What happens after inbreeding avoidance? Inbreeding by rejected relatives and the inclusive fitness benefit of inbreeding avoidance

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Duthie, A Bradley ^a   Reid, Jane M ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AVOIDANCE BEHAVIOR; BREED; COMPETITION; FAMILY; INBREEDING; INBREEDING DEPRESSION; MODEL; OUTBREEDING; POPULATION MODEL; PREDICTION; PROGENY; QUANTITATIVE STUDY; RELATIVE; ANIMAL; BIOLOGICAL MODEL; FAMILY RELATION; FEMALE; MALE; MATE CHOICE; PHYSIOLOGY; PROCEDURES; REPRODUCTION; SEXUAL BEHAVIOR;

ANIMALS; FAMILY RELATIONS; FEMALE; INBREEDING; MALE; MATING PREFERENCE, ANIMAL; MODELS, BIOLOGICAL; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL;

EID: 84947305892     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125140     Document Type: Article

References (77)

1. Goodwillie C, Kalisz S, Eckert CG. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol Syst. 2005;36:47-79. doi: 10.1146/annurev. ecolsys.36.091704.175539
2. Charlesworth D. Evolution of plant breeding systems. Curr Biol. 2006;16:R726-R735. doi: 10.1016/j. cub.2006.07.068 PMID: 16950099
3. Charlesworth D, Willis JH. The genetics of inbreeding depression. Nat Rev Genet. 2009;10:783-796. doi: 10.1038/nrg2664 PMID: 19834483
4. Pusey AE. Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol. 1987;2:295-299. doi: 10.1016/0169-5347 (87) 90081-4 PMID: 21227869
5. Szulkin M, Sheldon BC. Dispersal as a means of inbreeding avoidance in a wild bird population. Proc R Soc Lond B. 2008;275:703-711. doi: 10.1098/rspb.2007.0989
6. Saccheri I, Kuussaari M, Kankare M, Vikman P, Hanski IA. Inbreeding and extinction in a butterfly metapopulation. Nature. 1998;45:1996-1999.
7. Keller LF, Waller DM. Inbreeding effects in wild populations. Trends Ecol Evol. 2002;17:19-23. doi: 10.1016/S0169-5347 (02) 02489-8
8. Byers DL, Waller DM. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst. 1999;30:479-513. doi: 10.1146/annurev. ecolsys.30.1.479
9. Crnokrak P, Barrett SCH. Perspective: purging the genetic load: a review of the experimental evidence. Evolution. 2002;56:2347-2358. doi: 10.1111/j.0014-3820.2002.tb00160.x PMID: 12583575
10. Szulkin M, Stopher KV, Pemberton JM, Reid JM. Inbreeding avoidance, tolerance, or preference in animals? Trends Ecol Evol. 2013;28:205-211. doi: 10.1016/j.tree.2012.10.016 PMID: 23182684
11. Charlesworth B. The cost of sex in relation to mating system. J Theor Biol. 1980;84:655-671. doi: 10. 1016/S0022-5193 (80) 80026-9 PMID: 7431946
12. Lande R, Schemske DW. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution. 1985;39:24-40. doi: 10.2307/2408514
13. Lloyd D. Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci. 1992;153:370-380. doi: 10.1086/297041
14. Tsitrone A, Duperron S, David P. Delayed selfing as an optimal mating strategy in preferentially outcrossing species: theoretical analysis of the optimal age at first reproduction in relation to mate availability. Am Nat. 2003;162:318-331. doi: 10.1086/375542 PMID: 12970840
15. Porcher E, Lande R. The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. J Evol Biol. 2005;18:497-508. doi: 10.1111/j.1420-9101.2005.00905.x PMID: 15842479
16. Porcher E, Kelly JK, Cheptou PO, Eckert CG, Johnston MO, Kalisz S. The genetic consequences of fluctuating inbreeding depression and the evolution of plant selfing rates. J Evol Biol. 2009;22:708-717. doi: 10.1111/j.1420-9101.2009.01705.x PMID: 19228271
17. Fisher RA. Average excess and average effect of a gene substitution. Ann Eugen. 1941;11:53-63. doi: 10.1111/j.1469-1809.1941.tb02272.x
18. Schultz ST, Willis JH. Individual variation in inbreeding depression: the roles of inbreeding history and mutation. Genetics. 1995;141:1209-1223. PMID: 8582625
19. Crnokrak P, Roff DA. Inbreeding depression in the wild. Heredity. 1999;83:260-270. doi: 10.1038/sj. hdy.6885530 PMID: 10504423
20. Armbruster P, Reed DH. Inbreeding depression in benign and stressful environments. Heredity. 2005;95:235-242. doi: 10.1038/sj.hdy.6800721 PMID: 16077737
21. Blouin SF, Blouin M. Inbreeding avoidance behaviors. Trends Ecol Evol. 1988;3:230-233. doi: 10. 1016/0169-5347 (88) 90164-4 PMID: 21227237
