Deleterious alleles in the context of domestication, inbreeding, and selection

Evolutionary Applications

Volumn 12, Issue 1, 2019, Pages 6-17

  Bosse, Mirte ^a   Megens, Hendrik Jan ^a   Derks, Martijn F L ^a   de Cara, Ángeles M R ^b   Groenen, Martien A M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIV MONTPELLIER   (France)

Author keywords

deleterious alleles; domestication; genetic load; inbreeding; selection

Indexed keywords

EID: 85053240932     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12691     Document Type: Article

References (82)

1. Agrawal, A. F., & Whitlock, M. C. (2012). Mutation load: The fitness of individuals in populations where deleterious alleles are abundant. Annual Review of Ecology, Evolution, and Systematics, 43, 115–135. https://doi.org/10.1146/annurev-ecolsys-110411-160257
2. Araki, H., Berejikian, B. A., Ford, M. J., & Blouin, M. S. (2008). Fitness of hatchery-reared salmonids in the wild. Evolutionary Applications, 1(2), 342–355. https://doi.org/10.1111/j.1752-4571.2008.00026.x
3. Begun, D. J., & Aquadro, C. F. (1992). Levels of naturally-occurring DNA polymorphism correlate with recombination rates in Drosophila melanogaster. Nature, 356(6369), 519–520. https://doi.org/10.1038/356519a0
4. Bosse, M., Megens, H. J., Frantz, L. A. F., Madsen, O., Larson, G., Paudel, Y.,… Groenen, M. A. M. (2014). Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression. Nature Communications, 5, 4392
5. Bosse, M., Megens, H. J., Madsen, O., Frantz, L. A. F., Paudel, Y., Crooijmans, R. P. M. A., & Groenen, M. A. M. (2014). Untangling the hybrid nature of modern pig genomes: A mosaic derived from biogeographically distinct and highly divergent Sus scrofa populations. Molecular Ecology, 23(16), 4089–4102. https://doi.org/10.1111/mec.12807
6. Bosse, M., Megens, H. J., Madsen, O., Paudel, Y., Frantz, L. A. F., Schook, L. B., … Groenen, M. A. M. (2012). Regions of homozygosity in the porcine genome: Consequence of demography and the recombination landscape. Plos Genetics, 8(11), e1003100. https://doi.org/10.1371/journal.pgen.1003100
7. de Cara, M. A. R., Villanueva, B., Toro, M. A., & Fernandez, J. (2013a). Purging deleterious mutations in conservation programmes: Combining optimal contributions with inbred matings. Heredity, 110(6), 530–537. https://doi.org/10.1038/hdy.2012.119
8. de Cara, M. A. R., Villanueva, B., Toro, M. A., & Fernandez, J. (2013b). Using genomic tools to maintain diversity and fitness in conservation programmes. Molecular Ecology, 22(24), 6091–6099. https://doi.org/10.1111/mec.12560
9. Casals, F., Hodgkinson, A., Hussin, J., Idaghdour, Y., Bruat, V., de Maillard, T., … Awadalla, P. (2013). Whole-exome sequencing reveals a rapid change in the frequency of rare functional variants in a founding population of humans. Plos Genetics, 9(9)
10. Charlesworth, D. (2006). Balancing selection and its effects on sequences in nearby genome regions. Plos Genetics, 2(4), 379–384
11. Charlesworth, D., & Willis, J. H. (2009). Fundamental concepts in genetics the genetics of inbreeding depression. Nature Reviews Genetics, 10(11), 783–796. https://doi.org/10.1038/nrg2664
12. Charlier, C., Li, W., Harland, C., Littlejohn, M., Coppieters, W., Creagh, F., … Georges, M. (2016). NGS-based reverse genetic screen for common embryonic lethal mutations compromising fertility in livestock. Genome Research, 26(10), 1333–1341. https://doi.org/10.1101/gr.207076.116
13. Chen, J., Glemin, S., & Lascoux, M. (2017). Genetic diversity and the efficacy of purifying selection across plant and animal species. Molecular Biology and Evolution, 34(6), 1417–1428. https://doi.org/10.1093/molbev/msx088
14. Chun, S., & Fay, J. C. (2011). Evidence for hitchhiking of deleterious mutations within the human genome. Plos Genetics, 7(8), e1002240. https://doi.org/10.1371/journal.pgen.1002240
