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Extra-pair paternity and the variance in male fitness in song sparrows (Melospiza melodia).

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Lebigre, Christophe [UCL] Arcese, Peter [Centre for applied conservation research, forest sciences centre, university of British Columbia] Sardell, Rebecca J. [Institute of biological and environmental sciences, school of biological sciences, university of Aberdeen] Keller, Lukas F. [Institute of evolutionary biology and environmental studies, university of Zurich] Reid, Jane M. [Institute of biological and environmental sciences, school of biological sciences, university of Aberdeen]

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra-pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males' apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free-living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within-pair reproductive success (WPRS) and extra-pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0-27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males' contributions to future generations, its impact on population-level parameters such as the opportunity for selection and effective population size was limited.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2012
Language Anglais
Journal information "Evolution : international journal of organic evolution" - Vol. 66, no.10, p. 3111-3129 (2012)
Peer reviewed yes
Publisher Wiley-Blackwell Publishing Ltd. ((United Kingdom) Oxford)
issn 0014-3820
e-issn 1558-5646
Publication status Publié
Affiliation UCL - SST/ELI/ELIB - Biodiversity
Keywords Animals ; Female ; Genetic ; Fitness ; Male Reproduction ; Selection ; 3123
Links
  1. Akçay, Evol. Ecol. Res., 9, 855 (2007)
  2. Albrecht T., Schnitzer J., Kreisinger J., Exnerova A., Bryja J., Munclinger P., Extrapair paternity and the opportunity for sexual selection in long-distant migratory passerines, 10.1093/beheco/arm001
  3. ALBRECHT T., VINKLER M., SCHNITZER J., POLÁKOVÁ R., MUNCLINGER P., BRYJA J., Extra-pair fertilizations contribute to selection on secondary male ornamentation in a socially monogamous passerine, 10.1111/j.1420-9101.2009.01815.x
  4. Arcese Peter, Intrasexual competition, mating system and natal dispersal in song sparrows, 10.1016/s0003-3472(89)80137-x
  5. Arcese Peter, Smith James N. M., Hochachka Wesley M., Rogers Christopher M., Ludwig Donald, Stability, Regulation, and the Determination of Abundance in an Insular Song Sparrow Population, 10.2307/1940159
  6. Arnold Stevan J., Wade Michael J., On the Measurement of Natural and Sexual Selection: Theory, 10.2307/2408383
  7. Balenger Susan L., Scott Johnson L., Mays Jr Herman L., Masters Brian S., Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection, 10.1111/j.1600-048x.2009.04521.x
  8. Brommer Jon E., Merilä Juha, Kokko Hanna, Reproductive timing and individual fitness : Reproductive timing and fitness, 10.1046/j.1461-0248.2002.00369.x
  9. Byers Bruce E., Mays Herman L., Stewart Ian R. K., Westneat David F., EXTRAPAIR PATERNITY INCREASES VARIABILITY IN MALE REPRODUCTIVE SUCCESS IN THE CHESTNUT-SIDED WARBLER (DENDROICA PENSYLVANICA), A SOCIALLY MONOGAMOUS SONGBIRD, 10.1642/0004-8038(2004)121[0788:epivim]2.0.co;2
  10. Cornwallis Charlie K., West Stuart A., Davis Katie E., Griffin Ashleigh S., Promiscuity and the evolutionary transition to complex societies, 10.1038/nature09335
  11. Clutton-Brock, Reproductive success (1988)