22. Pusey A, Wolf M. Inbreeding avoidance in animals. Trends Ecol Evol. 1996;5347:298-301.
23. Tennenhouse EM. Inbreeding avoidance in male primates: a response to female mate choice? Ethology. 2014;120:111-119.
24. Parker GA. Sexual selection and sexual conflict. In: Blum MS, Blum NA, editors. Sexual selection and reproductive competition in insects. New York: Academic Press, Inc; 1979. p. 123-166.
25. Parker GA. Sexual conflict over mating and fertilization: an overview. Philos Trans R Soc Lond B Biol Sci. 2006;361:235-259. doi: 10.1098/rstb.2005.1785 PMID: 16612884
26. Waser PM, Austad SN, Keane B. When should animals tolerate inbreeding? Am Nat. 1986;128:529-537.
27. Kokko H, Ots I. When not to avoid inbreeding. Evolution. 2006;60:467-475. doi: 10.1554/05-613.1 PMID: 16637492
28. Puurtinen M. Mate choice for optimal (k) inbreeding. Evolution. 2011;65:1501-1505. doi: 10.1111/j. 1558-5646.2010.01217.x PMID: 21521199
29. Jamieson IG, Taylor SS, Tracy LN, Kokko H, Armstrong DP. Why some species of birds do not avoid inbreeding: insights from New Zealand robins and saddlebacks. Behav Ecol. 2009;20:575-584. doi: 10. 1093/beheco/arp034
30. Clutton-Brock T, Parker GA. Sexual coercion in animal societies. Anim Behav. 1995;49:1345-1365. doi: 10.1006/anbe.1995.0166
31. Ala-Honkola O, Uddström A, Pauli BD, Lindström K. Strong inbreeding depression in male mating behaviour in a poeciliid fish. J Evol Biol. 2009;22:1396-1406. doi: 10.1111/j.1420-9101.2009.01765.x PMID: 19486236
32. Kuriwada T, Kumano N, Shiromoto K, Haraguchi D. Inbreeding avoidance or tolerance? Comparison of mating behavior between mass-reared and wild strains of the sweet potato weevil. Behav Ecol Sociobiol. 2011;65:1483-1489. doi: 10.1007/s00265-011-1158-6
33. Kuriwada T, Kumano N, Shiromoto K, Haraguchi D. The effect of inbreeding on mating behaviour of West Indian sweet potato weevil Euscepes postfasciatus. Ethology. 2011;117:822-828. doi: 10.1111/j. 1439-0310.2011.01937.x
34. Tan CKW, Løvlie H, Pizzari T, Wigby S. No evidence for precopulatory inbreeding avoidance in Drosophila melanogaster. Anim Behav. 2012;83:1433-1441. doi: 10.1016/j.anbehav. 2012.03.015
35. Wright S. Coefficients of inbreeding and relationship. Am Nat. 1922;56:330-338. doi: 10.1086/279872
36. Lehmann L, Perrin N. Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am Nat. 2003;162:638-652. doi: 10.1086/378823 PMID: 14618541
37. Hamilton WD. Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst. 1972;3:193-232. doi: 10.1146/annurev. es.03.110172.001205
38. Michod RE, Anderson WW. Measures of genetic relationship and the concept of inclusive fitness. Am Nat. 1979;114:637-647. doi: 10.1086/283513
39. Morton NE, Crow JF, Muller HJ. An estimate of the mutational damage in man from data on consanguineous marriages. Proc Natl Acad Sci USA. 1956;42:855-863. doi: 10.1073/pnas.42.11.855 PMID: 16589958
40. Mills LS, Smouse PE. Demographic consequences of inbreeding in remnant populations. Am Nat. 1994;144:412-431. doi: 10.1086/285684
41. Ralls K, Ballou JD, Templeton A. Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv Biol. 1988;2:185-193. doi: 10.1111/j.1523-1739.1988.tb00169.x
42. Keane B, Creel SR, Waser PM. No evidence of inbreeding avoidance or inbreeding depression in a social carnivore. Behav Ecol. 1996;7:480-489. doi: 10.1093/beheco/7.4.480
