Inbreeding and inbreeding depression in endangered red wolves (Canis rufus)

Molecular Ecology

Volumn 23, Issue 17, 2014, Pages 4241-4255

  Brzeski, Kristin E ^a   Rabon, David R ^b   Chamberlain, Michael J ^c   Waits, Lisette P ^d   Taylor, Sabrina S ^a  

^a LOUISIANA STATE UNIVERSITY AGRICULTURAL CENTER   (United States)

^b Red Wolf Recovery Program   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d UNIVERSITY OF IDAHO   (United States)

Author keywords

body size; Canis rufus; inbreeding; inbreeding depression; pedigree

Indexed keywords

CANIS FAMILIARIS; CANIS RUFUS;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BODY SIZE; BREEDING; CANIS RUFUS; ENDANGERED SPECIES; ENVIRONMENTAL PROTECTION; FEMALE; FOUNDER EFFECT; GENETICS; INBREEDING; INBREEDING DEPRESSION; MALE; PEDIGREE; POPULATION GENETICS; REPRODUCTIVE FITNESS; UNITED STATES; WOLF;

BODY SIZE; CANIS RUFUS; INBREEDING; INBREEDING DEPRESSION; PEDIGREE;

ANIMALS; BREEDING; CONSERVATION OF NATURAL RESOURCES; ENDANGERED SPECIES; FEMALE; FOUNDER EFFECT; GENETIC FITNESS; GENETICS, POPULATION; INBREEDING; MALE; MODELS, GENETIC; NORTH CAROLINA; WOLVES;

EID: 84906668577     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12871     Document Type: Article

References (104)