  12. Cornell S. J, Tregenza T., A new theory for the evolution of polyandry as a means of inbreeding avoidance, 10.1098/rspb.2007.0926
  13. Crow, Hum. Biol., 30, 1 (1958)
  14. Dolan A. C., Murphy M. T., Redmond L. J., Sexton K., Duffield D., Extrapair paternity and the opportunity for sexual selection in a socially monogamous passerine, 10.1093/beheco/arm068
  15. Downhower Jerry F., Blumer Lawrence S., Brown Luther, Opportunity for Selection: An Appropriate Measure for Evaluating Variation in the Potential for Selection?, 10.2307/2409103
  16. DuVal E. H, Kempenaers B., Sexual selection in a lekking bird: the relative opportunity for selection by female choice and male competition, 10.1098/rspb.2008.0151
  17. Freeman-Gallant, Evolution, 59, 422 (2005)
  18. Griffith Simon C., Owens Ian P. F., Thuman Katherine A., Extra pair paternity in birds: a review of interspecific variation and adaptive function : EXTRA PAIR PATERNITY IN BIRDS, 10.1046/j.1365-294x.2002.01613.x
  19. Gustafsson Lars, Sutherland William J., The costs of reproduction in the collared flycatcher Ficedula albicollis, 10.1038/335813a0
  20. Hasselquist D., Social mating systems and extrapair fertilizations in passerine birds, 10.1093/beheco/12.4.457
  21. Hill Christopher E., Akçay Çağlar, Campbell S. Elizabeth, Beecher Michael D., Extrapair paternity, song, and genetic quality in song sparrows, 10.1093/beheco/arq171
  22. Hochachka, Conservation and biology of small populations-the song sparrow of Mandarte island, 155 (2006)
  23. Hochachka, Lifetime reproduction in birds, 135 (1989)
  24. JENNIONS MICHAEL D., PETRIE MARION, Why do females mate multiply? A review of the genetic benefits, 10.1017/s0006323199005423
  25. Johnsen Arild, Lifjeld Jan, Amundsen Trond, Andersson Staffan, Örnborg Jonas, MALE CHARACTERISTICS AND FERTILISATION SUCCESS IN BLUETHROATS, 10.1163/156853901317367645
  26. Jones A. G., Walker D., Kvarnemo C., Lindstrom K., Avise J. C., How cuckoldry can decrease the opportunity for sexual selection: Data and theory from a genetic parentage analysis of the sand goby, Pomatoschistus minutus, 10.1073/pnas.171310198
  27. Keller Lukas F., Inbreeding and Its Fitness Effects in an Insular Population of Song Sparrows (Melospiza melodia), 10.2307/2410939
  28. Keller L. F., Jeffery K. J., Arcese P., Beaumont M. A., Hochachka W. M., Smith J. N. M., Bruford M. W., Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers, 10.1098/rspb.2001.1607
  29. Keller L.F, Reid J.M, Arcese P, Testing evolutionary models of senescence in a natural population: age and inbreeding effects on fitness components in song sparrows, 10.1098/rspb.2007.0961
  30. Kempenaers Bart, Mate Choice and Genetic Quality: A Review of the Heterozygosity Theory, Advances in the Study of Behavior (2007) ISBN:9780120045372 p.189-278, 10.1016/s0065-3454(07)37005-8
  31. Kempenaers Bart, Verheyen Geert R., den Broeck Marleen Van, Burke Terry, Broeckhoven Christine Van, Dhondt André, Extra-pair paternity results from female preference for high-quality males in the blue tit, 10.1038/357494a0
  32. Ketterson, Ornithol. Monogr., 49, 81 (1997)
  33. Kingsolver J. G., Hoekstra H. E., Hoekstra J. M., Berrigan D., Vignieri S. N., Hill C. E., Hoang A., Gibert P., Beerli P., The Strength of Phenotypic Selection in Natural Populations, 10.1086/319193
  34. Kleven Oddmund, Jacobsen Frode, Izadnegahdar Rasa, Robertson Raleigh J., Lifjeld Jan T., Male tail streamer length predicts fertilization success in the North American barn swallow (Hirundo rustica erythrogaster), 10.1007/s00265-005-0065-0