43. Jennions MD, Hunt J, Graham R, Brooks R. No evidence for inbreeding avoidance through postcopulatory mechanisms in the black field cricket, Teleogryllus commodus. Evolution. 2004;58:2472-2477. doi: 10.1554/04-261 PMID: 15612290
44. Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HW, et al. Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc Lond B. 2005;272:497-503. doi: 10.1098/rspb.2004.2963
45. Schmoll T, Quellmalz A, Dietrich V, Winkel W, Epplen JT, Lubjuhn T. Genetic similarity between pair mates is not related to extrapair paternity in the socially monogamous coal tit. Anim Behav. 2005;69:1013-1022. doi: 10.1016/j.anbehav. 2004.08.010
46. Holand O, Askim KR, Roed KH, Weladji RB, Gjostein H, Nieminen M. No evidence of inbreeding avoidance in a polygynous ungulate: the reindeer (Rangifer tarandus). Biol Lett. 2007;3:36-39. doi: 10. 1098/rsbl.2006.0575 PMID: 17443960
47. Billing AM, Lee AM, Skjelseth S, Borg AA, Hale MC, Slate J, et al. Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population. Mol Ecol. 2012;21:1487-1499. doi: 10.1111/j.1365-294X.2012.05490.x PMID: 22335620
48. Cohen LB, Dearborn DC. Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav. 2004;68:1229-1236. doi: 10.1016/j.anbehav. 2003.12.021
49. Kleven O, Jacobsen F, Robertson RJ, Lifjeld JT. Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett. 2005;1:389-392. doi: 10.1098/rsbl.2005.0376 PMID: 17148214
50. Wang C, Lu X. Female ground tits prefer relatives as extra-pair partners: driven by kin-selection? Mol Ecol. 2011;20:2851-2863. doi: 10.1111/j.1365-294X.2011.05070.x PMID: 21438933
51. Olson LE, Blumstein DT, Pollinger JR, Wayne RK. No evidence of inbreeding avoidance despite demonstrated survival costs in a polygynous rodent. Mol Ecol. 2012;21:562-571. doi: 10.1111/j.1365-294X.2011.05389.x PMID: 22145620
52. Robinson SP, Kennington WJ, Simmons LW. Preference for related mates in the fruit fly, Drosophila melanogaster. Anim Behav. 2012;84:1169-1176. doi: 10.1016/j.anbehav. 2012.08.020
53. Chapman T, Arnqvist G, Bangham J, Rowe L. Sexual conflict. Trends Ecol Evol. 2003;18:41-47. doi: 10.1016/S0169-5347 (02) 00004-6
54. Grafen A. Optimization of inclusive fitness. J Theor Biol. 2006;238:541-563. doi: 10.1016/j.jtbi.2005. 06.009 PMID: 16046225
55. Ohtsuki H. Evolutionary dynamics of n-player games played by relatives. Philos Trans R Soc Lond B Biol Sci. 2014;369:20130359. doi: 10.1098/rstb.2013.0359 PMID: 24686931
56. Grafen A. The hawk-dove game played between relatives. Anim Behav. 1979;27:905-907. doi: 10. 1016/0003-3472 (79) 90028-9
57. Uyenoyama MK. Inbreeding and the cost of meiosis: the evolution of selfing in populations practicing biparental inbreeding. Evolution. 1986;40:388-404. doi: 10.2307/2408817
58. Nason JD, Ellstrand NC. Lifetime estimates of biparental inbreeding depression in the self-incompatible annual plant Raphanus sativus. Evolution. 1995;49:307-316. doi: 10.2307/2410341
59. Herlihy CR, Eckert CG. Experimental dissection of inbreeding and its adaptive significance in a flowering plant, Aquilegia canadensis (Ranunculaceae). Evolution. 2004;58:2693-2703. doi: 10.1554/04-439 PMID: 15696748
60. Hirao AS. Kinship between parents reduces offspring fitness in a natural population of Rhododendron brachycarpum. Ann Bot. 2010;105:637-646. doi: 10.1093/aob/mcq018 PMID: 20202970
