A pedigree gone bad: increased offspring survival after using DNA-based relatedness to minimize inbreeding in a captive population

Animal Conservation

Volumn 19, Issue 3, 2016, Pages 296-303

  Hammerly, S C ^a   de la Cerda, D A ^a   Bailey, H ^b   Johnson, J A ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

^b Houston Zoo   (United States)

Author keywords

captive breeding; ex situ population; inbreeding; mean kinship; microsatellite DNA; pedigree; relatedness

Indexed keywords

CAPTIVE BREEDING; CAPTIVE POPULATION; CONSERVATION GENETICS; DNA; ENDANGERED SPECIES; GAMEBIRD; INBREEDING; KINSHIP; SURVIVAL;

TYMPANUCHUS; TYMPANUCHUS CUPIDO ATTWATERI;

EID: 84953791706     PISSN: 13679430     EISSN: 14691795     Source Type: Journal    
DOI: 10.1111/acv.12247     Document Type: Article

References (57)

1. Ballou, J.D. & Lacy, R.C. (1995). Identifying genetically important individuals for management of genetic variation 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.
2. Bergner, L.M., Jamieson, I.G. & Robertson, B.C. (2014). Combining genetic data to identify relatedness among founders in a genetically depauperate parrot, the Kakapo (Strigops habroptilus). Conserv. Genet. 15, 1013–1020.
3. Bilski, D.R., Pie, M.R. & Passos, F.C. (2013). Variable inbreeding effects across life-history stages in a captive carnivorous mammal population. Anim. Conserv. 16, 633–640.
4. Blouin, M.S. (2003). DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol. Evol. 18, 503–511.
5. Boakes, E.H., Wang, J. & Amos, W. (2007). An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98, 172–182.
6. Bouzat, J.L., Cheng, H., Lewin, H.A., Westemeier, R.L., Brawn, J.D. & Paige, K.N. (1998). Genetic evaluation of a demographic bottleneck in the Greater Prairie Chicken. Conserv. Biol. 12, 836–843.
7. Caizergues, A., Dubois, S., Mondor, G. & Rasplus, J.Y. (2001). Isolation and characterisation of microsatellites loci in black grouse (Tetrao tetrix). Mol. Ecol. Notes 1, 36–38.
8. Charlesworth, D. & Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 237–268.
9. Conde, D.A., Colchero, F., Gusset, M., Pearce-Kelly, P., Byers, O., Flasness, N., Browne, R.K. & Jones, O.R. (2013). Zoos through the lens of the IUCN Red List: a global metapopulation approach to support conservation breeding programs. PLoS ONE 8, e80311. (Online DOI:10.1371/journal.pone.0080311)
10. Csillery, K., Johnson, T., Beraldi, D., Clutton-Brock, T., Coltman, D., Hansson, B., Spong, G. & Pemberton, J.M. (2006). Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics 173, 2091–2101.
11. Engelsma, K.A., Veerkamp, R.K., Calus, M.P.L. & Windig, J.J. (2011). Consequences for diversity when prioritizing animals for conservation with pedigree or genomic information. J. Anim. Breed. Genet. 128, 473–481.
12. Fernández, J., Clemente, I., Amador, C., Membrillo, A., Azor, P. & Molina, A. (2012). Use of different sources of information for the recovery and genetic management of endangered populations: example with the extreme case of Iberian pig Dorado strain. Livest. Sci. 149, 282–288.
13. Ferrie, G.M., Cohen, O.R., Schutz, P., Leighty, K.A., Plasse, C., Bettinger, T.L. & Hoffman, E.A. (2013). Identifying parentage using molecular markers: improving accuracy of studbook records for a captive flock of marabou storks (Leptoptilus crumeniferus). Zoo. Biol. 32, 556–564.
14. Grueber, C.E., Wallis, G.P. & Jamieson, I.G. (2008). Heterozygosity-fitness correlations and their relevance to studies on inbreeding depression in threatened species. Mol. Ecol. 17, 3978–3984.
15. 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.
