Promiscuous mating produces offspring with higher lifetime fitness

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1730, 2012, Pages 860-866

  Gerlach, Nicole M ^a   McGlothlin, Joel W ^b   Parker, Patricia G ^c   Ketterson, Ellen D ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF MISSOURI ST LOUIS   (United States)

Author keywords

Extra pair mating; Indirect fitness benefits; Lifetime reproductive success; Multiple mating; Sexual selection

Indexed keywords

BROOD REARING; EXTRA-PAIR COPULATION; HYPOTHESIS TESTING; INCLUSIVE FITNESS; LIFE HISTORY TRAIT; MATING SUCCESS; MULTIPLE MATING; REPRODUCTIVE PRODUCTIVITY; SEXUAL SELECTION; SONGBIRD; SURVIVAL;

JUNCO HYEMALIS; PASSERI;

EID: 84856250249     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1547     Document Type: Article

References (57)

1. Birkhead, T. R. & Møller, A. P. 1998 Sperm competition and sexual selection., London, UK: Academic Press.
2. Bateman, A. J. 1948 Intra-sexual selection in Drosophila, Heredity, 2, 349-368. (doi:10.1038/hdy.1948.21)
3. Arnqvist, G. & Nilsson, T. 2000 The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav., 60, 145-164. (doi:10.1006/anbe.2000.1446)
4. Andersson, M. 1994 Sexual selection., Princeton, NJ: Princeton University Press.
5. Iwasa, Y. & Pomiankowski, A. 1991 The evolution of costly mate preferences. II. The handicap principle. Evolution, 45, 1431-1442. (doi:10.2307/2409890)
6. Colegrave, N., Kotiaho, J. S. & Tomkins, J. L. 2002 Mate choice or polyandry: reconciling genetic compatibility and good genes sexual selection. Evol. Ecol. Res., 4, 911-917.
7. Mays Jr, H. L. & Hill, G. E. 2004 Choosing mates: good genes versus genes that are a good fit. Trends Ecol. Evol., 19, 554-559. (doi:10.1016/j.tree.2004.07.018)
8. Pryke, S. R., Rollins, L. A. & Griffith, S. C. 2010 Females use multiple mating and genetically loaded sperm competition to target compatible genes. Science, 329, 964-967. (doi:10.1126/science.1192407)
9. Jennions, M. D. & Petrie, M. 2000 Why do females mate multiply? A review of the genetic benefits. Biol. Rev., 75, 21-64. (doi:10.1017/S0006323199005423)
10. Griffith, S. C., Owens, I. P. F. & Thuman, K. 2002 Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol., 11, 2195-2212. (doi:10.1046/j.1365-294X.2002.01613.x)
11. Drevon, T. & Slagsvold, T. 2005 When and from whom do female pied flycatchers (Ficedula hypoleuca) solicit copulations. Behaviour, 142, 1059-1076. (doi:10.1163/ 156853905774405335)
12. Double, M. C. & Cockburn, A. 2000 Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens. Proc. R. Soc. Lond. B, 267, 465-470. (doi:10.1098/rspb.2000.1023)
13. Westneat, D. F., Sherman, P. W. & Morton, M. L. 1990 The ecology and evolution of extra-pair copulations in birds. Curr. Ornithol., 7, 331-369.
14. Westneat, D. F. & Stewart, I. 2003 Extra-pair paternity in birds: causes, correlates and conflict. Annu. Rev. Ecol. Evol. Syst., 34, 365-396. (doi:10.1146/annurev. ecolsys.34.011802.132439)
15. Akçay, E. & Roughgarden, J. 2007 Extra-pair paternity in birds: review of the genetic benefits. Evol. Ecol. Res., 9, 855-868.
16. Schmoll, T., Dietrich-Bischoff, V., Winkel, W., Epplen, J. T. & Lubjuhn, T. 2003 Long-term fitness consequences of female extra-pair matings in a socially monogamous passerine. Proc. R. Soc. Lond. B, 270, 259-264. (doi:10.1098/rspb.2002.2216)
17. Schmoll, T., Dietrich-Bischoff, V., Winkel, W., Epplen, J. T., Schurr, F. & Lubjuhn, T. 2005 Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine. Evolution, 59, 645-657.
18. Schmoll, T., Schurr, F. M., Winkel, W., Epplen, J. T. & Lubjuhn, T. 2009 Lifespan, lifetime reproductive performance and paternity loss of within-pair and extrapair offspring in the coal tit Periparus ater, Proc. R. Soc. B, 276, 337-345. (doi:10.1098/rspb.2008.1116)
