Genomics advances the study of inbreeding depression in the wild

Evolutionary Applications

Volumn 9, Issue 10, 2016, Pages 1205-1218

  Kardos, Marty ^a   Taylor, Helen R ^b   Ellegren, Hans ^a   Luikart, Gordon ^c,d   Allendorf, Fred W ^c  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c UNIVERSITY OF MONTANA   (United States)

^d UNIVERSITY OF MONTANA   (United States)

Author keywords

conservation genetics; fitness; identity by descent; pedigree analysis; whole genome resequencing

Indexed keywords

EID: 84995686682     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12414     Document Type: Review

References (125)

1. Adzhubei, I. A., Schmidt, S., Peshking, L., Ramensky, V. E., Gerasimova, A., Bork, P., … Sunyaev, S. R. (2010). A method and server for predicting damaging missense mutations. Nature Methods, 7, 248–249.
2. Allendorf, F. W., Hohenlohe, P. A., & Luikart, G. (2010). Genomics and the future of conservation genetics. Nature Reviews Genetics, 11, 697–709.
3. Amos, W., Wilmer, J. W., Fullard, K., Burg, T. M., Croxall, J. P., Bloch, D., & Coulson, T. (2001). The influence of parental relatedness on reproductive success. Proceedings of the Royal Society of London Series B: Biological Sciences, 268, 2021–2027.
4. Andrews, K. R., Good, J. M., Miller, M. R., Luikart, G., & Hohenlohe, P. A. (2016). Harnessing the power of RADseq for ecological and evolutionary genomics. Nature Reviews Genetics, 17, 81–92.
5. Ballou, J. D. (1997). Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. Journal of Heredity, 88, 169–178.
6. Balloux, F. (2004). Heterozygote excess in small populations and the heterozygote-excess effective population size. Evolution, 58, 1891–1900.
7. Balloux, F., Amos, W., & Coulson, T. (2004). Does heterozygosity estimate inbreeding in real populations? Molecular Ecology, 13, 3021–3031.
8. Barson, N. J., Aykanat, T., Hindar, K., Baranski, M., Bolstad, G. H., Fiske, P., … Primmer, C. R. (2015). Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature, 528, 405–408.
9. Bérénos, C., Ellis, P. A., Pilkington, J. G., & Pemberton, J. M. (2016). Genomic analysis reveals depression due to both individual and maternal inbreeding in a free-living mammal population. Molecular Ecology, 25, 3152–3168.
10. Bijlsma, R., Bundgaard, J., & van Putten, W. F. (1999). Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology, 12, 1125–1137.
11. Blouin, M. S. (2003). DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends in Ecology & Evolution, 18, 503–511.
12. Boakes, E., Wang, J., & Amos, W. (2007). An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity, 98, 172–182.
13. Boitard, S., Rodriguez, W., Jay, F., Mona, S., & Austeritz, F. (2016). Inferring population size history from large samples of genome wide molecular data-an approximate Bayesian computation approach. PLoS Genetics, 12, e1005877.
14. Broman, K. W., & Weber, J. L. (1999). Long homozygous chromosomal segments in reference families from the centre d'Etude du polymorphisme humain. American Journal of Human Genetics, 65, 1493–1500.
15. Browning, B. L., & Browning, S. R. (2013). Detecting identity by descent and estimating genotype error rates in sequence data. American Journal of Human Genetics, 93, 840–851.
16. Browning, S. R., & Browning, B. L. (2015). Accurate non-parametric estimation of recent effective population size from segments of identity by descent. American Journal of Human Genetics, 97, 404–418.
17. Byers, D., & Waller, D. (1999). Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics, 30, 479–513.
18. Casellas, J., Piedrafita, J., Caja, G., & Varona, L. (2009). Analysis of founder-specific inbreeding depression on birth weight in Ripollesa lambs. Journal of Animal Science, 87, 72–79.
19. Chapman, J. R., Nakagawa, S., Coltman, D. W., Slate, J., & Sheldon, B. C. (2009). A quantitative review of heterozygosity–fitness correlations in animal populations. Molecular Ecology, 18, 2746–2765.
20. Charlesworth, D., & Willis, J. H. (2009). The genetics of inbreeding depression. Nature Reviews Genetics, 10, 783–796.