61. Arnqvist G, Rowe L. Sexual Conflict. Princeton, New Jersey: Princeton University Press; 2005.
62. Emlen ST. An evolutionary theory of the family. Proc Natl Acad Sci USA. 1995;92:8092-8099. doi: 10.1073/pnas.92.18.8092 PMID: 7667250
63. Sharp SP, Simeoni M, Hatchwell BJ. Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird. Proc R Soc Lond B. 2008;275:2125-2130. doi: 10.1098/rspb.2008. 0398
64. Hinde CA, Johnstone RA, Kilner RM. Parent-offspring conflict and coadaptation. Science. 2010;327:1373-1376. doi: 10.1126/science.1186056 PMID: 20223985
65. Stucki D, Mathias K. Coevolutionary feedbacks between family interactions and life history. Evolution. 2013;67:3208-3220. doi: 10.1111/evo.12187 PMID: 24152003
66. Haig D. Asymmetric relations: Internal conflicts and the horror of incest. Evol Hum Behav. 1999;98:83-98. doi: 10.1016/S1090-5138 (98) 00042-7
67. Welbergen JA, Quader S. Mother guarding: how offspring may influence the extra-pair behaviour of their parents. Proc R Soc Lond B. 2006;273:2363-2368. doi: 10.1098/rspb.2006.3591
68. Parker GA, Partridge L. Sexual conflict and speciation. Philos Trans R Soc Lond B Biol Sci. 1998;353:261-274. doi: 10.1098/rstb.1998.0208 PMID: 9533125
69. Maynard Smith J, Price GR. The logic of animal conflict. Nature. 1973;246:15-18. doi: 10.1038/246015a0
70. Maynard Smith J, Parker GA. The logic of asymmetric contests. Anim Behav. 1976;24:159-175. doi: 10.1016/S0003-3472 (76) 80110-8
71. Barrett SCH, Charlesworth D. Effects of a change in the level of inbreeding on genetic load. Nature. 1991;352:522-524. doi: 10.1038/352522a0 PMID: 1865906
72. Uyenoyama MK, Waller DM. Coevolution of self-fertilization and inbreeding depression. I. Mutation-selection balance at one and two loci. Theor Popul Biol. 1991;40:14-46. doi: 10.1016/0040-5809 (91) 90052-H PMID: 1948770
73. Escobar JS, Auld JR, Correa AC, Alonso JM, Bony YK, Coutellec MA, et al. Patterns of mating-system evolution in hermaphroditic animals: correlations among selfing rate, inbreeding depression, and the timing of reproduction. Evolution. 2011;65:1233-1253. doi: 10.1111/j.1558-5646.2011.01218.x PMID: 21521187
74. Uyenoyama MK, Waller DM. Coevolution of self-fertilization and inbreeding depression. III. Homozygous lethal mutations at multiple loci. Theor Ecol. 1991;40:173-210.
75. Glémin S. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution. 2003;57:2678-2687. doi: 10.1554/03-406 PMID: 14761049
76. Roze D, Blanckaert A. Epistasis, pleiotropy, and the mutation load in sexual and asexual populations. Evolution. 2014;68:137-49. doi: 10.1111/evo.12232 PMID: 24372600
77. Evans MR, Grimm V, Johst K, Knuuttila T, de Langhe R, Lessells CM, et al. Do simple models lead to generality in ecology? Trends Ecol Evol. 2013;28:578-583. doi: 10.1016/j.tree.2013.05.022 PMID: 23827437