19. Hunt, J., Bussiere, L. F., Jennions, M. D. & Brooks, R. 2004 What is genetic quality? Trends Ecol. Evol., 19, 329-333. (doi:10.1016/j.tree.2004.03.035)
20. Arnqvist, G. & Kirkpatrick, M. 2005 The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am. Nat., 165, S26-S37. (doi:10. 1086/429350)
21. Ketterson, E. D., Parker, P. G., Raouf, S. A., Nolan Jr, V., Ziegenfus, C. & Chandler, C. R. 1997 The relative impact of extra-pair fertilizations on variation in male and female reproductive success in dark-eyed juncos (Junco hyemalis). Ornithol. Monogr., 49, 81-101.
22. Fisher, R. A. 1930 The genetical theory of natural selection., Oxford, UK: Clarendon Press.
23. Lande, R. 1981 Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA, 78, 3721-3725. (doi:10.1073/pnas.78.6.3721)
24. Kokko, H., Brooks, R., McNamara, J. & Houston, A. 2002 The sexual selection continuum. Proc. R. Soc. Lond. B, 269, 1331-1340. (doi:10.1098/rspb.2002.2020)
25. Chandler, C. R., Ketterson, E. D., Nolan Jr, V. & Ziegenfus, C. 1994 Effects of testosterone on spatial activity in free-ranging male dark-eyed juncos, Junco hyemalis, Anim. Behav., 47, 1445-1455. (doi:10.1006/ anbe.1994.1191)
26. Reed, W., Clark, M., Parker, P. G., Raouf, S. A., Arguedas, N., Monk, D., Snajdr, E. A., Nolan Jr, V. & Ketterson, E. D. 2006 Physiological effects on demography: a long-term experimental study of testosterone's effects on fitness. Am. Nat., 167, 667-683. (doi:10. 1086/503054)
27. Raouf, S. A., Parker, P. G., Ketterson, E. D., Nolan Jr, V. & Ziegenfus, C. 1997 Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis). Proc. R. Soc. Lond. B, 264, 1599-1603. (doi:10.1098/rspb.1997. 0223)
28. Marshall, T., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. 1998 Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol., 7, 639-655. (doi:10.1046/j.1365-294x.1998.00374.x)
29. Kalinowski, S., Taper, M. L. & Marshall, T. 2007 Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol., 16, 1099-1106. (doi:10.1111/j. 1365-294X.2007.03089.x)
30. O'Neal, D. M., Reichard, D. G., Pavilis, K. & Ketterson, E. D. 2008 Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the dark-eyed junco (Junco hyemalis). Horm. Behav., 54, 571-578. (doi:10.1016/j.yhbeh.2008.05.017)
31. Clotfelter, E. D., O'Neal, D. M., Gaudioso, J. M., Casto, J. M., Parker-Renga, I. M., Snajdr, E. A., Duffy, D. L., Nolan Jr, V. & Ketterson, E. D. 2004 Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Horm. Behav., 46, 171-178. (doi:10.1016/j. yhbeh.2004.03.003)
32. Gilmour, A. R., Gogel, B. J., Cullis, B. R. & Thompson, R. 2009 ASREML user guide release 3.0., Hemel Hempstead, UK: VSN International Ltd.
33. Engqvist, L. 2005 The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav., 70, 967-971. (doi:10.1016/j.anbehav.2005.01.016)
34. Whittingham, L. A., Taylor, P. D. & Robertson, R. J. 1992 Confidence of paternity and male parental care. Am. Nat., 139, 1115-1125. (doi:10.1086/285376)
35. Owens, I. 1993 When kids just aren't worth it: cuckoldry and parental care. Trends Ecol. Evol., 8, 269-271. (doi:10.1016/0169-5347(93)90251-J)
36. Gerlach, N. M., McGlothlin, J. W., Parker, P. G. & Ketterson, E. D. Submitted. Interpreting positive Bateman gradients in female and male dark-eyed juncos.
37. Hettyey, A., Hegyi, G., Puurtinen, M., Hoi, H., Torok, J. & Penn, D. J. 2010 Mate choice for genetic benefits: time to put the pieces together. Ethology, 116, 1-9. (doi:10.1111/j. 1439-0310.2009.01704.x)
38. Neff, B. D. & Pitcher, T. 2005 Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol., 14, 19-38. (doi:10.1111/j. 1365-294X.2004.02395.x)
39. Magrath, M. J. L., Vedder, O., van der Velde, M. & Komdeur, J. 2009 Maternal effects contribute to the superior performance of extra-pair offspring. Curr. Biol., 19, 792-797. (doi:10.1016/j.cub.2009.03.068)
