Reintroduction of confiscated and displaced mammals risks outbreeding and introgression in natural populations, as evidenced by orang-utans of divergent subspecies

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Banes, Graham L ^a,b,c   Galdikas, Biruté M F ^d   Vigilant, Linda ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^c MAX PLANCK INSTITUTE   (Germany)

^d SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; BORNEO; BREEDING; ENDANGERED SPECIES; MAMMAL; MOLECULAR EVOLUTION; PHYLOGENY; POPULATION DYNAMICS; POPULATION GENETICS;

ANIMALS; BORNEO; BREEDING; DNA, MITOCHONDRIAL; ENDANGERED SPECIES; EVOLUTION, MOLECULAR; GENETICS, POPULATION; MAMMALS; PHYLOGENY; POPULATION DYNAMICS;

EID: 84959419289     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22026     Document Type: Article

References (77)

1. Lockhart, J. M., Thorne, E. T. & Gober, D. R. In Recovery of the black-footed ferret: progress and continuing challenges (eds Roelle, J. E., Miller, B. J., Godbey, J. L. & Biggins, D. E.) 6-19 (US Geological Survey Scientific Investigations Report 2005-5293, 2005
2. Kierulff, M. C. M., et al. The golden lion tamarin Leontopithecus rosalia: a conservation success story. Int. Zoo. Yearb. 46, 36-45 (2012
3. Platt, J. R. Eyes in the sky: crowdfunded drones could help protect Kenyan rhinos. Sci. Am. 308, 32-32 (2013
4. Gibbs, J. P., Hunter, E. A., Shoemaker, K. T., Tapia, W. H. & Cayot, L. J. Demographic outcomes and ecosystem implications of giant tortoise reintroduction to Espanola Island, Galapagos. PLoS ONE 9, e110742, doi: 10.1371/journal.pone.0110742 (2014
5. Keane, A., Jones, J. P. G., Edwards-Jones, G. & Milner-Gulland, E. J. The sleeping policeman: understanding issues of enforcement and compliance in conservation. Anim. Conserv. 11, 75-82 (2008
6. Challender, D. W. S. & MacMillan, D. C. Poaching is more than an enforcement problem. Conserv. Lett. 7, 484-494 (2014
7. Robbins, M. M., et al. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS ONE 6, e19788, doi: 10.1371/journal.pone.0019788 (2011
8. Shan, L., et al. Large-scale genetic survey provides insights into the captive management and reintroduction of giant pandas. Mol. Biol. Evol. 31, 2663-2671 (2014
9. Burrows, R., Hofer, H. & East, M. L. Demography, extinction and intervention in a small population: the case of the Serengeti wild dogs. Proc. R. Soc. B. 256, 281-292 (1994
10. Woodroffe, R. Assessing the risks of intervention: immobilization, radio-collaring and vaccination of African wild dogs. Oryx 35, 234-244 (2001
11. IUCN/SSC. IUCN Guidelines for the Placement of Confiscated Animals (IUCN Species Survival Commission, Gland, Switzerland, 2000
12. IUCN/SSC. Guidelines for Reintroductions and other Conservation Translocations (IUCN Species Survival Commission, Gland, Switzerland, 2013
13. Unwin, S., et al. Does confirmed pathogen transfer between sanctuary workers and great apes mean that reintroduction should not occur?. Am. J. Primatol. 74, 1076-1083 (2012
14. Trayford, H. R. & Farmer, K. H. Putting the spotlight on internally displaced animals (IDAs): a survey of primate sanctuaries in Africa, Asia, and the Americas. Am. J. Primatol. 75, 116-134 (2012
15. Frankham, R., et al. Predicting the probability of outbreeding depression. Conserv. Biol. 25, 465-475 (2011
16. Frankham, R. Genetic rescue of small inbred populations: meta-Analysis reveals large and consistent benefits of gene flow. Mol. Ecol. 24, 2610-2618 (2015
17. Waller, D. M. Genetic rescue: a safe or risky bet?. Mol. Ecol. 24, 2595-2597 (2015
18. Hedrick, P. W. Gene flow and genetic restoration: the Florida panther as a case study. Conserv. Biol. 9, 996-1007 (1995
19. Land, E. D. & Lacy, R. C. Introgression level achieved through Florida panther genetic restoration. Endang. Sp. Update, 7(5), 100-105 (2000
20. Mansfield, K. G. & Land, E. D. Cryptorchidism in Florida panthers: prevalence, features, and influence of genetic restoration. J. Wildl. Dis. 38, 693-698 (2002
21. Johnson, W. E., et al. Genetic restoration of the Florida panther. Science 329, 1641-1645 (2010
22. Vila, C., et al. Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc. R. Soc. B. 270, 91-97 (2003