15. Cooper, G. M., Stone, E. A., Asimenos, G., Green, E. D., Batzoglou, S., Sidow, A., & Progra, N. C. S. (2005). Distribution and intensity of constraint in mammalian genomic sequence. Genome Research, 15(7), 901–913. https://doi.org/10.1101/gr.3577405
16. Crow, J. F. (1970a). Genetic loads and the cost of natural selection. Mathematical Topics in Population Genetics, 1, 128–177. https://doi.org/10.1007/978-3-642-46244-3
17. Crow, J. F. (1970b). An introduction to population genetics theory. Caldwell, NJ: Blackburn Press
18. Cruz, F., Vila, C., & Webster, M. T. (2008). The legacy of domestication: Accumulation of deleterious mutations in the dog genome. Molecular Biology and Evolution, 25(11), 2331–2336. https://doi.org/10.1093/molbev/msn177
19. Curik, I., Ferencakovic, M., & Solkner, J. (2014). Inbreeding and runs of homozygosity: A possible solution to an old problem. Livestock Science, 166, 26–34. https://doi.org/10.1016/j.livsci.2014.05.034
20. Derks, M. F. L., Megens, H. J., Bosse, M., Lopes, M. S., Harlizius, B., & Groenen, M. A. M. (2017). A systematic survey to identify lethal recessive variation in highly managed pig populations. BMC Genomics, 18, 858. https://doi.org/10.1186/1471-2164-15-601
21. Derks, M., Megens, H., Bosse, M., Visscher, J., Peeters, K., Bink, M.,… Groenen, M. (2018). A survey of functional genomic variation in domesticated chicken populations. Genetics Selection Evolution, 50, 17
22. Frantz, L. A. F., Schraiber, J. G., Madsen, O., Megens, H. J., Cagan, A., Bosse, M.,… Groenen, M. A. M. (2015). Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes. Nature Genetics, 47(10), 1141–1148
23. Fu, W. Q., Gittelman, R. M., Bamshad, M. J., & Akey, J. M. (2014). Characteristics of neutral and deleterious protein-coding variation among individuals and populations. American Journal of Human Genetics, 95(4), 421–436. https://doi.org/10.1016/j.ajhg.2014.09.006
24. Fumihito, A., Miyake, T., Takada, M., Shingu, R., Endo, T., Gojobori, T., … Ohno, S. (1996). Monophyletic origin and unique dispersal patterns of domestic fowls. Proceedings of the National Academy of Sciences of the United States of America, 93(13), 6792–6795. https://doi.org/10.1073/pnas.93.13.6792
25. Garcia de Leaniz, C., Fleming, I. A., Einum, S., Verspoor, E., Jordan, W. C., Consuegra, S., … Quinn, T. P. (2007). A critical review of adaptive genetic variation in Atlantic salmon: Implications for conservation. Biological Reviews, 82(2), 173–211. https://doi.org/10.1111/j.1469-185X.2006.00004.x
26. Garcia-Dorado, A. (2003). Tolerant versus sensitive genomes: The impact of deleterious mutation on fitness and conservation. Conservation Genetics, 4(3), 311–324. https://doi.org/10.1023/A:1024029432658
27. Garcia-Dorado, A. (2012). Understanding and predicting the fitness decline of shrunk populations: Inbreeding, purging, mutation, and standard selection. Genetics, 190(4), 1461–1476. https://doi.org/10.1534/genetics.111.135541
28. Gazave, E., Chang, D., Clark, A. G., & Keinan, A. (2013). Population growth inflates the per-individual number of deleterious mutations and reduces their mean effect. Genetics, 195(3), 969–978
29. Good, B. H., & Desai, M. M. (2014). Deleterious passengers in adapting populations. Genetics, 198(3), 1183–1208. https://doi.org/10.1534/genetics.114.170233
30. Groenen, M. A. M., Archibald, A. L., Uenishi, H., Tuggle, C. K., Takeuchi, Y., Rothschild, M. F., … Schook, L. B. (2012). Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 491(7424), 393–398. https://doi.org/10.1038/nature11622
31. Hedrick, P. W., & Garcia-Dorado, A. (2016). Understanding inbreeding depression, purging, and genetic rescue. Trends in Ecology and Evolution, 31(12), 940–952. https://doi.org/10.1016/j.tree.2016.09.005