1. Adams JR, (2006) A multi-faceted molecular approach to red wolf (Canis rufus) conservation and management. PhD dissertation, University of Idaho, Moscow, Idaho.
2. Ala-Honkola O, Uddström A, Diaz Pauli B, Lindström K, (2009) Strong inbreeding depression in male mating behavior in a poeciliid fish. Journal of Evolutionary Biology, 22, 1396-1406.
3. Allendorf FW, Luikart G, (2007) Conservation Genetics. Blackwell Publishing, Malden, Massachusetts.
4. Allendorf FW, Leary RF, Spruell P, Wenburg JK, (2001) The problems with hybrids: setting conservation guidelines. TRENDS in Ecology and Evolution, 16, 613-622.
5. Asa C, Miller P, Agnew M, et al,. (2007) Relationship of inbreeding with sperm quality and reproductive success in Mexican gray wolves. Animal Conservation, 10, 326-331.
6. Ballou JD, (1997) Effects of ancestral inbreeding on genetic load in mammalian populations. Journal of Heredity, 88, 169-178.
7. Barton K, (2009) MuMIn: multi-model inference. R package, version 0.12.2. Available from: http://r-forge.r-project.org/projects/mumin/.
8. Barton NH, Keightley PD, (2002) Understanding quantitative genetic variation. Nature Reviews, Genetics, 3, 11-21.
9. Bates D, Maechler M, (2010) lme4: Linear Mixed-Effects Models Using S4 Classes., R Package Version 0.999375-999335. Available from http://CRAN.R- project.org/package=lme4
10. Bolund E, Martin K, Kempenaers B, Forstmeier W, (2010) Inbreeding depression of sexually selected traits and attractiveness in the zebra finch. Animal Behaviour, 79, 947-955.
11. Burnham KP, Anderson DR, (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York City, New York.
12. Charlesworth B, Charlesworth D, (1999) The genetic basis of inbreeding depression. Genetic Resources, Cambridge, 74, 329-340.
13. Charlesworth D, Willis JH, (2009) The genetics of inbreeding depression. Nature Reviews Genetics, 10, 783-798.
14. Coltman DW, Pilkington JG, Smith JA, Pemberton JM, (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution, 53, 1259-1267.
15. Crnokrak P, Roff DA, (1995) Dominance variance: associations with selection and fitness. Heredity, 75, 530-540.
16. Crnokrak P, Roff DA, (1999) Inbreeding depression in the wild. Heredity, 83, 260-270.
17. Curio E, (1983) Why do young birds reproduce less well? Ibis, 125, 400-404.
18. Custer JW, Pence DB, (1981) The ecological analyses of helminth populations of wild canids from the gulf coast prairies of Texas and Louisiana. Journal of Parasitology, 67, 289-307.
19. Daniels SJ, Walters JR, (2000) Inbreeding depression and its effects on natal dispersal in red-cockaded woodpeckers. The Condor, 102, 482-491.
20. De Rose MA, Roff DA, (1999) A comparison of inbreeding depression in life history and morphological traits in animals. Evolution, 53, 1288-1292.
21. Dunn SJ, Clancey E, Waits LP, Byers JA, (2011) Inbreeding depression in pronghorn (Antilocapra americana) fawns. Molecular Ecology, 20, 4889-4898.
22. Edmands S, (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology, 16, 463-475.
23. Ericsson G, Wallin K, Ball JP, Broberg M, (2001) Age-related reproductive efforts and senescence in free-ranged moose, Alces alces. Ecology, 82, 1613-1620.
24. Fadao T, Tingzheng W, Yajun Z, (2000) Inbreeding avoidance and mate choice in the mandarin vole (Microtus mandarinus). Canadian Journal of Zoology, 78, 2119-2125.
25. Falconer DS, (1960) Introduction to Quantitative Genetics. Robert MacLehose and Company Limited, Glasgow, UK.
26. Franke K, Fischer K, (2013) Effects of inbreeding and temperature stress on life history and immune function in a butterfly. Journal of Evolutionary Biology, 26, 517-528.
27. Fredrickson R, Hedrick P, (2002) Body size in endangered Mexican Wolves: effects of inbreeding and cross-lineage matings. Animal Conservation, 18, 164-165.
28. Fredrickson RJ, Siminski P, Woolf M, Hedrick PW, (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proceedings of the Royal Society B-Biological Sciences, 274, 2365-2371.
29. Gage MJG, Surridge AK, Tomkins JL, et al,. (2006) Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Current Biology, 16, 612-617.
30. Gelman A, Su YS, Yajima M, et al,. (2009) arm: data analysis using regression and multilevel/hierarchical models. R package, version 9.01. Available from: http://CRAN.R-project.org/package=arm.
31. Grant PR, Grant BR, Keller LF, Markert JA, Petren K, (2003) Inbreeding and interbreeding in Darwin's Finches. Evolution, 57, 2911-2916.
32. Grueber CE, Laws RJ, Nakagawa S, Jamieson IG, (2010) Inbreeding depression accumulation across life-history stages of the endangered Takahe. Conservation Biology, 24, 1617-1625.
33. Grueber CE, Nakagawa S, Laws RJ, Jamieson IG, (2011a) Multimodel inference in ecology and evolution: challenges and solutions. Journal of Evolutionary Biology, 24, 699-711.
34. Grueber CE, Waters JM, Jamieson IG, (2011b) The imprecision of heterozygosity-fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species. Molecular Ecology, 20, 67-79.
35. Hedrick W, Fredrickson RJ, (2008) Captive breeding and the reintroduction of Mexican and red wolves. Molecular Ecology, 17, 344-350.
36. Hedrick W, Kalinowski ST, (2000) Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics, 31, 139-162.
37. Hinton JW, Chamberlain MJ, Rabon DR, (2013) Red wolf (Canis rufus) recovery: a review with suggestions for future research. Animals, 3, 722-744.