16. Henkel, J.R., Jones, K.L., Hereford, S.G., Savoie, M.L., Leibo, S.P. & Howard, J.J. (2012). Integrating microsatellite and pedigree analyses to facilitate the captive management of the endangered Mississippi sandhill crane (Grus canadensis pulla). Zoo. Biol. 31, 322–335.
17. Hess, B.D., Dunn, P.O. & Whittingham, L.A. (2011). Females choose multiple mates in the lekking Greater Prairie-chicken (Tympanuchus cupido). Auk 129, 1–7.
18. Hill, W.G. & Weir, B.S. (2011). Variation in actual relationship as a consequence of Mendelian sampling and linkage. Genet. Res. 93, 47–64.
19. Ishtiaq, F., Prakash, V., Green, R.E. & Johnson, J.A. (2015). Management implications of genetic studies for ex situ populations of three critically endangered Asian Gyps vultures. Anim. Conserv. 18, 259–270.
20. Ivy, J.A. & Lacy, R.C. (2010). Using molecular methods to improve the genetic management of captive breeding programs for threatened species. In Molecular approaches in natural resource conservation and management: 267–295. DeWoody, J.A., Bickham, J.W., Michler, C.H., Nichols, K.M., Rhodes, O.E. & Woeste, K.E. (Eds). New York: Cambridge University Press.
21. 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.
22. Johnson, J.A., Schroeder, M.A. & Robb, L.A. (2011). Greater Prairie-chicken (Tympanuchus cupido). In The birds of North America online. Poole, A. (Ed). Ithaca: Cornell Lab of Ornithology. Available at http://bna.birds.cornell.edu/bna/species/036.
23. Jones, K.L., Glenn, T.C., Lacy, R.C., Pierce, J.R., Unruh, N., Mirande, C.M. & Chavez-Ramirez, F. (2002). Refining the Whooping Crane studbook by incorporating microsatellite DNA and leg-band analyses. Conserv. Biol. 16, 789–799.
24. Kalinowski, S.T., Taper, M.L. & Marshall, T.C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106.
25. Kardos, M., Luikart, G. & Allendorf, F.W. (2015). Measuring individual inbreeding in the age of genomics: marker-based measures are better than pedigrees. Heredity 115, 63–72.
26. Lacy, R.C. (1994). Managing genetic diversity in captive populations of animals. In Restoration of endangered species: conceptual issues, planning and implementation: 63–89. Bowles, M.L. & Whelan, C.J. (Eds). Cambridge: Cambridge University Press.
27. Lacy, R.C. (2009). Stopping evolution: genetic management of captive populations. In Conservation genetics in the age of genomics: 58–81. Amato, G., DeSalle, R., Ryder, O.A. & Rosenbaum, H.C. (Eds). New York: Columbia University Press.
28. Lacy, R.C. & Ballou, J.D. (1998). Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution 52, 900–909.
29. Lacy, R.C., Petric, A.M. & Warneke, M. (1993). Inbreeding and outbreeding depression in captive populations of wild species. In The natural history of inbreeding and outbreeding: 352–374. Thornhill, N.W. (Ed). Chicago: University of Chicago Press.
30. Laws, R.J. & Jamieson, I.G. (2010). Is lack of evidence of inbreeding depression in a threatened New Zealand robin indicative of reduced genetic load? Anim. Conserv. 14, 47–55.
31. Lewis, P.O. & Zaykin, D. (2001). Genetic data analysis: computer program for the analysis of allelic data, version 1.1. Storrs: University of Connecticut.
32. Morrow, M.E., Rossignol, T.A. & Silvy, N.J. (2004). Federal listing of prairie grouse: lessons from the Attwater's prairie-chicken. Wildl. Soc. Bull. 32, 112–118.
33. Morrow, M.E., Rossignol, T.A., Toepfer, J.E. & Pratt, A. (2010). Attwater's prairie-chicken recovery – the beginning or the end? Grouse Partnership News 2010–2011, 12–18.
