Resolving the conundrum of inbreeding depression but no inbreeding avoidance: Estimating sex-specific selection on inbreeding by song sparrows (Melospiza melodia)

Evolution

Volumn 69, Issue 11, 2015, Pages 2846-2861

  Reid, Jane M ^a   Arcese, Peter ^b   Bocedi, Greta ^a   Duthie, A Bradley ^a   Wolak, Matthew E ^a   Keller, Lukas F ^c  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Fitness; Mate choice; Mating system; Pedigree; Relatedness; Selection gradient

Indexed keywords

FITNESS; INBREEDING AVOIDANCE; MATE CHOICE; PASSERINE; PHENOTYPE; RELATEDNESS; REPRODUCTION; REPRODUCTIVE STRATEGY; SEXUAL SELECTION; SURVIVAL;

MELOSPIZA; MELOSPIZA MELODIA;

ANIMAL; FEMALE; GENETICS; INBREEDING; MALE; PEDIGREE; PHENOTYPE; REPRODUCTION; REPRODUCTIVE FITNESS; SEXUAL BEHAVIOR; SPARROW;

ANIMALS; FEMALE; GENETIC FITNESS; INBREEDING; MALE; PEDIGREE; PHENOTYPE; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SPARROWS;

EID: 84955178182     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12780     Document Type: Article

References (91)

