer program for the analysis of allelic data. Version 1.0 (d16c). Free program distributed by the authors over the Internet from http://lewis.eeb.uconn.edu/lewishome/software.html (accessed on September 2011).
52. Lippé, C., Dumont, P. & Bernatchez, L. (2006). High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae, Pisces): the positive sides of a long generation time. Mol. Ecol. 15, 1769-1780.
53. Luikart, G., Cornuet, J.-M. & Allendorf, F.W. (1999). Temporal changes in allele frequencies provide estimates of population bottleneck size. Conserv. Biol. 13, 523-530.
54. Lynch, M. & Ritland, K. (1999). Estimation of pairwise relatedness with molecular markers. Genetics 152, 1753-1766.
55. Margan, S.H., Nurthen, R.K., Montgomery, M.E., Woodworth, L.M., Lowe, E.H., Briscoe, D.A. & Frankham, R. (1998). Single large or several small? Population fragmentation in the captive management of endangered species. Zoo Biol. 17, 467-480.
56. Mira, S., Billot, C., Guillemaud, T., Palma, L. & Cancela, M.L. (2002). Isolation and characterization of polymorphic microsatellite markers in Eurasian vulture Gyps fulvus. Mol. Ecol. Notes 2, 557-558.
57. Newton, I. (1979). Population ecology of raptors. Vermillion: Buteo Books; Hertfordshire: T. & A. D. Poyser Ltd.
58. Nicholls, J.A., Double, M.C., Rowell, D.M. & Magrath, R.D. (2000). The evolution of cooperative and pair breeding in thornbills Acanthiza (Paradalotidae). J. Avian. Biol. 31, 165-176.
59. Niel, C. & Lebreton, J.-D. (2005). Using demographic invariants to detect overharvested bird populations from incomplete data. Conserv. Biol. 19, 826-835.
60. Oaks, J.L., Gilbert, M., Virani, M.Z., Watson, R.T., Meteyer, C.U., Rideout, B., Shivaprasad, H.L., Ahmed, S., Chaudhry, M.J.I., Arshad, M., Mahmood, S., Ali, A. & Khan, A.A. (2004). Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427, 630-633.
61. Pain, D.J., Bowden, C.G.R., Cunningham, A.A., Cuthbert, R., Das, D., Gilbert, M., Jakati, R.D., Jhala, Y., Khan, A.A., Naidoo, V., Oaks, J.L., Parry-Jones, J., Prakash, V., Rahmani, A., Ranade, S.P., Baral, H.S., Senacha, K.R. & Saravanan, S. (2008). The race to prevent the extinction of South Asian vultures. Bird Conserv. Int. 18, S30-S48.
62. Peery, M.Z., Kirby, R., Reid, B.N., Stoelting, R., Doucet-Bëer, E., Robinson, S., Vásquez-Carrillo, C., Pauli, J.N. & Palsbøll, P.J. (2012). Reliability of genetic bottleneck tests for detecting recent population declines. Mol. Ecol. 21, 3403-3418.
63. Pemberton, J. (2004). Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol. Evol. 19, 613-615.
64. Pemberton, J. (2008). Wild pedigrees: the way forward. Proc. Roy. Soc. Lond. Ser. B. 275, 613-621.
65. Piry, S., Luikart, G. & Cornuet, J.M. (1999). Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90, 502-550.
66. Pittman, S.E., King, T.L., Faurby, S. & Dorcas, M.E. (2011). Demographic and genetic status of an isolated population of bog turtles (Glyptemys muhlenbergii): implications for managing small populations of long-lived animals. Conserv. Genet. 12, 1589-1601.
67. Prakash, V., Green, R.E., Pain, D.J., Ranade, S.P., Saravanan, S., Prakash, N., Venkitachalam, R., Cuthbert, R., Rahmani, A.R. & Cunningham, A.A. (2007). Recent changes in populations of resident Gyps vultures in India. J. Bombay Nat. Hist. Soc. 104, 129-135.
