Phenotype-associated inbreeding biases estimates of inbreeding depression in a wild bird population

Journal of Evolutionary Biology

Volumn 29, Issue 1, 2016, Pages 35-46

  Becker, P J J ^a   Hegelbach, J ^a   Keller, L F ^a   Postma, E ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Animal model; Heritability; Inbreeding; Phenotype dependent dispersal; White throated dipper

Indexed keywords

BIRD; DISPERSAL; HERITABILITY; INBREEDING; PHENOTYPE; POPULATION GENETICS;

ANIMALIA; AVES; CINCLUS CINCLUS;

ANATOMY AND HISTOLOGY; ANIMAL; BIOLOGICAL MODEL; FEMALE; GENETICS; INBREEDING; MALE; PASSERIFORMES; PHENOTYPE; PHYSIOLOGY; POPULATION GENETICS; SWITZERLAND; WING;

ANIMALS; FEMALE; GENETICS, POPULATION; INBREEDING; MALE; MODELS, GENETIC; PASSERIFORMES; PHENOTYPE; SWITZERLAND; WINGS, ANIMAL;

EID: 84953365795     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12759     Document Type: Article

References (63)

1. Alatalo, R.V., Gustafsson, L. & Lundberg, A. 1984. Why do young passerine birds have shorter wings than older birds. The Ibis 126: 410-415.
2. Balloux, F., Amos, W. & Coulson, T. 2004. Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 13: 3021-3031.
3. Bérénos, C., Ellis, P.A., Pilkington, J.G. & Pemberton, J.M. 2014. Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches. Mol. Ecol. 23: 3434-3451.
4. Chaput-Bardy, A., Gregoire, A., Baguette, M., Pagano, A. & Secondi, J. 2010. Condition and phenotype-dependent dispersal in a Damselfly, Calopteryx splendens. PLoS ONE 5: e10694.
5. Charlesworth, D. & Charlesworth, B. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18: 237-268.
6. Cheptou, P.O. & Donohue, K. 2011. Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol. 189: 395-407.
7. Cote, J., Fogarty, S., Brodin, T., Weinersmith, K. & Sih, A. 2011. Personality-dependent dispersal in the invasive mosquitofish: group composition matters. Proc. R. Soc. B 278: 1670-1678.
8. Crow, J.F. & Kimura, M. 1970. An Introduction to Population Genetics Theory. The Blackburn Press, Caldwell, New Jersey.
9. Curik, I., Solkner, J. & Stipic, N. 2001. The influence of selection and epistasis on inbreeding depression estimates. J. Anim. Breed. Genet. 118: 247-262.
10. Darwin, C. 1876. The Effects of Cross and Self-Fertilisation in the Vegetable Kingdom. John Murray, London.
11. Dawideit, B.A., Phillimore, A.B., Laube, I., Leisler, B. & Böhning-Gaese, K. 2009. Ecomorphological predictors of natal dispersal distances in birds. J. Anim. Ecol. 78: 388-395.
12. De Boer, I.J.M. & Van Arendonk, J.A.M. 1992. Prediction of additive and dominance effects in selected or unselected populations with inbreeding. Theor. Appl. Genet. 84: 451-459.
13. DeRose, M.A. & Roff, D.A. 1999. A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53: 1288-1292.
14. Duarte, L.C., Bouteiller, C., Fontanillas, P., Petit, E. & Perrin, N. 2003. Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57: 638-645.
15. Edelaar, P. & Bolnick, D.I. 2012. Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol. Evol. 27: 659-665.
16. Falconer, D. & Mackay, T. 1996. Introduction to Quantitative Genetics. Longman, Harlow.
17. Friedenberg, N.A. 2003. Experimental evolution of dispersal in spatiotemporally variable microcosms. Ecol. Lett. 6: 953-959.
18. Gienapp, P., Postma, E. & Visser, M.E. 2006. Why breeding time has not responded to selection for earlier breeding in a songbird population. Evolution 60: 2381-2388.