1. Ala-Honkola, O., M. K. Manier, S. Lüpold, and S. Pitnick . 2011. No evidence for postcopulatory inbreeding avoidance in Drosophila melanogaster. Evolution 65:2699-2705.
2. Benesh, D. P., F. Weinreich, M. Kalbe, and M. Milinski . 2014. Lifetime inbreeding depression, purging, and mating system evolution in a simultaneous hermaphrodite tapeworm. Evolution 68:1762-1774.
3. Billing, A. M., A. M. Lee, S. Skjelseth, Å. A. Borg, M. C. Hale, J. Slate, H. Pärn, T. H. Ringsby, B.-E. Sæther, and H. Jensen . 2012. Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population. Mol. Ecol. 21:1487-1499.
4. Breden, F., and M. J. Wade . 1991. Runaway social evolution: reinforcing selection for inbreeding and altruism. J. Theor. Biol. 153:323-337.
5. Bretman, A., D. Newcombe, and T. Tregenza . 2009. Promiscuous females avoid inbreeding by controlling sperm storage. Mol. Ecol. 18:3340-3345.
6. Busch, J. W., and L. F. Delph . 2012. The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Ann. Bot. 109:553-562.
7. Chapman, J. R., S. Nakagawa, D. W. Coltman, J. Slate, and B. C. Sheldon . 2009. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol. Ecol. 18:2746-2765.
8. Charlesworth, D. 2006. Evolution of plant breeding systems. Cur. Biol. 16:R726-R735.
9. Charlesworth, D., and B. Charlesworth . 1987. Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecol. Syst. 18:237-268.
10. Charlesworth, D., and J. H. Willis . 2009. The genetics of inbreeding depression. Nat. Rev. Gen. 10:783-796.
11. Day, T., and S. P. Otto . 2001. Fitness. Encyclopedia of life sciences. John Wiley & Sons.
12. Duthie, A. B., and J. M. Reid . 2015. Inbreeding by rejected relatives and the inclusive fitness benefit of inbreeding avoidance. PLoS One 10:e0125140.
13. Edvardsson, M., R. Rodríguez-Muñoz, and T. Tregenza . 2008. No evidence that female bruchid beetles, Callosobruchus maculatus, use remating to reduce costs of inbreeding. Anim. Behav. 75:1519-1524.
14. Engen, S., R. Lande, and B.-E. Sæther . 2011. Evolution of a plastic quantitative trait in an age-structured population in a fluctuating environment. Evolution 65:2893-2906.
15. Firman, R. C., and L. W. Simmons . 2007. Polyandry facilitates postcopulatory inbreeding avoidance in house mice. Evolution 62:603-611.
16. Fitzpatrick, J. L., and J. P. Evans . 2014. Postcopulatory inbreeding avoidance in guppies. J. Evol. Biol. 27:2686-2694.
17. Goodwillie, C., S. Kalisz, and C. G. Eckert . 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 36:47-79.
18. Griffith, S. C., I. P. F. Owens, and K. A. Thuman . 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11:2195-2212.
19. Grueber, C. E., R. J. Laws, S. Nakagawa, and I. G. Jamieson . 2010. Inbreeding depression accumulation across life-history stages of the endangered Takahe. Cons. Biol. 24:1617-1625.
20. Hadfield, J. D. 2008. Estimating evolutionary parameters when viability selection is operating. Proc. R. Soc. B 275:723-734.
21. Hansson, B., L. Jack, J. K. Christians, J. M. Pemberton, M. Åkesson, H. Westerdahl, S. Bensch, and D. Hasselquist . 2007. No evidence for inbreeding avoidance in a great reed warbler population. Behav. Ecol. 18:157-164.
22. Hereford, J., T. F. Hansen, and D. Houle . 2004. Comparing strengths of directional selection: how strong is strong? Evolution 58:2133-2143.
23. Herfindal, I., H. Haanes, K. H. Røed, E. J. Solberg, S. S. Markussen, M. Heim, and B.-E. Sæther . 2014. Population properties affect inbreeding avoidance in moose. Biol. Lett. 10:20140786.
24. Hunt, J., L. F. Bussière, M. D. Jennions, and R. Brooks . 2004. What is genetic quality? Trends Ecol. Evol. 19:329-333.
25. Ihle, M., and W. Forstmeier . 2013. Revisiting the evidence for inbreeding avoidance in zebra finches. Behav. Ecol. 24:1356-1362.
26. Jamieson, I. G., S. S. Taylor, L. N. Tracy, H. Kokko, and D. P. Armstrong . 2009. Why some species of birds do not avoid inbreeding: insights from New Zealand robins and saddlebacks. Behav. Ecol. 20:575-584.
27. Jarne, P., and D. Charlesworth . 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annu. Rev. Ecol. Syst. 24:441-466.
28. Jennions, M. D., J. Hunt, R. Graham, and R. Brooks . 2004. No evidence for inbreeding avoidance through postcopulatory mechanisms in the black field cricket, Teleogryllus commodus. Evolution 58:2472-2477.
29. Keller, L. F. 1998. Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240-250.
30. Keller, L. F., and P. Arcese . 1998. No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia). Am. Nat. 152:380-392.
31. Keller, L. F., and D. M. Waller . 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230-241.
32. Keller, L. F., K. J. Jeffery, P. Arcese, M. A. Beaumont, W. M. Hochachka, J. N. M. Smith, and M. W. Bruford . 2001. Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc. R. Soc. B 268:1387-1394.