21. Charlier, C., Coppieters, W., Rollin, F., Desmecht, D., Agerholm, J. S., Cambisano, N., … Fasquelle, C. (2008). Highly effective SNP-based association mapping and management of recessive defects in livestock. Nature Genetics, 40, 449–454.
22. Choi, Y., Sims, G. E., Murphy, S., Miller, J. R., & Chan, A. P. (2012). Predicting the functional effect of amino acid substitutions and indels. PLoS One, 7, e46688.
23. Coltman, D. W., Pilkington, J. G., Smith, J. A., & Pemberton, J. M. (1999). Parasite-mediated selection against inbred Soay sheep in a free-living island population. Evolution, 53, 1259–1267.
24. Coulson, T. N., Pemberton, J. M., Albon, S. D., Beaumont, M., Marshall, T. C., Slate, J., Guinness, F. E., & Clutton-Brock, T. H. (1998). Microsatellites reveal heterosis in red deer. Proceedings of the Royal Society of London Series B: Biological Sciences, 265, 489–495.
25. Crow, J. F., & Denniston, C. (1988). Inbreeding and variance effective population numbers. Evolution, 42, 482–495.
26. Crow, J. F., & Kimura, M. (1970). An introduction to population genetics theory. Caldwell, NJ: The Blackburn Press.
27. Csilléry, K., Blum, M. G. B., Gaggioti, O. E., & François, O. (2010). Approximate Bayesian computation (ABC) in practice. Trends in Ecology & Evolution, 25, 410–418.
28. Curik, I., Ferenčaković, M., & Sölkner, J. (2014). Inbreeding and runs of homozygosity: A possible solution to an old problem. Livestock Science, 166, 26–34.
29. Darwin, C. (1896). The variation of animals and plants under domestication (Vol. 2). New York, NY: D. Appleton and Co.
30. Dobrynin, P., Liu, S., Tamazian, G., Xiong, Z., Yurchenko, A. A., Krasheninnikova, K., … O'Brien, S. J. (2015). Genomic legacy of the African cheetah, Acinonyx jubatus. Genome Biology, 16, 1–20.
31. Domitrz, I., Kosiorek, M., Żekanowski, C., & Kamińska, A. (2016). Genetic studies of Polish migraine patients: Screening for causative mutations in four migraine-associated genes. Human Genomics, 10, 3.
32. Ellegren, H. (2014). Genome sequencing and population genomics in non-model organisms. Trends in Ecology & Evolution, 29, 51–63.
33. Enciso-Mora, V., Hosking, F. J., & Houlston, R. S. (2010). Risk of breast and prostate cancer is not associated with increased homozygosity in outbred populations. European Journal of Human Genetics, 18, 909–914.
34. Felsenstein, J. (2015). Theoretical evolutionary genetics. Retrieved from http://evolution.gs.washington.edu/pgbook/pgbook.pdf
35. Fisher, R. A. (1965). The theory of inbreeding (2nd ed.). Edinburgh, UK: Oliver & Boyd.
36. Forstmeier, W., Schielzeth, H., Mueller, J. C., Ellegren, H., & Kempenaers, B. (2012). Heterozygosity-fitness correlations in zebra finches: Microsatellite markers can be better than their reputation. Molecular Ecology, 21, 3237–3249.
37. Frankham, R. (1995). Inbreeding and extinction: A threshold effect. Conservation Biology, 9, 792–799.
38. Frankham, R. (2005). Genetics and extinction. Biological Conservation, 126, 131–140.
39. Franklin, I. (1977). The distribution of the proportion of the genome which is homozygous by descent in inbred individuals. Theoretical Population Biology, 11, 60–80.
40. García-Dorado, A. (2012). Understanding and predicting the fitness decline of shrunk populations: Inbreeding, purging, mutation, and standard selection. Genetics, 190, 1461–1476.
41. Gazal, S., Sahbatou, M., Babron, M. C., Génin, E., & Leutenegger, A. L. (2014). FSuite: Exploiting inbreeding in dense SNP chip and exome data. Bioinformatics, 30, 1940–1941.
42. Gebremedhin, B., Ficetola, G., Naderi, S., Rezaei, H. R., Maudet, C., Rioux, D., … Taberlet, P. (2009). Combining genetic and ecological data to assess the conservation status of the endangered Ethiopian walia ibex. Animal Conservation, 12, 89–100.
