Inbreeding rate modifies the dynamics of genetic load in small populations

Ecology and Evolution

Volumn 2, Issue 8, 2012, Pages 1791-1804

  Pekkala, Nina ^a   Knott, K Emily ^a   Kotiaho, Janne S ^a   Puurtinen, Mikael ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

Author keywords

Drosophila littoralis; Extinction; Genetic drift; Inbreeding depression; Offspring production; Purging

Indexed keywords

EID: 84868202356     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.293     Document Type: Article

References (69)

1. Amos, W., and A. Balmford. 2001. When does conservation genetics matter?Heredity 87:257-265.
2. Ballou, J. D. 1997. Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. J. Hered. 88:169-178.
3. Barrett, S. C. H., and D. Charlesworth. 1991. Effects of a change in the level of inbreeding on the genetic load. Nature 352:522-524.
4. Bataillon, T., and M. Kirkpatrick. 2000. Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter. Genet. Res. 75:75-81.
5. Bijlsma, R., J. Bundgaard, and W. F. van Putten. 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J. Evol. Biol. 12:1125- 1137.
6. Bijlsma, R., J. Bundgaard, and A. C. Boerema. 2000. Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J. Evol. Biol. 13:502-514.
7. Boakes, E. H., J. Wang, and W. Amos. 2007. An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98:172-182.
8. Bryant, E. H., L. M. Meffert, and S. A. McCommas. 1990. Fitness rebound in serially bottlenecked populations of the house fly. Am. Nat. 136:542-549.
9. Bryant, E. H., V. L. Vackus, M. E. Clark, and D. H. Reed. 1999. Experimental tests of captive breeding for endangered species. Conserv. Biol. 13:1487-1496.
10. Byers, D. L., and D. M. Waller. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu. Rev. Ecol. Syst. 30:479-513.
11. Charlesworth, D., and J. H. Willis. 2009. The genetics of inbreeding depression. Nat. Rev. Genet. 10:783-796.
12. Crnokrak, P., and S. C. H. Barrett. 2002. Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347-2358.
13. Crow, J., and M. Kimura. 1970. An introduction to population genetics theory. Harper & Row, New York.
14. Day, S. B., E. H. Bryant, and L. M. Meffert. 2003. The influence of variable rates of inbreeding on fitness, environmental responsiveness, and evolutionary potential. Evolution 57:1314-1324.
15. Demontis, D., C. Pertoldi, V. Loeschcke, K. Mikkelsen, T. Axelsson, and T. N. Kristensen. 2009. Efficiency of selection, as measured by single nucleotide polymorphism variation, is dependent on inbreeding rate in Drosophila melanogaster. Mol. Ecol. 18:4551-4563.
16. Ehiobu, N. G., M. E. Goddard, and J. F. Taylor. 1989. Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster. Theor. Appl. Genet. 77:123-127.
17. Ellegren, H., G. Hartman, M. Johansson, and L. Andersson. 1993. Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc. Natl Acad. Sci. USA 90:8150-8153.
18. Ewers, R. M., and R. K. Didham. 2006. Confounding factors in the detection of species responses to habitat fragmentation. Biol. Rev. 81:117-142.
19. Eyre-Walker, A., and P. D. Keightley. 2007. The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8:610- 618.
20. Facon, B., R. A. Hufbauer, A. Tayeh, A. Loiseau, E. Lombaert, R. Vitalis, et al. 2011. Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr. Biol. 21:424-427.
21. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Prentice Hall, Harlow, England.
22. Frankham, R. 1995. Inbreeding and extinction - a threshold effect. Conserv. Biol. 9:792-799.
23. Frankham, R. 2005. Genetics and extinction. Biol. Conserv. 126:131-140.
24. Frankham, R. 2007. Effective population size/adult population size ratios in wildlife: a review (Reprinted from Genet. Res., Camb., vol 66, pg 95-107, 1995). Genet. Res. 89:491-503.
25. Frankham, R., D. Gilligan, D. Morris, and D. Briscoe. 2001. Inbreeding and extinction: effects of purging. Conserv. Genet. 2:279-285.
26. Glemin, S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678-2687.
27. Goudet, J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at http://www2.unil.ch/popgen/softwares/fstat.html. Accessed May 1, 2012.
28. Hedrick, P. W. 1994. Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73:363-372.
29. Hedrick, P. W. 2002. Lethals in finite populations. Evolution 56:654-657.
30. Hoelzel, A. R., J. Halley, S. J. Obrien, C. Campagna, T. Arnbom, B. Leboeuf, et al. 1993. Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. J. Hered. 84:443-449.
31. IUCN. 2011. The IUCN red list of threatened species. Version 2011.2. Available at http://www.iucnredlist.org. Accessed on April 13, 2012.
32. Kimura, M., T. Maruyama, and J. F. Crow. 1963. The mutation load in small populations. Genetics 48:1303-1312.
33. Kirkpatrick, M., and P. Jarne. 2000. The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155:154-167.