23. Westemeier, R. L., et al. Tracking the long-term decline and recovery of an isolated population. Science 282, 1695-1698 (1998
24. Madsen, T., Shine, R., Olsson, M. & Wittzell, H. Conservation biology: restoration of an inbred adder population. Nature 402, 34-35 (1999
25. Arrendal, J., Walker, C. W., Sundqvist, A.-K., Hellborg, L. & Vila, C. Genetic evaluation of an otter translocation program. Conserv. Genet. 5, 79-88 (2004
26. Rhymer, J. M. & Simberloff, D. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27, 83-109 (1996
27. Allendorf, F. W., Leary, R. F., Spruell, P. & Wenburg, J. K. The problems with hybrids: setting conservation guidelines. Trends Ecol. Evol. 16, 613-622 (2001
28. Tallmon, D., Luikart, G. & Waples, R. The alluring simplicity and complex reality of genetic rescue. Trends Ecol. Evol. 19, 489-496 (2004
29. Edmands, S. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol. Ecol. 16, 463-475 (2007
30. Gharrett, A. J., Smoker, W. W., Reisenbichler, R. R. & Taylor, S. G. Outbreeding depression in hybrids between odd- and evenbroodyear pink salmon. Aquaculture 173, 117-129 (1999
31. Huff, D. D., Miller, L. M., Chizinski, C. J. & Vondracek, B. Mixed-source reintroductions lead to outbreeding depression in secondgeneration descendants of a native North American fish. Mol. Ecol. 20, 4246-4258 (2011
32. Alstad, D. N. & Edmunds, G. F. Selection, outbreeding depression, and the sex ratio of scale insects. Science 220, 93-95 (1983
33. Edmands, S. Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53, 1757 (1999
34. Marr, A. B., Keller, L. F. & Arcese, P. Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution, 56, 131-42 (2002
35. Turček, F. J. & Hickey, J. J. Effect of introductions on two game populations in Czechoslovakia. Jour. Wild. Mgmt. 15, 113 (1951
36. Lacy, R. C., Petric, A. & Warneke, M. In The Natural History of Inbreeding and Outbreeding (ed Thornhill, N. W.) 352-374 (University of Chicago Press, 1993
37. Soehartono, T., et al Strategi dan rencana aksi konservasi orangutan Indonesia 2007-2017 (Direktorat Jenderal Perlindungan Hutan dan Konservasi Alam, Departemen Kehutanan, Jakarta, 2007
38. Arora, N., et al. Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus). PNAS 107, 21376-21381 (2010
39. Nater, A., et al. Reconstructing the demographic history of orang-utans using Approximate Bayesian Computation. Mol. Ecol. 24, 310-327 (2015
40. Goossens, B., et al. Patterns of genetic diversity and migration in increasingly fragmented and declining orang-utan (Pongo pygmaeus) populations from Sabah, Malaysia. Mol. Ecol. 14, 441-456 (2005
41. Jalil, M. F., et al. Riverine effects on mitochondrial structure of Bornean orang-utans (Pongo pygmaeus) at two spatial scales. Mol. Ecol. 17, 2898-2909 (2008
42. Kanthaswamy, S. & Smith, D. G. Population subdivision and gene flow among wild orangutans. Primates 43, 315-327 (2002
43. Warren, K. S., et al. Speciation and intrasubspecific variation of Bornean orangutans, Pongo pygmaeus pygmaeus. Mol. Biol. Evol. 18, 472-480 (2001
44. Galdikas, B. M. F. Reflections of Eden. (Little, Brown and Co., New York, 1995
45. Galdikas, B. M. & Ashbury, A. Reproductive parameters of female orangutans (Pongo pygmaeus wurmbii) 1971-2011, a 40-year study at Tanjung Puting National Park, Central Kalimantan, Indonesia. Primates, 54, 61-72 (2012
46. Yeager, C. P. Orangutan rehabilitation in Tanjung Puting National Park, Indonesia. Conserv. Biol. 11, 802-805 (1997
47. Banes, G. L., Galdikas, B. M. F. & Vigilant, L. Male orang-utan bimaturism and reproductive success at Camp Leakey in Tanjung Puting National Park, Indonesia. Behav. Ecol. Sociobiol. 69, 1785-1794 (2015
48. Thalmann, O., Hebler, J., Poinar, H. N., Paabo, S. & Vigilant, L. Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Mol. Ecol. 13, 321-335 (2004
49. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 (2013
50. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004
51. Ronquist, F., et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542 (2012
52. Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772-772 (2012