  35. Kokko Hanna, Mackenzie Aulay, Reynolds John D., Lindström Jan, Sutherland William J., Measures of Inequality Are Not Equal, 10.1086/303235
  36. McGraw James B., Caswell Hal, Estimation of Individual Fitness from Life-History Data, 10.1086/285839
  37. Moller A. P., Birkhead T. R., The Evolution of Plumage Brightness in Birds is Related to Extrapair Paternity, 10.2307/2410369
  38. Møller Anders Pape, Ninni Paola, Sperm competition and sexual selection: a meta-analysis of paternity studies of birds, 10.1007/s002650050501
  39. Morisita Masaaki, I σ-Index, a measure of dispersion of individuals, 10.1007/bf02533903
  40. Newton, Lifetime reproduction in birds (1989)
  41. Nunney Leonard, The Influence of Mating System and Overlapping Generations on Effective Population Size, 10.2307/2410151
  42. Nunney Leonard, Elam Diane R., Estimating the Effective Population Size of Conserved Populations, 10.1046/j.1523-1739.1994.08010175.x
  43. D. O'Connor Kathleen, B. Marr Amy, Arcese Peter, F. Keller Lukas, J. Jeffery Kathryn, W. Bruford Michael, Extra-pair fertilization and effective population size in the song sparrow Melospiza melodia, 10.1111/j.2006.0908-8857.03681.x
  44. Otter Ken, Ratcliffe Laurene, Michaud Denise, Boag Peter T., Do female black-capped chickadees prefer high-ranking males as extra-pair partners?, 10.1007/s002650050463
  45. Owens I. P. F., Hartley I. R., Sexual dimorphism in birds: why are there so many different forms of dimorphism?, 10.1098/rspb.1998.0308
  46. Postma E., Heinrich F., Koller U., Sardell R. J., Reid J. M., Arcese P., Keller L. F., Disentangling the effect of genes, the environment and chance on sex ratio variation in a wild bird population, 10.1098/rspb.2010.2763
  47. R Development Core Team, R: a language and environment for statistical computing (2009)
  48. Reid Jane M., Keller Lukas F., CORRELATED INBREEDING AMONG RELATIVES: OCCURRENCE, MAGNITUDE, AND IMPLICATIONS : CORRELATED INBREEDING AMONG RELATIVES, 10.1111/j.1558-5646.2009.00865.x
  49. Reid Jane M., Arcese Peter, Cassidy Alice L.E.V., Hiebert Sara M., Smith James N.M., Stoddard Philip K., Marr Amy B., Keller Lukas F., Song repertoire size predicts initial mating success in male song sparrows, Melospiza melodia, 10.1016/j.anbehav.2004.07.003
  50. Reid Jane M., Arcese Peter, Cassidy Alice L. E. V., Hiebert Sara M., Smith James N. M., Stoddard Philip K., Marr Amy B., Keller Lukas F., Fitness Correlates of Song Repertoire Size in Free‐Living Song Sparrows (Melospiza melodia), 10.1086/428299
  51. Reid Jane M., Arcese Peter, Sardell Rebecca J., Keller Lukas F., Additive Genetic Variance, Heritability, and Inbreeding Depression in Male Extra-Pair Reproductive Success, 10.1086/657977
  52. Reid J. M., Sardell R. J., Indirect selection on female extra-pair reproduction? Comparing the additive genetic value of maternal half-sib extra-pair and within-pair offspring, 10.1098/rspb.2011.2230
  53. Richardson D. S., Burke T., Extra-pair paternity in relation to male age in Bullock's orioles, 10.1046/j.1365-294x.1999.00832.x
  54. Richardson David S., Burke Terry, Extrapair paternity and variance in reproductive success related to breeding density in Bullock's orioles, 10.1006/anbe.2001.1778
  55. SARDELL REBECCA J., KELLER LUKAS F., ARCESE PETER, BUCHER THOMAS, REID JANE M., Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows, Melospiza Melodia : EXTRA-PAIR PATERNITY, LOCATION AND STATUS, 10.1111/j.1365-294x.2010.04805.x