32. Henn, B. M., Botigue, L. R., Bustamante, C. D., Clark, A. G., & Gravel, S. (2015). Estimating the mutation load in human genomes. Nature Reviews Genetics, 16(6), 333–343. https://doi.org/10.1038/nrg3931
33. Hernandez, R. D., Kelley, J. L., Elyashiv, E., Melton, S. C., Auton, A., McVean, G.,… G. Project. (2011). Classic selective sweeps were rare in recent human evolution. Science, 331(6019), 920–924
34. Herrero-Medrano, J. M., Megens, H. J., Groenen, M. A. M., Bosse, M., Perez-Enciso, M., & Crooijmans, R. P. M. A. (2014). Whole-genome sequence analysis reveals differences in population management and selection of European low-input pig breeds. BMC Genomics, 15, 601
35. Howrigan, D. P., Simonson, M. A., & Keller, M. C. (2011). Detecting autozygosity through runs of homozygosity: A comparison of three autozygosity detection algorithms. BMC Genomics, 12, 460
36. Kadri, N. K., Sahana, G., Charlier, C., Iso-Touru, T., Guldbrandtsen, B., Karim, L., … Druet, T. (2014). A 660-kb deletion with antagonistic effects on fertility and milk production segregates at high frequency in Nordic red cattle: Additional evidence for the common occurrence of balancing selection in livestock. Plos Genetics, 10(1), e1004049. https://doi.org/10.1371/journal.pgen.1004049
37. Keller, L. F., & Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology and Evolution, 17(5), 230–241. https://doi.org/10.1016/S0169-5347(02)02489-8
38. Kettunen, A., Daverdin, M., Helfjord, T., & Berg, P. (2017). Cross-breeding is inevitable to conserve the highly inbred population of puffin hunter: The Norwegian Lundehund. PLoS ONE, 12(1), e0170039. https://doi.org/10.1371/journal.pone.0170039
39. Kijas, J. M. H., & Andersson, L. (2001). A phylogenetic study of the origin of the domestic pig estimated from the near-complete mtDNA genome. Journal of Molecular Evolution, 52(3), 302–308. https://doi.org/10.1007/s002390010158
40. Kim, E. S., Cole, J. B., Huson, H., Wiggans, G. R., Van Tassell, C. P., Crooker, B. A., … Sonstegard, T. S. (2013). Effect of artificial selection on runs of homozygosity in US Holstein Cattle. PLoS ONE, 8(11), e80813. https://doi.org/10.1371/journal.pone.0080813
41. Kimura, M. (1963). The mutation load in small populations. Genetics, 48, 1303–1312
42. Kircher, M., Witten, D. M., Jain, P., B. J. O'Roak, G. M. Cooper., & Shendure, J. (2014). A general framework for estimating the relative pathogenicity of human genetic variants. Nature Genetics, 46(3), 310–315
43. Kono, T. J. Y., Fu, F. L., Mohammadi, M., Hoffman, P. J., Liu, C., Stupar, R. M., … Morrell, P. L. (2016). The role of deleterious substitutions in crop genomes. Molecular Biology and Evolution, 33(9), 2307–2317. https://doi.org/10.1093/molbev/msw102
44. Kumar, P., Henikoff, S., & Ng, P. C. (2009). Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nature Protocols, 4(7), 1073–1082. https://doi.org/10.1038/nprot.2009.86
45. Larson, G., Dobney, K., Albarella, U., Fang, M. Y., Matisoo-Smith, E., Robins, J., … Cooper, A. (2005). Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science, 307(5715), 1618–1621. https://doi.org/10.1126/science.1106927
46. Li, Y. R., Vinckenbosch, N., Tian, G., Huerta-Sanchez, E., Jiang, T., Jiang, H., … Wang, J. (2010). Resequencing of 200 human exomes identifies an excess of low-frequency non-synonymous coding variants. Nature Genetics, 42(11), 969–982. https://doi.org/10.1038/ng.680
47. Liu, Q. P., Zhou, Y. F., Morrell, P. L., & Gaut, B. S. (2017). Deleterious variants in Asian rice and the potential cost of domestication. Molecular Biology and Evolution, 34(4), 908–924
48. Lohmueller, K. E. (2014). The distribution of deleterious genetic variation in human populations. Current Opinion in Genetics and Development, 29, 139–146. https://doi.org/10.1016/j.gde.2014.09.005