34. Morrow, M.E., Chester, R.E., Lehnen, S.E., Drees, B.M. & Toepfer, J.E. (2015). Indirect effects of red imported fire ants on Attwater's prairie-chicken brood survival. J. Wildl. Mgmt. 79, 898–906.
35. Oliehoek, P.A. & Bijma, P. (2009). Effects of pedigree errors on the efficiency of conservation decisions. Genetic Sel. Evol. 41, 9.
36. Oyler-McCance, S.J. & St. John, J. (2010). Characterization of small microsatellite loci for use in noninvasive sampling studies of Gunnison Sage-Grouse (Centrocercus minimus). Conserv. Genet. Resour. 2, 17–20.
37. Piertney, S.B. & Dallas, J.F. (1997). Isolation and characterization of hypervariable microsatellites in Red Grouse Lagopus lagopus scoticus. Mol. Ecol. 6, 93–95.
38. Piertney, S.B. & Höglund, J. (2001). Polymorphic microsatellite DNA markers in black grouse (Tetrao tetrix). Mol. Ecol. Notes 1, 303–304.
39. Pratt, A.C. (2010). Evaluation of the reintroduction of Attwater's prairie-chickens in Goliad County, Texas. MS thesis, Texas A&M University-Kingsville.
40. Ralls, K., Brugger, K. & Ballou, J.D. (1979). Inbreeding and juvenile mortality in small populations of ungulates. Science 206, 1101–1103.
41. Ralls, K., Ballou, J.D. & Templeton, A.R. (1988). Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv. Biol. 2, 185–193.
42. Reid, J.M., Keller, L.F., Marr, A.B., Nietlisbach, P., Sardell, R.J. & Arcese, P. (2014). Pedigree error due to extra-pair reproduction substantially biases estimates of inbreeding depression. Evolution 68, 802–815.
43. Rice, W.R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
44. 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.
45. Russello, M.A. & Amato, G. (2004). Ex situ population management in the absence of pedigree information. Mol. Ecol. 13, 2829–2840.
46. Segelbacher, G., Paxton, R.J., Steinbrück, G., Trontelj, P. & Storch, I. (2000). Characterization of microsatellites in capercaillie Tetrao urogallus (AVES). Mol. Ecol. 9, 1934–1935.
47. Shan, L., Hu, Y., Zhu, L., Yan, L., Wang, C., Li, D., Jin, X., Zhang, C. & Wei, F. (2014). Large-scale genetic survey provides insights into the captive management and reintroduction of giant pandas. Mol. Biol. Evol. 31, 2663–2671.
48. Speed, D. & Balding, D.J. (2015). Relatedness in the post-genomic era: is it still useful? Nat. Rev. Genet. 16, 33–44.
49. Taylor, S.E., Oyler-McCance, S.J. & Quinn, T.W. (2003). Isolation and characterization of microsatellite loci in Greater Sage-Grouse (Centrocercus urophasianus). Mol. Ecol. Notes 3, 262–264.
50. Tzika, A.C., Remy, C., Givson, R. & Milinkovitch, M.C. (2009). Molecular genetic analysis of a captive breeding program: the vulnerable endemic Jamaican yellow boa. Conserv. Genet. 10, 67–77.
51. U.S. Fish and Wildlife Service. (2010). Attwater's prairie-chicken recovery plan, second revision. Albuquerque: U.S. Fish and Wildlife Service.
52. Van de Casteele, T., Galbusera, P. & Matthysen, E. (2001). A comparison of microsatellite-based pairwise relatedness estimators. Mol. Ecol. 10, 1539–1549.
53. Wang, J. (2007). Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet. Res. 89, 135–153.
54. Wang, J. (2011). Coancestry: a program for simulating, estimating and analyzing relatedness and inbreeding coefficients. Mol. Ecol. 11, 141–145.
55. Williams, S.E. & Hoffman, E.A. (2009). Minimizing genetic adaptation in captive breeding programs: a review. Biol. Conserv. 142, 2388–2400.
56. Willoughby, J.R., Fernandez, N.B., Lamb, M.C., Ivy, J.A., Lacy, R.C. & DeWoody, J.A. (2015). The impacts of inbreeding, drift, and selection on genetic diversity in captive breeding populations. Mol. Ecol. 24, 98–110.
57. Witzenberger, K.A. & Hochkirch, 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.