38. Hogg JT, Forbes SH, Steele BM, Luikart G, (2006) Genetic rescue of an insular population of large mammals. Proceedings of the Royal Society B-Biological Sciences, 273, 1491-1499.
39. vonHoldt BM, Stahler DR, Smith DW, Earl DA, Pollinger JP, Wayne RK, (2007) The genealogy and genetic viability of reintroduced Yellowstone grey wolves. Molecular Ecology, 17, 252-274.
40. Ibáñez B, Moreno E, Barbosa A, (2011) No inbreeding effects on body size in two captive endangered gazelles. Mammalian Biology, 76, 748-754.
41. ISIS (2011) SPARKS (Single Population Analysis and Records Keeping System) ver 1.6. International Species Information System, Eagan, Minnesota.
42. Jamieson IG, Taylor SS, Tracy LN, Kokko H, Armstrong DP, (2009) Why some species of birds do not avoid inbreeding: insights from New Zealand robins and saddlebacks. Behavioral Ecology, 20, 575-584.
43. Johnson WE, Onorato DP, Roelke ME, et al,. (2010) Genetic restoration of the Florida Panther. Science, 329, 1641-1644.
44. Kalinowski ST, Hedrick PW, (1998) An improved method for estimating inbreeding depression in pedigrees. Zoo Biology, 17, 481-497.
45. Kalinowski ST, Hedrick PW, Miller PS, (1999) No evidence for inbreeding depression in Mexican and red wolf captive breeding programs. Conservation Biology, 13, 1371-1377.
46. Keller LF, (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution, 52, 240-250.
47. Keller LF, Waller DM, (2002) Inbreeding effects in wild populations. Trends in Ecology & Evolution, 17, 230-241.
48. Kelly BT, Miller PS, Seal US, (eds) (1999) Population and Habitat Viability Assessment Workshop for the Red Wolf (Canis Rufus). Conservation Breeding Specialist Group (SSC/IUCN), Apple Valley, Minnesota.
49. Kruuk LEB, Sheldon BC, Merilä J, (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proceedings of the Royal Society B-Biological Sciences, 269, 1581-1589.
50. Lacy RC, (1997) Importance of genetic variation to the viability of mammalian populations. Journal of Mammalogy, 78, 320-335.
51. Lacy RC, Ballou JD, (1998) Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution, 52, 900-909.
52. Lacy RC, Alaks G, Walsh A, (1996) Hierarchical analysis of inbreeding depression in Peromyscus polionotus. Evolution, 50, 2187-2200.
53. Lacy RC, Ballou JD, Pollak JP, (2011) PMx: software package for demographic and genetic analysis and management of pedigreed populations. Methods in Ecology and Evolution, 3, 433-437.
54. Laikre L, (1999) Conservation genetics of Nordic carnivores: lessons from zoos. Hereditas, 130, 203-216.
55. Laikre L, Ryman N, (1991) Inbreeding depression in a captive wolf (Canis lupus) population source. Conservation Biology, 5, 33-40.
56. Laikre L, Rayman N, Thompson EA, (1993) Hereditary blindness in a captive wolf (Canis lupus) population: frequency reduction of a deleterious allele in relation to gene conservation. Conservation Biology, 7, 592-601.
57. Laws RJ, Townsend SM, Nakagawa SI, Jamieson G, (2010) Limited inbreeding depression in a bottlenecked population is age but not environment dependent. Journal of Avian Biology, 41, 645-652.
58. Liberg O, Andrén H, Pedersen HC, et al,. (2005) Severe inbreeding depression in a wild wolf (Canis lupus) population. Biology Letters, 1, 17-20.
59. Mech LD, (2000) Leadership in wolf, Canis lupus, packs. Canadian Field Naturalist, 114, 259-263.
60. Miller CR, Adams JR, Waits LP, (2003) Pedigree-based assignment tests for reversing coyote (Canis latrans) introgression into the wild red wolf (Canis rufus) population. Molecular Ecology, 12, 3287-3301.
61. Morton NE, Crow JF, Muller HJ, (1956) An estimate of the mutational damage in man from data on consanguineous marriages. Proceedings of the National Academy of Sciences, USA, 42, 855-863.
62. Naish KA, Seamons TR, Dauer MB, Hauser L, Quinn TP, (2013) Relationship between effective population size, inbreeding and adult fitness-related traits in a steelhead (Oncorhynchus mykiss) population released in the wild. Molecular Ecology, 22, 1295-1309.
63. Nielsen JF, English S, Goodall-Copestake WP, et al,. (2012) Inbreeding and inbreeding depression of early life traits in a cooperative mammal. Molecular Ecology, 21, 2788-2804.
64. Nowak RM, (2002) The original status of wolves in eastern North America. Southeastern Naturalist, 1, 95-130.
65. O'Grady JJ, Brook BW, Reed DH, Ballou JD, Tonkyn DW, Frankham R, (2006) Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biological Conservation, 133 (42-5), 1.
66. Paradiso JL, Nowak RM, (1972) Canis rufus. Mammalian Species, 22, 1-4.
67. Pemberton J, (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology & Evolution, 19, 613-615.
68. Pemberton JM, (2008) Wild pedigrees: the way forward. Proceedings of the Royal Society B-Biological Sciences, 275, 613-621.
69. Phillips MK, Parker WT, (1988) Red wolf recovery: a progress report. Conservation Biology, 2, 139-141.
70. Phillips MK, Henry VG, Kelly BT, (2003) Restoration of the red wolf. In: Wolves: Behavior, Ecology, and Conservation (eds, Mech DL, Boitani L,), pp. 272-288. University Chicago Press, Chicago, Illinois.
71. Pusey A, Wolf M, (1996) Inbreeding avoidance in animals. Trends in Ecology & Evolution, 11, 201-206.
72. Rabon DR Jr, (2014) Effects of age and experience on reproductive performance of captive red wolves (Canis rufus). Canadian Journal of Zoology, 92, 251-258.