49. Lohmueller, K. E., Indap, A. R., Schmidt, S., Boyko, A. R., Hernandez, R. D., Hubisz, M. J., … Bustamante, C. D. (2008). Proportionally more deleterious genetic variation in European than in African populations. Nature, 451(7181), 994–995. https://doi.org/10.1038/nature06611
50. Lu, J., Tang, T., Tang, H., Huang, J. Z., Shi, S. H., & Wu, C. I. (2006). The accumulation of deleterious mutations in rice genomes: A hypothesis on the cost of domestication. Trends in Genetics, 22(3), 126–131. https://doi.org/10.1016/j.tig.2006.01.004
51. Lush, J. L. (1946). Chance as a cause of changes in gene frequency within pure breeds of livestock. American Naturalist, 80(792), 318–342. https://doi.org/10.1086/281448
52. Lynch, M., Ackerman, M. S., Gout, J. F., Long, H., Sung, W., Thomas, W. K., & Foster, P. L. (2016). Genetic drift, selection and the evolution of the mutation rate. Nature Reviews Genetics, 17(11), 704–714. https://doi.org/10.1038/nrg.2016.104
53. Lynch, M., Conery, J., & Burger, R. (1995). Mutation accumulation and the extinction of small populations. American Naturalist, 146(4), 489–518. https://doi.org/10.1086/285812
54. Makino, T., Rubin, C. J., Carneiro, M., Axelsson, E., Andersson, L., & Webster, M. T. (2018). Elevated proportions of deleterious genetic variation in domestic animals and plants. Genome Biology and Evolution, 10(1), 276–290. https://doi.org/10.1093/gbe/evy004
55. Marsden, C. D., Ortega-Del Vecchyo, D., O'Brien, D. P., Taylor, J. F., Ramirez, O., Vila, C., … Lohmueller, K. E. (2016). Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs. Proceedings of the National Academy of Sciences of the United States of America, 113(1), 152–157. https://doi.org/10.1073/pnas.1512501113
56. Maruyama, T. (1974). The age of a rare mutant gene in a large population. American Journal of Human Genetics, 26(669)
57. Maynard Smith, J., & Haigh, J. (1974). The hitch-hiking effect of a favourable gene. Genetics Research, 23, 23–35. https://doi.org/10.1017/S0016672300014634
58. McLaren, W., Gil, L., Hunt, S. E., Riat, H. S., Ritchie, G. R. S., Thormann, A.,… Cunningham, F. (2016). The ensembl variant effect predictor. Genome Biology, 17(1), 122. https://doi.org/10.1186/s13059-016-0974-4
59. Mezmouk, S., & Ross-Ibarra, J. (2014). The pattern and distribution of deleterious mutations in maize. G3-Genes, Genomes, Genetics, 4(1), 163–171
60. Miao, Y. W., Peng, M. S., Wu, G. S., Ouyang, Y. N., Yang, Z. Y., Yu, N., … Zhang, Y. P. (2013). Chicken domestication: An updated perspective based on mitochondrial genomes. Heredity, 110(3), 277–282. https://doi.org/10.1038/hdy.2012.83
61. Mukai, T., Chigusa, S. I., Crow, J. F., & Mettler, L. E. (1972). Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics, 72(2), 335–355
62. Ngeno, K. (2015). Breeding program for indigenous chicken in Kenya. Analysis of diversity in indigenous chicken populations, Wageningen University
63. Ngeno, K., Van der Waaij, E., Megens, H., Kahi, A., Van Arendonk, J., & Crooijmans, R. (2015). Genetic diversity of different indigenous chicken ecotypes using highly polymorphic MHC-linked and non-MHC microsatellite markers. Animal Genetic Resources/Ressources Génétiques Animales/Recursos Genéticos Animales, 56, 1–7
64. Ohta, T. (1973). Slightly deleterious mutant substitutions in evolution. Nature, 246(5428), 96–98. https://doi.org/10.1038/246096a0
65. Oldenbroek, K. (2017). Genomic management of animal genetic diversity. Wageningen, The Netherlands: Wageningen Academic Publishers. https://doi.org/10.3920/978-90-8686-297-9
66. Pausch, H., Schwarzenbacher, H., Burgstaller, J., Flisikowski, K., Wurmser, C., Jansen, S.,… Fries, R. (2015). Homozygous haplotype deficiency reveals deleterious mutations compromising reproductive and rearing success in cattle. BMC Genomics, 16, 312. https://doi.org/10.1186/s12864-015-1483-7