  56. Sardell R. J., Arcese P., Keller L. F., Reid J. M., Sex-specific differential survival of extra-pair and within-pair offspring in song sparrows, Melospiza melodia, 10.1098/rspb.2011.0173
  57. Schmoll Tim, Mund Verena, Dietrich-Bischoff Verena, Winkel Wolfgang, Lubjuhn Thomas, Male age predicts extrapair and total fertilization success in the socially monogamous coal tit, 10.1093/beheco/arm082
  58. SHELDON BEN C., ELLEGREN HANS, Sexual selection resulting from extrapair paternity in collared flycatchers, 10.1006/anbe.1998.0968
  59. Shuster S. M., Sexual selection and mating systems, 10.1073/pnas.0901132106
  60. Shuster, Mating systems and strategies (2003)
  61. Smith James N. M., Does High Fecundity Reduce Survival in Song Sparrows?, 10.2307/2408128
  62. Arcese Peter, How Fit are Floaters? Consequences of Alternative Territorial Behaviors in a Nonmigratory Sparrow, 10.1086/284955
  63. Smith, Conservation and biology of small populations- the song sparrow of Mandarte island (2006)
  64. Stearns, The evolution of life histories (1992)
  65. Stutchbury Bridget J. M., Piper W. H., Neudorf D. L., Tarof S. A., Rhymer Judith M., Fuller G., Fleischer R. C., Correlates of extra-pair fertilization success in hooded warblers, 10.1007/s002650050324
  66. Tsuji Kazuki, Tsuji Nobuyuki, Indices of reproductive skew depend on average reproductive success, 10.1023/a:1006575411224
  67. Waples R. S., Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species, 10.1093/jhered/89.5.438
  68. Weatherhead, Ecology, 78, 884 (1997)
  69. Webster M. S., Microsatellite identification of extrapair sires in a socially monogamous warbler, 10.1093/beheco/12.4.439
  70. Webster Michael S., Pruett-Jones Stephen, Westneat David F., Arnold Stevan J., Measuring the Effects of Pairing Success, Extra-Pair Copulations and Mate Quality on the Opportunity for Sexual Selection, 10.2307/2410439
  71. Webster Michael S., Tarvin Keith A., Tuttle Elaina M., Pruett-Jones Stephen, PROMISCUITY DRIVES SEXUAL SELECTION IN A SOCIALLY MONOGAMOUS BIRD, 10.1111/j.1558-5646.2007.00208.x
  72. Westneat David F., Stewart Ian R.K., Extra-Pair Paternity in Birds: Causes, Correlates, and Conflict, 10.1146/annurev.ecolsys.34.011802.132439
  73. Whittingham L. A., Effects of extra-pair and within-pair reproductive success on the opportunity for selection in birds, 10.1093/beheco/arh140
  74. Whittingham L. A., Lifjeld J. T., High paternal investment in unrelated young: extra-pair paternity and male parental care in house martins, 10.1007/bf00164155
  75. Wilson Amy G., Arcese Peter, Influential factors for natal dispersal in an avian island metapopulation, 10.1111/j.0908-8857.2008.04239.x
  76. Wolf J. B., Wade M. J., On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? : Whose fitness is it?, 10.1046/j.1420-9101.2001.00277.x
  77. Wright, Genetics, 16, 97 (1931)
  78. Yezerinac Stephen M., Weatherhead Patrick J., Boag Peter T., Extra-pair paternity and the opportunity for sexual selection in a socially monogamous bird (Dendroica petechia), 10.1007/bf00176715
Bibliographic reference Lebigre, Christophe ; Arcese, Peter ; Sardell, Rebecca J. ; Keller, Lukas F. ; Reid, Jane M.. Extra-pair paternity and the variance in male fitness in song sparrows (Melospiza melodia).. In: Evolution : international journal of organic evolution, Vol. 66, no.10, p. 3111-3129 (2012)
Permanent URL http://hdl.handle.net/2078.1/138942