19. Gilmour, A.R., Gogel, B.J., Cullis, B.R. & Thompson, R. 2009. ASReml User Guide Release 3.0. VSN Int. Ltd., Hemel Hempstead, UK.
20. Griffiths, R., Double, M.C., Orr, K. & Dawson, R.J. 1998. A DNA test to sex most birds. Mol. Ecol. 7: 1071-1075.
21. Hegelbach, J. 2013. Temperaturabhänigiger Brutbeginn, Pflanzenphänologie und Zweitbrutanteil bei der Wasseramsel Cinclus cinclus. Der Ornithologische Beobachter 110: 453-464.
22. Hemmings, N.L., Slate, J. & Birkhead, T.R. 2012. Inbreeding causes early death in a passerine bird. Nat. Comm. 3: 863.
23. Henderson, C.R. 1950. Estimation of genetic parameters. Ann. Math. Stats. 21: 309-310.
24. Hoeck, P., Bucher, T., Wandeler, P. & Keller, L. 2009. Microsatellite primers for the four Galápagos mockingbird species (Mimus parvulus, Mimus macdonaldi, Mimus melanotis and Mimus trifasciatus). Mol. Ecol. Resour. 9: 1538-1541.
25. Hoeschele, I. & Van Raden, P.M. 1991. Rapid inversion of dominance relationship matrices for noninbred populations by including sire by dam subclass effects. J. Dairy Sci. 74: 557-569.
26. Innocent, T.M., Abe, J., West, S.A. & Reece, S.E. 2010. Competition between relatives and the evolution of dispersal in a parasitoid wasp. J. Evol. Biol. 23: 1374-1385.
27. Keller, L.F. 1998. Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52: 240-250.
28. Keller, L.F. & Waller, D.M. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17: 230-241.
29. Keller, L.F., Grant, P.R., Grant, B.R. & Petren, K. 2002. Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin's finches. Evolution 56: 1229-1239.
30. Keller, L.F., Marr, A.B. & Reid, J.M. 2006. The genetic consequences of small population size: inbreeding and loss of genetic variation. In: Conservation and Biology of Small Populations: the Song Sparrows of Mandarte Island (J.N.M. Smith, L.F. Keller, A.B. Marr & P. Arcese, eds), pp. 113-137. Oxford University Press, New York.
31. Kruuk, L.E.B. 2004. Estimating genetic parameters in natural populations using the 'animal model'. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359: 873-890.
32. Kruuk, L.E.B., Sheldon, B.C. & Merila, J. 2002. Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc. R. Soc. B 269: 1581-1589.
33. Lande, R. 1988. Genetics and demography in biological conservation. Science 241: 1455-1460.
34. Lenormand, T. 2002. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17: 183-189.
35. Lynch, M. & Walsh, B. 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Inc. Publishers, Sunderland, Massachusetts, USA.
36. Malécot, G.M. 1948. Les Mathématiques de l'hérédité. Masson et Cie.
37. Marr, A.B., Arcese, P., Hochachka, W.M., Reid, J.M. & Keller, L.F. 2006. Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. J. Anim. Ecol. 75: 1406-1415.
38. Mousseau, T.A. & Roff, D.A. 1987. Natural selection and the heritability of fitness components. Heredity 59: 181-197.
39. Newman, D. & Pilson, D. 1997. Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51: 354-362.
40. Nieminen, M., Singer, M.C., Fortelius, W., Schops, K. & Hanski, I. 2001. Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. Am. Nat. 157: 237-244.
41. Øigarden, T., Borge, T. & Lifjeld, J.T. 2010. Extrapair paternity and genetic diversity: the white-throated dipper Cinclus cinclus. J. Avian Biol. 41: 248-257.
42. Paradis, E., Baillie, S.R., Sutherland, W.J. & Gregory, R.D. 1998. Patterns of natal and breeding dispersal in birds. J. Anim. Ecol. 67: 518-536.