43. Gorman, G. C., & Renzi Jr, J. (1979). Genetic distance and heterozygosity estimates in electrophoretic studies: Effects of sample size. Copeia, 2, 242–249.
44. Gutenkust, R. N., Hernandez, R. D., Williamson, S. H., & Bustamante, C. D. (2009). Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genetics, 5, e1000695.
45. Haddad, N. M., Brudvig, L. A., Clobert, J., Davies, K. F., Gonzalez, A., Holt, R. D., … Townshend, J. R. (2015). Habitat fragmentation and its lasting impact on Earth's ecosystems. Science Advances, 1, e1500052.
46. Hedrick, P. W., & García-Dorado, A. (in press). Understanding inbreeding depression, purging, and genetic rescue. Trends in Ecology and Evolution, doi: http://dx.doi.org/10/1016/j.tree.2016.09.005 [In Press].
47. Hedrick, P. W., Hellsten, U., & Grattapaglia, D. (2016). Examining the cause of high inbreeding depression: Analysis of whole-genome sequence data in 28 selfed progeny of Eucalyptus grandis. New Phytologist, 209, 600–611.
48. Hedrick, P. W., Hoeck, P. E., Fleischer, R. C., Farabaugh, S., & Masuda, B. M. (2015). The influence of captive breeding management on founder representation and inbreeding in the ‘Alalā, the Hawaiian crow. Conservation Genetics, 17, 369–378.
49. Hedrick, P. W., & Kalinowski, S. T. (2000). Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics, 31, 139–162.
50. Hill, W. G., & Weir, B. S. (2011). Variation in actual relationship as a consequence of Mendelian sampling and linkage. Genetics Research, 93, 47–64.
51. Hoffman, J. I., Simpson, F., David, P., Rijks, J. M., Kuiken, T., Thorne, M. A., … Dasmahapatra, K. K. (2014). High-throughput sequencing reveals inbreeding depression in a natural population. Proceedings of the National Academy of Sciences USA, 111, 3775–3780.
52. Howard, J. T., Haile-Mariam, M., Pryce, J. E., & Maltecca, C. (2015). Investigation of regions impacting inbreeding depression and their association with the additive genetic effect for United States and Australia Jersey dairy cattle. BMC Genomics, 16, 813.
53. Hudson, A. G., Vonlanthen, P., & Seehausen, O. (2014). Population structure, inbreeding, and local adaptation within an endangered riverine specialist. Conservation Genetics, 15, 933–951.
54. Huisman, J., Kruuk, L. E., Ellis, P. A., Clutton-Brock, T., & Pemberton, J. M. (2016). Inbreeding depression across the lifespan in a wild mammal population. Proceedings of the National Academy of Sciences USA, 113, 3585–3590.
55. Husband, B. C., & Schemske, D. W. (1996). Evolution of the magnitude and timing of inbreeding depression in plants. Evolution, 50, 54–70.
56. Jacquard, A. (1975). Inbreeding: One word, several meanings. Theoretical Population Biology, 7, 338–363.
57. Johnson, H. E., Mills, L. S., Wehausen, J. D., Stephenson, T. R., & Luikart, G. (2011). Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep. Conservation Biology, 25, 1240–1249.
58. Johnston, S. E., Gratten, J., Bérénos, C., Pilkington, J. G., Clutton-Brock, T. H., Pemberton, J. M., & Slate, J. (2013). Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature, 502, 93–95.
59. Kardos, M., Husby, A., McFarlane, S. E., Qvarnström, A., & Ellegren, H. (2015). Whole-genome resequencing of extreme phenotypes in collared flycatchers highlights the difficulty of detecting quantitative trait loci in natural populations. Molecular Ecology Resources, 16, 727–741.
60. 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.
61. Keller, M. C., Simonson, M. A., Ripke, S., Neale, B. M., Gejman, P. V., Howrigan, D. P., … Schizophrenia Psychiatric Genome-Wide Association Study Consortium. (2012). Runs of homozygosity implicate autozygosity as a schizophrenia risk factor. PLoS Genetics, 8, e1002656.
62. Keller, M. C., Visscher, P. M., & Goddard, M. E. (2011). Quantification of inbreeding due to distant ancestors and its detection using dense single nucleotide polymorphism data. Genetics, 189, 237–249.