73. Rabon DR Jr, Waddell W, (2010) Effects of inbreeding on reproductive success, performance, litter size, and survival in captive red wolves (Canis rufus). Zoo Biology, 29, 36-49.
74. Rabon DR Jr, Bartel R, Beyer A, (2013) Red Wolf Adaptive Management Plan FY13-FY15, pp. 14. US Fish and Wildlife Service, Manteo, North Carolina.
75. Räikkönen J, Vucetich JA, Peterson RO, Nelson MP, (2009) Congenital bone deformities and the inbred wolves (Canis lupus) of Isle Royale. Biological Conservation, 142, 1025-1031.
76. Ralls K, Ballou J, Templeton A, (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conservation Biology, 2, 185-193.
77. Reed DH, Lowe EH, Briscoe DA, Frankham R, (2003) Inbreeding and extinction: effects of rate of inbreeding. Conservation Genetics, 4, 405-410.
78. Rhymer JM, Simberloff D, (1996) Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27, 83-109.
79. Riley GA, McBride RT, (1975) A survey of the red wolf (Canis rufus). In: The Wild Canids; Their Systematics, Behavioral Ecology, and Evolution (ed., Fox MW,), pp. 263-277. Van Nostrand Reinhold Co, New York City, New York.
80. Rioux-Paquette E, Festa-Bianchet M, Coltman DW, (2010) No inbreeding avoidance in an isolated population of bighorn sheep. Animal Behaviour, 80, 865-871.
81. Rodrigáñeza J, Toro MA, Rodrigues MC, Silió L, (1998) Effect of founder allele survival and inbreeding depression on litter size in a closed line of large white pigs. Animal Science, 67, 573-582.
82. Roff DA, (1998) Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity, 81, 28-37.
83. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I, (1998) Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491-494.
84. Sillero-Zubiri C, Gottelli D, Macdonald DW, (1996) Male philopatry, extra-pair copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behavioral Ecology & Sociobiology, 38, 331-340.
85. Smith D, Meier T, Geffen E, et al,. (1997) Is incest common in gray wolf packs? Behavioral Ecology, 8, 384-391.
86. Sparkman AM, Adams JR, Beyer A, Steury TD, Waits LP, Murray DL, (2011) Helper effects on pup lifetime fitness in the cooperatively breeding red wolf (Canis rufus). Proceedings of the Royal Society B-Biological Sciences, 278, 1381-1389.
87. Sparkman AM, Adams JR, Steury TD, Waits LP, Murray DL, (2012a) Pack social dynamics and inbreeding avoidance in the cooperatively breeding red wolf. Behavioral Ecology, 23, 1186-1194.
88. Sparkman AM, Adams JR, Steury TD, Waits LP, Murray DL, (2012b) Direct fitness benefits of delayed dispersal in the cooperatively breeding red wolf (Canis rufus). Behavioral Ecology, 83, 1091-1098.
89. Spiering PA, Gunther MS, Somers MJ, Walters DE, Wilson AS, Maldonado JE, (2011) Inbreeding, heterozygosity and fitness in a reintroduced population of endangered African wild dogs (Lycaon pictus). Conservation Genetics, 12, 401-412.
90. Stoskopf MK, Beck K, Fazio BB, et al,. (2005) From the Field: implementing recovery of the red wolf-integrating research scientists and managers. Wildlife Society Bulletin, 33, 1145-1152.
91. Szulkin M, Garant D, McCleery RH, Sheldon BC, (2007) Inbreeding depression along a life-history continuum in the great tit. Journal of Evolutionary Biology, 20, 1531-1543.
92. Szulkin M, Bierne N, David P, (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution, 64, 1202-1217.
93. Taylor SS, Sardell RJ, Reid JM, et al,. (2010) Inbreeding coefficient and heterozygosity-fitness correlations in unhatched and hatched song sparrow nestmates. Molecular Ecology, 19, 4454-4461.
94. Therneau T, (2013) coxme: mixed effects cox models R package version 22-3. Available from http://CRANR-projectorg/package=coxme.
95. Therneau T, Atkinson E, Sinnwell J, Schaid D, McDonnell S, (2014) kinship2: Pedigree functions R package version 157. Available from: http://r-forger-projectorg.
96. Townsend AK, Clark AB, McGowan KJ, Buckles EL, Miller AD, Lovette IJ, (2009) Disease-mediated inbreeding depression in a large, open population of cooperative crows. Proceedings of the Royal Society B-Biological Sciences, 276, 2057-2064.
97. United State Fish and Wildlife Service (2013) Red Wolf Recovery Program 3rd Quarterly Report: April-June 2013. USFWS, Manteo, North Carolina.
98. ® Yellow Program. Population Management Center, Lincoln Park Zoo, Chicago, Illinois.
99. Walling CA, Nussey DH, Morris A, Clutton-Brock TH, Kruuk LEB, Pemberton JM, (2011) Inbreeding depression in red deer calves. BMC Evolutionary Biology, 11, 318-331.
100. Weimerskirch H, Barbraud C, Lys P, (2000) Sex differences in parental investment and chick growth in wandering albatrosses: fitness consequences. Ecology, 81, 309-318.
101. Wisely SM, Santymire RM, Livieri TM, Mueting SA, Howard J, (2008) Genotypic and phenotypic consequences of reintroduction history in the black-footed ferret (Mustela nigripes). Conservation Genetics, 9, 389-399.
102. Wright LI, Tregenza T, Hosken DJ, (2007) Inbreeding, inbreeding depression and extinction. Conservation Genetics, 9, 833-843.
103. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM, (2009) Mixed Effects Models and Extensions in Ecology With R. Springer Science+Business Media, LLC, New York City, New York.
104. Zuur AF, Ieno EN, Elphick CS, (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology & Evolution, 1, 3-14.