43. Postma, E. 2014. Four decades of estimating heritabilities in wild vertebrate populations: improved methods, more data, better estimates? In: Quantitative Genetics in the Wild (A. Charmantier, D. Garant & L.E.B. Kruuk, eds), pp. 16-33. Oxford University Press, Oxford, United Kingdom.
44. Postma, E. & Van Noordwijk, A.J. 2005. Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature 433: 65-68.
45. Postma, E., Martini, L. & Martini, P. 2010. Inbred women in a small and isolated Swiss village have fewer children. J. Evol. Biol. 23: 1468-1474.
46. R Development Core Team 2013. R: A Language and Environment for Statistical Computing Vers. 3.0.2, R Foundation for Statistical Computing, Vienna.
47. Räsänen, K. & Hendry, A.P. 2008. Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecol. Lett. 11: 624-636.
48. Reid, J.M., Arcese, P. & Keller, L.F. 2006. Intrinsic parent-offspring correlation in inbreeding level in a song sparrow (Melospiza melodia) population open to immigration. Am. Nat. 168: 1-13.
49. Reid, J.M., Arcese, P. & Keller, L.F. 2008. Individual phenotype, kinship, and the occurrence of inbreeding in song sparrows. Evolution 62: 887-899.
50. Richards, C.M. 2000. Inbreeding depression and genetic rescue in a plant metapopulation. Am. Nat. 155: 383-394.
51. Richardson, D.S., Komdeur, J. & Burke, T. 2004. Inbreeding in the seychelles warbler: environment-dependent maternal effects. Evolution 58: 2037-2048.
52. Ronce, O. & Clobert, J. 2012. Dispersal syndromes. In: Dispersal Ecology and Evolution (J. Clobert, M. Baguette, T.G. Benton & J.M. Bullock, eds), pp. 119-138. Oxford University Press, Oxford, United Kingdom.
53. Skjelseth, S., Ringsby, T.H., Tufto, J., Jensen, H. & Saether, B.E. 2007. Dispersal of introduced house sparrows Passer domesticus: an experiment. Proc. R. Soc. B 274: 1763-1771.
54. Slate, J., David, P., Dodds, K.G., Veenvliet, B.A., Glass, B.C., Broad, T.E. et al. 2004. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93: 255-265.
55. Szulkin, M. & Sheldon, B.C. 2008. Dispersal as a means of inbreeding avoidance in a wild bird population. Proc. R. Soc. B 275: 703-711.
56. Szulkin, M., Garant, D., McCleery, R.H. & Sheldon, B.C. 2007. Inbreeding depression along a life-history continuum in the great tit. J. Evol. Biol. 20: 1531-1543.
57. Thünken, T., Bakker, T.C.M., Baldauf, S.A. & Kullmann, H. 2007. Active inbreeding in a cichlid fish and its adaptive significance. Curr. Biol. 17: 225-229.
58. Uimari, P. & Kennedy, B.W. 1990. Mixed model methodology to estimate additive and dominance genetic values under complete dominance and inbreeding. Proc. 4th World Congr. Genet. Appl. Lifestock Prod. Vol. XIII, p. 297-300.
59. Van Noordwijk, A.J. & Scharloo, W. 1981. Inbreeding in an Island Population of the Great Tit. Evolution 35: 674-688.
60. Villanueva, B., Woolliams, J.A. & Gjerde, B. 1996. Optimum designs for breeding programmes under mass selection with an application in fish breeding. Anim. Sci. 63: 563-576.
61. Wilson, A.J., Réale, D., Clements, M.N., Morrissey, M.M., Postma, E., Walling, C.A. et al. 2010. An ecologist's guide to the animal model. J. Anim. Ecol. 79: 13-26.
62. Wolak, M.E. & Keller, L.F. 2014. Dominance genetic variance and inbreeding in natural populations. In: Quantitative Genetics in the Wild (A. Charmantier, D. Garant & L.E.B. Kruuk, eds), pp. 104-127. Oxford University Press, Oxford, United Kingdom.
63. Wright, S. 1922. Coefficients of inbreeding and relationship. Am. Nat. 56: 330-338.