67. Ramos, A. M., Crooijmans, R. P. M. A., Affara, N. A., Amaral, A. J., Archibald, A. L., Beever, J. E., … Groenen, M. A. M. (2009). Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS ONE, 4(8), e6524. https://doi.org/10.1371/journal.pone.0006524
68. Renaut, S., & Rieseberg, L. H. (2015). The accumulation of deleterious mutations as a consequence of domestication and improvement in sunflowers and other compositae crops. Molecular Biology and Evolution, 32(9), 2273–2283. https://doi.org/10.1093/molbev/msv106
69. Romiguier, J., Gayral, P., Ballenghien, M., Bernard, A., Cahais, V., Chenuil, A., … Galtier, N. (2014). Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515(7526), 261–263. https://doi.org/10.1038/nature13685
70. Scheu, A., Powell, A., Bollongino, R., Vigne, J. D., Tresset, A., Cakirlar, C.,… Burger, J. (2015). The genetic prehistory of domesticated cattle from their origin to the spread across Europe. BMC Genetics, 16, 54
71. Schoenebeck, J. J., & Ostrander, E. A. (2014). Insights into morphology and disease from the dog genome project. Annual Review of Cell and Developmental Biology, 30(30), 535–560. https://doi.org/10.1146/annurev-cellbio-100913-012927
72. Schubert, M., Jonsson, H., Chang, D., Sarkissian, C. D., Ermini, L., Ginolhac, A., … Orlando, L. (2014). Prehistoric genomes reveal the genetic foundation and cost of horse domestication. Proceedings of the National Academy of Sciences of the United States of America, 111(52), E5661–E5669. https://doi.org/10.1073/pnas.1416991111
73. Simons, Y. B., & Sella, G. (2016). The impact of recent population history on the deleterious mutation load in humans and close evolutionary relatives. Current Opinion in Genetics and Development, 41, 150–158. https://doi.org/10.1016/j.gde.2016.09.006
74. Simons, Y. B., Turchin, M. C., Pritchard, J. K., & Sella, G. (2014). The deleterious mutation load is insensitive to recent population history. Nature Genetics, 46(3), 220–224
75. Szpiech, Z. A., Xu, J. S., Pemberton, T. J., Peng, W. P., Zollner, S., Rosenberg, N. A., & Li, J. Z. (2013). Long runs of homozygosity are enriched for deleterious variation. American Journal of Human Genetics, 93(1), 90–102. https://doi.org/10.1016/j.ajhg.2013.05.003
76. VanRaden, P. M., Olson, K. M., Null, D. J., & Hutchison, J. L. (2011). Harmful recessive effects on fertility detected by absence of homozygous haplotypes. Journal of Dairy Science, 94(12), 6153–6161. https://doi.org/10.3168/jds.2011-4624
77. Wang, K., Li, M. Y., & Hakonarson, H. (2010). ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Research, 38(16), e164. https://doi.org/10.1093/nar/gkq603
78. White, S. (2011). From globalized pig breeds to capitalist pigs: A study in animal cultures and evolutionary history. Environmental History, 16(1), 94–120. https://doi.org/10.1093/envhis/emq143
79. Whitlock, M. C. (2000). Fixation of new alleles and the extinction of small populations: Drift load, beneficial alleles, and sexual selection. Evolution, 54(6), 1855–1861. https://doi.org/10.1111/j.0014-3820.2000.tb01232.x
80. Yang, B., Cui, L. L., Perez-Enciso, M., Traspov, A., Crooijmans, R. P. M. A., Zinovieva, N.,… Megens, H. J. (2017). Genome-wide SNP data unveils the globalization of domesticated pigs. Genetics Selection Evolution, 49, 71
81. Zhang, Q. Q., Guldbrandtsen, B., Bosse, M., Lund, M. S., & Sahana, G. (2015). Runs of homozygosity and distribution of functional variants in the cattle genome. BMC Genomics, 16, 542
82. Zhou, Y. F., Massonnet, M., Sanjak, J. S., Cantu, D., & Gaut, B. S. (2017). Evolutionary genomics of grape (Vitis vinifera ssp. vinifera) domestication. Proceedings of the National Academy of Sciences of the United States of America, 114(44), 11715–11720