63. Keller, L. F., & Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology & Evolution, 17, 230–241.
64. Kijas, J. W. (2013). Detecting regions of homozygosity to map the cause of recessively inherited disease. In C. Gondro, J. van der Werf, & B. Hayes (Eds.), Genome-wide association studies and genomic prediction (pp. 91–106). New York, Heidelberg, Dordrecht, London: Springer.
65. Kirin, M., McQuillan, R., Franklin, C. S., Campbell, H., McKeigue, P. M., & Wilson, J. F. (2010). Genomic runs of homozygosity record population history and consanguinity. PLoS One, 5, e13996.
66. Knief, U., Hemmrich-Stanisak, G., Wittig, M., Franke, A., Griffith, S. C., Kempenaers, B., & Forstmeier, W. (2015). Quantifying realized inbreeding in wid and captive animal populations. Heredity, 114, 397–403.
67. Ku, C. S., Naidoo, N., Teo, S. M., & Pawitan, Y. (2011). Regions of homozygosity and their impact on complex diseases and traits. Human Genetics, 129, 1–15.
68. Lacy, R. C., Alaks, G., & Walsh, A. (1996). Hierarchical analysis of inbreeding depression in Peromyscus polionotus. Evolution, 50, 2187–2200.
69. Lamichhaney, S., Berglund, J., Almén, M. S., Maqbool, K., Grabherr, M., Martinez-Barrio, A., … Andersson, L. (2015). Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature, 518, 371–375.
70. Lander, E. S., & Botstein, D. (1987). Homozygosity mapping: A way to map human recessive traits with the DNA of inbred children. Science, 236, 1567–1570.
71. Lencz, T., Lambert, C., DeRosse, P., Burdick, K. E., Morgan, T. V., Kane, J. M., … Malhotra, A. K. (2007). Runs of homozygosity reveal highly penetrant recessive loci in schizophrenia. Proceedings of the National Academy of Sciences USA, 104, 19942–19947.
72. Li, S., Li, B., Cheng, C., Xiong, Z., Liu, Q., Lai, J., … Yan, J. (2014). Genomic signatures of near-extinction and rebirth of the crested ibis and other endangered species. Genome Biology, 15, 1–17.
73. Malécot, G. (1970). The mathematics of heredity. San Francisco, CA: W. H. Freeman.
74. Mayer, A. K., Rohrschneider, K., Strom, T. M., Glöckle, N., Kohl, S., Wissinger, B., & Weisschuh, N. (2016). Homozygosity mapping and whole-genome sequencing reveals a deep intronic PROM1 mutation causing cone–rod dystrophy by pseudoexon activation. European Journal of Human Genetics, 24, 459–462.
75. McQuillan, R., Eklund, N., Pirastu, N., Kuningas, M., McEvoy, B. P., Esko, T., … ROHgen Consortium. (2012). Evidence of inbreeding depression on human height. PLoS Genetics, 8, e1002655.
76. McQuillan, R., Leutenegger, A. L., Abdel-Rahman, R., Franklin, C. S., Pericic, M., Barac-Lauc, L., … Wilson, J. F. (2008). Runs of homozygosity in European populations. American Journal of Human Genetics, 83, 359–372.
77. Meagher, S., Penn, D. J., & Potts, W. K. (2000). Male–male competition magnifies inbreeding depression in wild house mice. Proceedings of the National Academy of Sciences USA, 97, 3324–3329.
78. Miller, J. M., Malenfant, R. M., David, P., Davis, C. S., Poissant, J., Hogg, J. T., … Coltman, D. W. (2014). Estimating genome-wide heterozygosity: Effects of demographic history and marker type. Heredity, 112, 240–247.
79. Mills, L. S., & Smouse, P. E. (1994). Demographic consequences of inbreeding in remnant populations. The American Naturalist, 144, 412–431.
80. Morton, N. E., Crow, J. F., & Muller, H. J. (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.
81. Nei, M., & Roychoudhury, A. (1974). Sampling variances of heterozygosity and genetic distance. Genetics, 76, 379–390.
82. Ng, P. C., & Hinikoff, S. (2001). Predicting deleterious amino acid substitutions. Genome Research, 11, 863–874.
83. O'Grady, J. J., Brook, B. W., Reed, D. H., Ballou, J. D., Tonkyn, D. W., & Frankham, R. (2006). Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biological Conservation, 133, 42–51.