53. Utami-Atmoko, S. S., Singleton, I., Van Noordwijk, M. A., Van Schaik, C. P. & Mitra-Setia, T. In Orangutans: Geographic Variation in Behavioral Ecology and Conservation (eds Wich, S. A., Utami Atmoko, S. S., Mitra Setia, T. & Van Schaik, C. P.) 225-234 (Oxford University Press, 2008
54. Spalding, L. The jungle took her. Outside, 23(5), 78-90 & 189-191 (1998
55. Spalding, L. The Follow. (Key Porter Books, Toronto, 1998
56. Kuze, N., et al. Factors affecting reproduction in rehabilitant female orangutans: young age at first birth and short inter-birth interval. Primates 53, 181-192 (2012
57. Perkins, L. A. & Maple, T. L. North American orangutan species survival plan: current status and progress in the 1980s. Zoo Biol. 9, 135-139 (1990
58. Van Bemmel, A. C. V. Contribution to the knowledge of the geographical races of Pongo pygmaeus (Hoppius). Bijdr. Dierkd. 38, 13-15 (1968
59. Jones, M. L. In Recent Advances in Primatology (ed. Hofer, H. O.) 217-223 (Karger, Basel, 1969
60. Mallinson, J. "Cocktail orangutans and the need to preserve pure-bred stock. Dodo. 15, 69-77 (1978
61. Seuanez, H. N., Evans, H. J., Martin, D. E. & Fletcher, J. An inversion of chromosome 2 that distinguishes between Bornean and Sumatran orangutans. Cytogenet. Cell Genet. 23, 137-140 (1979
62. Xu, X. & Arnason, U. The mitochondrial DNA molecule of sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan. J. Mol. Evol. 43, 431-437 (1996
63. Zhang, Y.-W., Ryder, O. A. & Zhang, Y.-P. Genetic divergence of orangutan subspecies (Pongo pygmaeus). J. Mol. Evol. 52, 516-526 (2014
64. Van Schaik, C. P., Marshall, A. J. & Wich, S. A. In Orangutans: Geographic Variation in Behavioral Ecology and Conservation (eds Wich, S. A., Utami Atmoko, S. S., Mitra Setia, T. & Van Schaik, C. P.) 351-362 (Oxford University Press, 2008
65. Gonder, M. K., et al. Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. PNAS 108, 4766-4771 (2011
66. Charpentier, M. J. E., et al. Genetic structure in a dynamic baboon hybrid zone corroborates behavioural observations in a hybrid population. Mol. Ecol. 21, 715-731 (2011
67. Stevison, L. S. & Kohn, M. H. Divergence population genetic analysis of hybridization between rhesus and cynomolgus macaques. Mol. Ecol. 18, 2457-2475 (2009
68. Hey, J. The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Mol. Biol. Evol. 27, 921-933 (2010
69. Fünfstück, T., et al. The genetic population structure of wild western lowland gorillas (Gorilla gorilla gorilla) living in continuous rain forest. Am. J. Primatol. 76, 868-878 (2014
70. Association of Zoos and Aquariums. Guidelines for reintroduction of animals born or held in captivity (Association of Zoos and Aquariums, Silver Spring, 1992
71. Beck, B., et al. Best practice guidelines for the re-introduction of great apes: occasional paper of the IUCN Species Survival Commission No. 35. 1-56 (SSC Primate Specialist Group of the World Conservation Union, Gland, Switzerland, 2007
72. Campbell, C. O., Cheyne, S. M. & Rawson, B. M. Best practice guidelines for the rehabilitation and translocation of gibbons. (IUCN SSC Primate Specialist Group, Gland, Switzerland, 2015
73. Sajuthi, D., et al. Recommendations to the Department of Forestry of the Republic of Indonesia on the medical quarantine of orangutans intended for reintroduction. Proceedings of the Great Apes Conference, 132-136 (Indonesian Department of Forestry and Department of Tourism, Jakarta, 1991
74. Tutin, C. E. G., et al. Conservation biology framework for the release of wild-born orphaned chimpanzees into the Conkouati Reserve, Congo. Conserv. Biol. 15, 1247-1257 (2001
75. Goossens, B., et al. Measuring genetic diversity in translocation programmes: principles and application to a chimpanzee release project. Anim. Conserv. 5, 225-236 (2002
76. Warren, K. S. Orang-utan conservation-epidemiological aspects of health management and population genetics. Ph.D. thesis, Murdoch University, Division of Veterinary and Biomedical Sciences, March (2001
77. Wich, S A., et al. Understanding the impacts of land-use policies on a threatened species: is there a future for the Bornean orangutan? PLoS ONE 7(11), e49142, doi: 10.1371/journal.pone.0049142 (2012