68. Prakash, V., Bishwakarma, M.C., Chaudhary, A., Cuthbert, R., Dave, R., Kulkarni, M., Kumar, S., Paudel, K., Ranade, S., Shringarpure, R. & Green, R.E. (2012). The population decline of Gyps vultures in India and Nepal has slowed since veterinary use of diclofenac was banned. PLoS ONE 7, e49118.
69. Pritchard, J.K., Stephens, M. & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945-959.
70. Queller, D.C. & Goodnight, K.F. (1989). Estimating relatedness using genetic markers. Evolution 43, 258-275.
71. Ralls, K. & Ballou, J. (1986). Captive breeding programs for populations with a small number of founders. Trends Ecol. Evol. 1, 19-22.
72. Ralls, K. & Ballou, J. (2004). Genetic status and management of California condors. Condor 106, 215-228.
73. Ralls, K., Brugger, K. & Ballou, J.D. (1979). Inbreeding and juvenile mortality in small populations of ungulates. Science 206, 1101-1103.
74. Reed, D.H. & Frankham, R. (2001). How closely correlated are molecular and quantitative measures of genetic diversity: a meta-analysis. Evolution 55, 1095-1103.
75. Rice, W.R. (1989). Analysing tables of statistical tests. Evolution 43, 223-225.
76. Robert, A. (2009). Captive breeding genetics and reintroduction success. Biol. Conserv. 142, 2915-2922.
77. Rudnick, J.A. & Lacy, R.C. (2008). The impact of assumptions about founder relationships on the effectiveness of captive breeding strategies. Conserv. Genet. 9, 1439-1450.
78. Russello, A. & Amato, G. (2004). Ex situ population management in the absence of pedigree information. Mol. Ecol. 13, 2829-2840.
79. Shultz, S., Baral, H.S., Charman, S., Cunningham, A.A., Das, D., Ghalsasi, D.R., Goudar, M.S., Green, R.E., Jones, A., Nighot, P., Pain, D.J. & Prakash, V. (2004). Diclofenac poisoning is widespread in declining vulture populations across the Indian subcontinent. Proc. Roy. Soc. Lond. Ser. B. (Suppl.) 271, S458-S460.
80. Snyder, N.F.R., Derrickson, S.R., Beissinger, S.R., Wiley, J.W., Smith, T.B., Toone, W.D. & Miller, B. (1996). Limitations of captive breeding in endangered species recovery. Conserv. Biol. 10, 338-348.
81. Spencer, C.C., Neigel, J.E. & Leberg, P.L. (2000). Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol. Ecol. 9, 1517-1528.
82. Sutton, J.T., Nakagawa, S., Robertson, B.C. & Jameison, I.G. (2011). Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol. Ecol. 20, 4408-4420.
83. Swan, G.E., Cuthbert, R., Quevedo, M., Green, R.E., Pain, D.J., Bartels, P., Cunningham, A.A., Duncan, N., Meharg, A.A., Oaks, J.L., Parry-Jones, J., Shultz, S., Taggart, M.A., Verdoorn, G. & Wolter, K. (2006). Toxicity of diclofenac to Gyps vultures. Biol. Lett. 2, 279-282.
84. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535-538.
85. Weir, B.S. & Cockerham, C.C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370.
86. Willi, Y., Griffin, P. & Van Buskirk, J. (2013). Drift load in populations of small size and low density. Heredity 110, 296-302.
87. Williams, S.E. & Hoffman, E.A. (2009). Minimizing genetic adaptation in captive breeding programs: a review. Biol. Conserv. 142, 2388-2400.
88. Williamson-Natesan, E.G. (2005). Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv. Genet. 6, 551-562.
89. Willis, K. & Willis, R.E. (2010). How many founders, how large a population? Zoo Biol. 29, 638-646.
90. Witzenberger, K.A. & Hockkirch, A. (2011). Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers. Conserv. 20, 1843-1861.