40. Ferree, E. D., Dickinson, J., Rendell, W., Stern, C. & Porter, S. 2010 Hatching order explains an extrapair chick advantage in western bluebirds. Behav. Ecol., 21, 802-807. (doi:10.1093/beheco/arq056)
41. Cordero, P. J., Wetton, J. H. & Parkin, D. T. 1999 Within-clutch patterns of egg viability and paternity in the house sparrow. J. Avian Biol., 30, 103-107. (doi:10. 2307/3677249)
42. Krist, M., Nadvornik, P., Uvirova, L. & Bures, S. 2005 Paternity covaries with laying and hatching order in the collared flycatcher Ficedula albicollis, Behav. Ecol. Sociobiol., 59, 6-11. (doi:10.1007/s00265-005-0002-2)
43. Nolan Jr, V., Ketterson, E. D., Cristol, D. A., Rogers, C. M., Clotfelter, E. D., Titus, R. C., Schoech, S. J. & Snajdr, E. 2002 Dark-eyed junco (Junco hyemalis). In The birds of North America, no. 716, (eds A. Poole & F. Gill). Philadelphia, PA: The Birds of North America, Inc.
44. Gowaty, P. 1996 Battles of the sexes and origins of monogamy. In Partnerships in birds: the study of monogamy, (ed. J. M. Black), pp. 21-52. Oxford, UK: Oxford University Press.
45. Bouwman, K. M. & Komdeur, J. 2005 Old female reed buntings (Emberiza schoeniclus) increase extra-pair paternity in their broods when mated to young males. Behaviour, 142, 1449-1463. (doi:10.1163/15685390 5774831819)
46. Grant, P. R. & Grant, B. R. 2011 Causes of lifetime fitness of Darwin's finches in a fluctuating environment. Proc. Natl Acad. Sci. USA, 108, 674-679. (doi:10.1073/ pnas.1018080108)
47. Burke, T., Davies, N. B., Bruford, M. W. & Hatchwell, B. J. 1989 Parental care and mating behaviour of polyandrous dunnocks Prunella modularis, related to paternity, by DNA fingerprinting. Nature, 338, 249-251. (doi:10. 1038/338249a0)
48. Westneat, D. F., Clark, A. B. & Rambo, K. C. 1995 Within brood patterns of paternity and paternal behavior in red-winged blackbirds. Behav. Ecol. Sociobiol., 37, 349-356. (doi:10.1007/BF00174140)
49. Briskie, J. V., Montgomerie, R., Poldmaa, T. & Boag, P. T. 1998 Paternity and paternal care in the polygynandrous Smith's longspur. Behav. Ecol. Sociobiol., 43, 181-190. (doi:10.1007/s002650050479)
50. Peterson, K., Thusius, K., Whittingham, L. A. & Dunn, P. O. 2001 Allocation of male parental care in relation to paternity within and among broods of the common yellowthroat (Geothlypis trichas). Ethology, 107, 573-586. (doi:10.1046/j.1439-0310.2001.00676.x)
51. Bouwman, K. M., Lessells, C. K. M. & Komdeur, J. 2005 Male reed buntings do not adjust parental effort in relation to extrapair paternity. Behav. Ecol., 16, 499-506. (doi:10.1093/beheco/ari021)
52. McFarlane, S. E., Lane, J. E., Taylor, R. W., Gorrell, J. C., Coltman, D. W., Humphries, M. M., Boutin, S. & McAdam, A. G. 2010 The heritability of multiple male mating in a promiscuous mammal. Biol. Lett., 7, 368-371. (doi:10.1098/rsbl.2010.1003)
53. Reid, J. M., Arcese, P., Sardell, R. J. & Keller, L. F. 2011 Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia). Proc. R. Soc. B, 278, 1114-1120. (doi:10.1098/rspb.2010.1704)
54. Weatherhead, P. J. & Robertson, R. J. 1979 Offspring quality and the polygyny threshold: 'the sexy son hypothesis'. Am. Nat., 113, 201-208. (doi:10.1086/283379)
55. Kokko, H., Jennions, M. D. & Brooks, R. 2006 Unifying and testing models of sexual selection. Annu. Rev. Ecol. Evol. Syst., 37, 43-66. (doi:10.1146/annurev.ecolsys.37.091305.110259)
56. Forstmeier, W., Martin, K., Bolund, E., Schielzeth, H. & Kempenaers, B. 2011 Female extrapair mating behavior can evolve via indirect selection on males. Proc. Natl Acad. Sci. USA, 108, 10 608-10 613. (doi:10.1073/ pnas.1103195108)
57. Gerlach, N. M., McGlothlin, J. W., Parker, P. G. & Ketterson, E. D. In preparation. Dark-eyed junco extrapair offspring are not of higher quality than within-pair offspring in their first year of life.