33. Keller, L. F., J. M. Reid, and P. Arcese . 2008. Testing evolutionary models of senescence in a natural population: age and inbreeding effects on fitness components in song sparrows. Proc. R. Soc. B 275:597-604.
34. Kirkpatrick, M., and N. H. Barton . 1996. The strength of indirect selection on female mating preferences. Proc. Natl. Acad. Sci. 94:1282-1286.
35. Kokko, H., and I. Ots . 2006. When not to avoid inbreeding. Evolution 60:467-475.
36. Kokko, H., R. Brooks, M. D. Jennions, and J. Morley . 2003. The evolution of mate choice and mating biases. Proc. R. Soc. B 270:653-664.
37. Kruuk, L. E. B., B. C. Sheldon, and J. Merilä . 2002. Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc. R. Soc. B 269:1581-1589.
38. Kruuk, L. E. B., J. Slate, and A. J. Wilson . 2008. New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annu. Rev. Ecol. Evol. Syst. 39:525-548.
39. Lande, R., and S. J. Arnold . 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
40. Lande, R., and D. W. Schemske . 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic model. Evolution 39:24-40.
41. Lebigre, C., P. Arcese, R. J. Sardell, L. F. Keller, and J. M. Reid . 2012. Extra-pair paternity and the variance in male fitness in song sparrows (Melospiza melodia). Evolution 66:3111-3129.
42. Lehmann, L., and N. Perrin . 2003. Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am. Nat. 162:638-652.
43. Liu, X., X. Tu, H. He, C. Chen, and F. Xue . 2014. Evidence for inbreeding depression and pre-copulatory but not post-copulatory inbreeding avoidance in the cabbage beetle Colaphellus bowringi. PLoS One 9:e94389.
44. Lynch, M., and B. Walsh . 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland.
45. Lyon, B. E., and R. Montgomerie . 2012. Sexual selection is a form of social selection. Phil. Trans. R. Soc. B 367:2266-2273.
46. Matsumura, S., R. Arlinghaus, and U. Dieckmann . 2012. Standardizing selection strengths to study selection in the wild: a critical comparison and suggestions for the future. BioScience 62:1039-1054.
47. Michod, R. 1979. Genetical aspects of kin selection: effects of inbreeding. J. Theor. Biol. 81:223-233.
48. Mojica, J. P., and J. K. Kelly . 2010. Viability selection prior to trait expression is an essential component of natural selection. Proc. R. Soc. B 277:2945-2950.
49. Morrissey, M. B., L. E. B. Kruuk, and A. J. Wilson . 2010. The danger of applying the breeder's equation in observational studies of natural populations. J. Evol. Biol. 23:2277-2288.
50. Morton, N. E., J. F. Crow, and H. J. Muller . 1956. An estimate of the mutational damage in man from data on consanguineous marriages. Proc. Natl. Acad. Sci. 42:855-863.
51. Nietlisbach, P., G. Camenisch, T. Bucher, J. Slate, L. F. Keller, and E. Postma . 2015. A microsatellite-based linkage map for song sparrows. Mol. Ecol. Res. 15:1486-1496.
52. Olson, L. E., D. T. Blumstein, J. R. Pollinger, and R. K. Wayne . 2012. No evidence of inbreeding avoidance despite demonstrated survival costs in a polygynous rodent. Mol. Ecol. 21:562-571.
53. Parker, G. A. 2006. Sexual conflict over mating and fertilization: an overview. Phil. Trans. R. Soc. B 361:235-259.
54. Pizzari, T., H. Løvlie, and C. K. Cornwallis . 2004. Sex-specific, counteracting responses to inbreeding in a bird. Proc. R. Soc. B 271:2115-2121.
55. Porcher, E., and R. Lande . 2005. The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. J. Evol. Biol. 18:497-508.
56. Pusey, A., and M. Wolf . 1996. Inbreeding avoidance in animals. Trends Ecol. Evol. 11:201-206.
57. R Core Team . 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.
58. Rausher, M. D. 1992. The measurement of selection on quantitative traits: biases due to environmental covariances between traits and fitness. Evolution 46:616-626.
59. Reid, J. M. 2012. Predicting evolutionary responses to selection on polyandry in the wild: additive genetic covariances with female extra-pair reproduction. Proc. R. Soc. B 279:4652-4660.
60. Reid, J. M., P. Arcese, A. L. E. V. Cassidy, S. M. Hiebert, J. N. M. Smith, P. K. Stoddard, A. B. Marr, and L. F. Keller . 2005. Fitness correlates of song repertoire size in free-living song sparrows. Am. Nat. 165:299-310.
61. Reid, J. M., P. Arcese, and L. F. Keller . 2006. Intrinsic parent-offspring correlation in inbreeding level in a song sparrow (Melospiza melodia) population open to immigration. Am. Nat. 168:1-13.
62. Reid, J. M., P. Arcese, and L. F. Keller . 2008. Individual phenotype, kinship, and the occurrence of inbreeding in song sparrows. Evolution 62:887-899.
63. Reid, J. M., P. Arcese, R. J. Sardell, and L. F. Keller . 2011a. Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia). Proc. R. Soc. B 278:1114-1120.