84. Ohta, T. (1971). Associative overdominance caused by linked detrimental mutations. Genetics Research, 18, 277–286.
85. Ouborg, N. J. (2009). Integrating population genetics and conservation biology in the era of genomics. Biology Letters, 6, 3–6.
86. Paetkau, D., Waits, L. P., Clarkson, P. L., Craighead, L., Vyse, E., Ward, R., & Strobeck, C. (1998). Variation in genetic diversity across the range of North American brown bears. Conservation Biology, 12, 418–429.
87. Paiva, S. R., da Silva Mariante, A., & Blackburn, H. D. (2011). Combining US and Brazilian microsatellite data for a meta-analysis of sheep (Ovis aries) breed diversity: Facilitating the FAO global plan of action for conserving animal genetic resources. Journal of Heredity, 102, 697–704.
88. Palamara, P. F., Lencz, T., Darvasi, A., & Pe'er, I. (2012). Length distributions of identity by descent reveal fine-scale demographic history. American Journal of Human Genetics, 91, 809–822.
89. Palkopoulou, E., Mallick, S., Skoglund, P., Enk, J., Rohland, N., Li, H., … Götherström, A. (2015). Complete genomes reveal signatures of demographic and genetic declines in the woolly mammoth. Current Biology, 25, 1395–1400.
90. Pemberton, J. (2004). Measuring inbreeding depression in the wild: The old ways are the best. Trends in Ecology & Evolution, 19, 613–615.
91. Pemberton, J. M. (2008). Wild pedigrees: The way forward. Proceedings of the Royal Society of London Series B: Biological Sciences, 275, 613–621.
92. Pemberton, T. J., Absher, D., Feldman, M. W., Myers, R. M., Rosenberg, N. A., & Li, J. Z. (2012). Genomic patterns of homozygosity in worldwide human populations. American Journal of Human Genetics, 91, 275–292.
93. Potter, K. M., Jetton, R. M., Dvorak, W. S., Hipkins, V. D., Rhea, R., & Whittier, W. A. (2012). Widespread inbreeding and unexpected geographic patterns of genetic variation in eastern hemlock (Tsuga canadensis), an imperiled North American conifer. Conservation Genetics, 13, 475–498.
94. Powell, J. E., Visscher, P. M., & Goddard, M. E. (2010). Reconciling the analysis of IBD with IBS in complex trait studies. Nature Reviews Genetics, 11, 800–805.
95. Pryce, J. E., Haile-Mariam, M., Goddard, M. E., & Hayes, B. J. (2014). Identification of genomic regions associated with inbreeding depression in Holstein and Jersey dairy cattle. Genetics Selection Evolution, 46, 1–14.
96. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A., Bender, D., … Sham, P. C. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559–575.
97. Putten, V. (1999). Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology, 12, 1125–1137.
98. Ralls, K., Ballou, J. D., Rideout, B. A., & Frankham, R. (2000). Genetic management of chondrodystrophy in California condors. Animal Conservation, 3, 145–153.
99. Ritland, K. (1996). Estimators for pairwise relatedness and individual inbreeding coefficients. Genetics Research, 67, 175–185.
100. Robertson, A. (1965). The interpretation of genotypic ratios in domestic animal populations. Animal Production, 7, 319–324.
101. Royer-Bertrand, B., Castillo-Taucher, S., Moreno-Salinas, R., Cho, T., Chae, J., Chou, M., … Superti-Furga, A. (2015). Mutations in the heat-shock protein A9 (HSPA9) gene cause the EVEN-PLUS syndrome of congenital malformations and skeletal dysplasia. Scientific Reports, 5, 17154.
102. Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W., & Hanski, I. (1998). Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491–494.
103. Santure, A. W., Stapley, J., Ball, A. D., Birkhead, T. R., Burke, T., & Slate, J. (2010). On the use of large marker panels to estimate inbreeding and relatedness: Empirical and simulation studies of a pedigreed zebra finch population typed at 771 SNPs. Molecular Ecology, 19, 1439–1451.
104. Shafer, A. B. A., Gattepaille, L. M., Stewart, R. A., & Wolf, J. B. W. (2015). Demographic inferences using short-read genomic data in an approximate Bayesian computation framework: In silico evaluation of power, biases, and proof of concept in Atlantic walrus. Molecular Ecology, 24, 328–345.
105. Slate, J., David, P., Dodds, K. G., Veenvliet, B. A., Glass, B. C., Broad, T. E., & McEwan, J. C. (2004). Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: Theoretical expectations and empirical data. Heredity, 93, 255–265.