34. Kristensen, T. N., M. R. Knudsen, and V. Loeschcke. 2011. Slow inbred lines of Drosophila melanogaster express as much inbreeding depression as fast inbred lines under seminatural conditions. Genetica 139:441-451.
35. Lacy, R. C., and J. D. Ballou. 1998. Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution 52:900-909.
36. Lakovaara, S. 1969. Malt as a culture medium for Drosophila species. Drosophila Inf. Serv. 44:128.
37. Lande, R. 1988. Genetics and demography in biological conservation. Science 241:1455-1460.
38. Lande, R. 1994. Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460-1469.
39. Lande, R. 1998. Risk of population extinction from fixation of deleterious and reverse mutations. Genetica 102-103: 21-27.
40. Larsen, L. K., C. Pelabon, G. H. Bolstad, A. Viken, I. A. Fleming, and G. Rosenqvist. 2011. Temporal change in inbreeding depression in life-history traits in captive populations of guppy (Poecilia reticulata): evidence for purging?J. Evol. Biol. 24:823-834.
41. Latter, B. D. H., J. C. Mulley, D. Reid, and L. Pascoe. 1995. Reduced genetic load revealed by slow inbreeding in Drosophila melanogaster. Genetics 139:287-297.
42. Leberg, P. L., and B. D. Firmin. 2008. Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol. Ecol. 17:334-343.
43. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MA.
44. Lynch, M., J. Conery, and R. Burger. 1995a. Mutation accumulation and the extinction of small population. Am. Nat. 146:489-518.
45. Lynch, M., J. Conery, and R. Burger. 1995b. Mutational meltdowns in sexual populations. Evolution 49:1067-1080.
46. Mikkelsen, K., V. Loeschcke, and T. N. Kristensen. 2010. Trait specific consequences of fast and slow inbreeding: lessons from captive populations of Drosophila melanogaster. Conserv. Genet. 11:479-488.
47. Miller, P. S., and P. W. Hedrick. 2001. Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. J. Evol. Biol. 14:595-601.
48. Mills, L. S. 2007. Conservation of wildlife populations: demography, genetics, and management. Blackwell Publishing, Malden, MA.
49. Newman, D., and D. Pilson. 1997. Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51:354-362.
50. O'Grady, J. J., B. W. Brook, D. H. Reed, J. D. Ballou, D. W. Tonkyn, and R. Frankham. 2006. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 133:42-51.
51. Peakall, R., and P. E. Smouse. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6:288-295.
52. Pedersen, K. S., T. N. Kristensen, and V. Loeschcke. 2005. Effects of inbreeding and rate of inbreeding in Drosophila melanogaster - Hsp70 expression and fitness. J. Evol. Biol. 18:756-762.
53. Radwan, J. 2003. Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini. Heredity 90:371-376.
54. Reed, D., and E. Bryant. 2001. Fitness, genetic load and purging in experimental populations of the housefly. Conserv. Genet. 2:57-61.
55. Reed, D. H., E. H. Lowe, D. A. Briscoe, and R. Frankham. 2003. Inbreeding and extinction: effects of rate of inbreeding. Conserv. Genet. 4:405-410.
56. Rosenthal, R. 1991. Meta-analytic procedures for social research. Sage, Newbury Park, CA.
57. Routtu, J., A. Hoikkala, and M. Kankare. 2007. Microsatellitebased species identification method for Drosophila virilis group species. Hereditas 144:213-221.
58. Saccheri, I. J., P. M. Brakefield, and R. A. Nichols. 1996. Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50:2000-2013.
59. Saccheri, I. J., M. Kuussaari, M. Kankare, P. Vikman, W. Fortelius, and I. Hanski. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392:491-494.
60. Spielman, D., B. W. Brook, and R. Frankham. 2004. Most species are not driven to extinction before genetic factors impact them. Proc. Natl Acad. Sci. USA 101: 15261-15264.
61. Swindell, W. R., and J. L. Bouzat. 2006a. Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution 60:762-767.
62. Swindell, W. R., and J. L. Bouzat. 2006b. Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J. Evol. Biol. 19:1257- 1264.
63. Swindell, W. R., and J. L. Bouzat. 2006c. Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 60:1014-1022.
64. Theodorou, K., and D. Couvet. 2006. On the expected relationship between inbreeding, fitness, and extinction. Genet. Select. Evol. 38:371-387.
65. Visscher, P. M. 2001. A viable herd of genetically uniform cattle. Nature 409:303.
66. Wang, J. L., W. G. Hill, D. Charlesworth, and B. Charlesworth. 1999. Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet. Res. 74:165-178.
67. Whitlock, M. C. 2000. Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 54:1855-1861.
68. Willis, J. H. 1999. The role of genes of large effect on inbreeding depression in Mimulus guttatus. Evolution 53:1678-1691.
69. Windig, J. J., R. F. Veerkamp, and S. Nylin. 2004. Quantitative genetic variation in an island population of the speckled wood butterfly (Pararge aegeria). Heredity 93:450-454.