64. Reid, J. M., P. Arcese, R. J. Sardell, and L. F. Keller . 2011b. Additive genetic variance, heritability and inbreeding depression in male extra-pair reproductive success. Am. Nat. 177:177-187.
65. Reid, J. M., L. F. Keller, A. B. Marr, P. Nietlisbach, R. J. Sardell, and P. Arcese . 2014. Pedigree error due to extra-pair reproduction substantially biases estimates of inbreeding depression. Evolution 68:802-815.
66. Reid, J. M., P. Arcese, L. F. Keller, R. R. Germain, A. B. Duthie, S. Losdat, M. E. Wolak, and P. Nietlisbach . 2015a. Quantifying inbreeding avoidance through extra-pair reproduction. Evolution 69:59-74.
67. Reid, J. M., A. B. Duthie, M. E. Wolak, and P. Arcese . 2015b. Demographic mechanisms of inbreeding adjustment through extra-pair reproduction. J. Anim. Ecol. 84:1029-1040.
68. Reynolds, S. M., J. A. C. Uy, G. L. Patricelli, S. W. Coleman, M. J. Braun, and G. Borgia . 2014. Tests of the kin selection model of mate choice and inbreeding avoidance in satin bowerbirds. Behav. Ecol. 25:1005-1014.
69. Rioux-Paquette, E., M. Festa-Bianchet, and D. W. Coltman . 2010. No inbreeding avoidance in an isolated population of bighorn sheep. Anim. Behav. 80:865-871.
70. Robinson, S. P., W. J. Kennington, and L. W. Simmons . 2012. Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster. J. Evol. Biol. 25:716-725.
71. Sardell, R. J., L. F. Keller, P. Arcese, T. Bucher, and J. M. Reid . 2010. Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows Melospiza melodia. Mol. Ecol. 19:4352-4364.
72. Schørring, S., and I. Jäger . 2007. Incestuous mate preference by a simultaneous hermaphrodite with strong inbreeding depression. Evolution 61:423-430.
73. Sletvold, N., M. Mousset, J. Hagenblad, B. Hansson, and J. Ågren . 2013. Strong inbreeding depression in two Scandinavian populations of the self-incompatible perennial herb Arabidopsis lyrata. Evolution 67:2876-2888.
74. Smith, J. N. M., L. F. Keller, A. B. Marr, and P. Arcese . 2006. Conservation and biology of small populations-the song sparrows of Mandarte island. Oxford Univ. Press, New York.
75. Stone, J. L., E. J. VanWyk, and J. R. Hale . 2014. Transmission advantage favors selfing allele in experimental populations of self-incompatible Witheringia solanacea (Solanaceae). Evolution 68:1845-1855.
76. Szulkin, M., and B. C. Sheldon . 2008. Dispersal as a means of inbreeding avoidance in a wild bird population. Proc. R. Soc. B 275:703-711.
77. Szulkin, M., D. Garant, R. H. McCleery, and B. C. Sheldon . 2007. Inbreeding depression along a life-history continuum in the great tit. J. Evol. Biol. 20:1531-1543.
78. Szulkin, M., K. V. Stopher, J. M. Pemberton, and J. M. Reid . 2013. Inbreeding avoidance, tolerance, or preference in animals? Trends Ecol. Evol. 28:205-211.
79. Tan, C. K. W., H. Løvlie, T. Pizzari, and S. Wigby . 2012. No evidence for pre-copulatory inbreeding avoidance in Drosophila melanogaster. Anim. Behav. 83:1433-1441.
80. Tregenza, T., and N. Wedell . 2000. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9:1013-1027.
81. van Buskirk, J., and Y. Willi . 2006. The change in quantitative genetic variation with inbreeding. Evolution 60:2428-2434.
82. Wagenius, S., H. H. Hangelbroek, C. E. Ridley, and R. G. Shaw . 2010. Biparental inbreeding and interremnant mating in a perennial pairie plant: fitness consequences for progeny in their first eight years. Evolution 64:761-771.
83. Waser, P. M., S. N. Austad, and B. Keane . 1986. When should animals tolerate inbreeding? Am. Nat. 128:529-537.
84. Webster, M. S., S. Pruett-Jones, D. F. Westneat, and S. J. Arnold . 1995. Measuring the effects of pairing success, extra-pair copulations and mate quality on the opportunity for sexual selection. Evolution 49:1147-1157.
85. Weir, L. K., J. W. A. Grant, and J. A. Hutchings . 2011. The influence of operational sex ratio on the intensity of competition for mates. Am. Nat. 177:167-176.
86. Willis, J. H. 1993. Effects of different levels of inbreeding on fitness components in Mimulus guttatus. Evolution 47:864-876.
87. Wilson, A. G., and P. Arcese . 2008. Influential factors for natal dispersal in an avian island metapopulation. J. Av. Biol. 39:341-347.
88. Wolak, M. E., and L. F. Keller . 2014. Dominance genetic variance and inbreeding in natural populations. In A. Charmantier, D. Garant, and L. E. B. Kruuk, eds. Quantitative genetics in the wild. Oxford Univ. Press, Oxford, U.K. 104-127.
89. Wolf, J. B., and M. J. Wade . 2001. On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J. Evol. Biol. 14:347-356.
90. Wolf, J. B., E. D. Bodie III, and A. J. Moore . 1999. Interacting phenotypes and the evolutionary process II. Selection resulting from social interactions. Am. Nat. 153:254-266.
91. Wright, S. I., S. Kalisz, and T. Slotte . 2013. Evolutionary consequences of self-fertilization in plants. Proc. R. Soc. B 280:20130133.