106. Soulé, M. E., & Mills, L. S. (1998). No need to isolate genetics. Science, 282, 1658–1659.
107. Speed, D., & Balding, D. J. (2015). Relatedness in the post-genomic era: Is it still useful? Nature Reviews Genetics, 16, 33–44.
108. Spencer, C. C., Su, Z., Donnelly, P., & Marchini, J. (2009). Designing genome-wide association studies: Sample size, power, imputation, and the choice of genotyping chip. PLoS Genetics, 5, e1000477.
109. Stam, P. (1980). The distribution of the fraction of the genome identical by descent in finite random mating populations. Genetics Research, 35, 131–155.
110. Stoffel, M. A., Esser, M., Kardos, M., Humble, E., Nichols, H., David, P., Hoffman, J. I. (2016). inbreedR: an R package for the analysis of inbreeding based on genetic markers. Methods in Ecology and Evolution, doi: 10.1111/2041-210X.12588. [Epub ahead of print].
111. Szulkin, M., Bierne, N., & David, P. (2010). Heterozygosity-fitness correlations: A time for reappraisal. Evolution, 64, 1202–1217.
112. Taylor, H. R. (2015). The use and abuse of genetic marker-based estimates of relatedness and inbreeding. Ecology and Evolution, 5, 3140–3150.
113. Taylor, H. R., Kardos, M. D., Ramstad, K. M., & Allendorf, F. W. (2015). Valid estimates of individual inbreeding coefficients from marker-based pedigrees are not feasible in wild populations with low allelic diversity. Conservation Genetics, 16, 901–913.
114. Templeton, A. R., & Read, B. (1994). Inbreeding: One word, several meanings, much confusion. In V. Loeschcke, J. Tomiuk, & S. K. Jain (Eds.), Conservation genetics (pp. 91–106). Basel, Switzerland: Birkhäuser-Verlag.
115. Thompson, E. A. (2013). Identity by descent: Variation in meiosis, across genome, and in population. Genetics, 194, 301–326.
116. Trask, A. E., Bignal, E. M., McCracken, D. I., Monaghan, P., Piertney, S. B., & Reid, J. M. (2016). Evidence of a the phenotypic expression of a lethal recessive allele under inbreeding in a wild population of conservation concern. Journal of Animal Ecology, 85, 879–891.
117. Vine, A. E., McQuillin, A., Bass, N. J., Pereira, A., Kandaswamy, R., Robinson, M., … Curtis, D. (2009). No evidence for excess runs of homozygosity in bipolar disorder. Psychiatric Genetics, 19, 165–170.
118. Vonholdt, B. M., Stahler, D. R., Smith, D. W., Earl, D. A., Pollinger, J. P., & Wayne, R. K. (2008). The genealogy and genetic viability of reintroduced Yellowstone grey wolves. Molecular Ecology, 17, 252–274.
119. Wang, J. (2016). Pedigrees or markers: Which are better in estimating relatedness and inbreeding coefficient? Theoretical Population Biology, 107, 4–13.
120. Wang, S., Haynes, C., Barany, F., & Ott, J. (2009). Genome-wide autozygosity mapping in human populations. Genetic Epidemiology, 33, 172–180.
121. Westemeier, R. L., Brawn, J. D., Simpson, S. A., Esker, T. L., Jansen, R. W., Walk, J. W., … Paige, K. N. (1998). Tracking the long-term decline and recovery of an isolated population. Science, 282, 1695–1698.
122. Willis, J. H. (1999). The role of genes of large effect on inbreeding depression in Mimulus guttatus. Evolution, 53, 1678–1691.
123. Wright, S. (1922). Coefficients of inbreeding and relationship. The American Naturalist, 56, 330–338.
124. Yang, J., Benyamin, B., McEvoy, B. P., Gordon, S., Henders, A. K., Nyholt, D. R., … Visscher, P. M. (2010). Common SNPs explain a large proportion of the heritability for human height. Nature Genetics, 42, 565–569.
125. Zemanová, B., Hájková, P., Hájek, B., Martínková, N., Mikulíček, P., Zima, J., & Bryja, J. (2015). Extremely low genetic variation in endangered Tatra chamois and evidence for hybridization with an introduced alpine population. Conservation Genetics, 16, 729–741.