Sperm competition and sexual selection: a meta-analysis of paternity studies of birds

Abstract Sperm competition (the competition among the sperm of different males for fertilization of the eggs of a female) has been suggested to be an important component of sexual selection, but no general assessment has been made of this proposition. We used a meta-analytic approach to assess the extensive literature on paternity (the proportion of offspring in a focal nest sired by an attending male) in birds based on allozyme and molecular techniques. The relative variance in male mating success was on average increased by a factor of 4.6 over the variance in apparent male success. Males with more extravagant secondary sexual characters had higher paternity in their own nests than less adorned males. There was a weak effect of male age being positively associated with paternity in own nests. Male body size measured as the length of wing and tarsus was weakly positively associated with paternity in own nests. Male survival prospect was positively associated with paternity in own nests. Polygynous males generally had decreased paternity of their broods compared to monogamous males. Paternity of the resident male decreased with increasing population density and breeding asynchrony. The intensity of paternity guards such as within-pair copulation rate and mate guarding were not significantly related to extra-pair paternity. Sperm competition was thus an important component of sexual selection by increasing the variance in male mating success, and by being associated with the expression of secondary sexual characters, in particular in dense and asynchronously breeding populations of birds.

[1]  T. Birkhead.  Behavioural adaptations to high density nesting in the common guillemot Uria aalge , 1978, Animal Behaviour.

[2]  T. Birkhead.  14 – Sperm Competition in Birds: Mechanisms and Function , 1998 .

[3]  P. Stockley.  Sperm Competition and Sexual Selection , 1999, Heredity.

[4]  D. Lack,et al.  Ecological adaptations for breeding in birds , 1969 .

[5]  D. Parkin,et al.  An association between fertility and cuckoldry in the house sparrow, Passer domesticus , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  Sperm competition and sexual selection , 1998 .

[7]  A. Møller,et al.  Female choice selects for male sexual tail ornaments in the monogamous swallow , 1988, Nature.

[8]  A. Møller,et al.  Cuckoldry and Sociality: A Comparative Study of Birds , 1993, The American Naturalist.

[9]  John C. Avise,et al.  Molecular Markers, Natural History and Evolution , 1993, Springer US.

[10]  A. Møller.  Immune defence, extra–pair paternity, and sexual selection in birds , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  A. C. Mateman,et al.  Low frequency of extra-pair fertilizations in the Great Tit Parus major revealed by DNA fingerprinting , 1997 .

[12]  L. Hedges,et al.  The Handbook of Research Synthesis , 1995 .

[13]  R. J. Robertson,et al.  The high frequency of extra-pair paternity in tree swallows is not an artifact of nestboxes , 1996, Behavioral Ecology and Sociobiology.

[14]  Derek A. Roff,et al.  The evolution of life histories : theory and analysis , 1992 .

[15]  Henrik G. Smith,et al.  Extra-Pair Paternity in the European Starling: The Effect of Polygyny , 1993 .

[16]  C. F. Thompson,et al.  Social mating system affects the frequency of extra-pair paternity in house wrens , 1997, Animal Behaviour.

[17]  A. Møller.  Sexual Selection and the Barn Swallow , 1994 .

[18]  L. Gustafsson,et al.  Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  B. Sheldon.  Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  P. Gowaty,et al.  Nestbox availability affects extra-pair fertilizations and conspecific nest parasitism in eastern bluebirds, Sialia sialis , 1991, Animal Behaviour.

[21]  A. Møller,et al.  Extra-pair paternity and tail ornamentation in the barn swallow Hirundo rustica , 1997, Behavioral Ecology and Sociobiology.

[22]  B. Kempenaers.  Does Reproductive Synchrony Limit Male Opportunities or Enhance Female Choice for Extra-Pair Paternity? , 1997 .

[23]  L. A. Whittingham,et al.  Extra-pair fertilizations increase the opportunity for sexual selection in the monogamous House Martin Delichon urbica , 1995 .

[24]  A. Dixon,et al.  Old, colourful male yellowhammers, Emberiza citrinella , benefit from extra-pair copulations , 1996, Animal Behaviour.

[25]  C. R. Freeman-Gallant.  DNA fingerprinting reveals female preference for male parental care in savannah sparrows , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  Bart Kempenaers,et al.  Extrapair paternity in the blue tit (Parus caeruleus) : female choice, male charateristics, and offspring quality , 1997 .

[27]  D. Price,et al.  Good genes and old age: Do old mates provide superior genes? , 1995 .

[28]  D. Bryant,et al.  Extra-pair fertilizations and paternity defence in house martins, Delichon urbica , 1995, Animal Behaviour.

[29]  A. Møller,et al.  Sperm competition in birds : evolutionary causes and consequences , 1992 .

[30]  C. A. May,et al.  Copulatory behaviour and paternity determined by DNA fingerprinting in kestrels: effects of cyclic food abundance , 1996, Animal Behaviour.

[31]  R. J. Robertson,et al.  Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows , 1994 .

[32]  A. Møller,et al.  Copulation Behaviour of Birds , 1987 .

[33]  P. Weatherhead,et al.  Breeding synchrony and extra-pair mating in red-winged blackbirds , 1997, Behavioral Ecology and Sociobiology.

[34]  A. Moller,et al.  A Pairwise Comparative Method as Illustrated by Copulation Frequency in Birds , 1992, The American Naturalist.

[35]  E. M. Gray,et al.  Female red-winged blackbirds accrue material benefits from copulating with extra-pair males , 1997, Animal Behaviour.

[36]  R. Rosenthal.  Parametric measures of effect size. , 1994 .

[37]  M. Hoi-Leitner,et al.  The importance of different paternity guards in the polygynandrous penduline tit (Remiz pendulinus) , 1997 .

[38]  P. Boag,et al.  Extrapair paternity and intraspecific brood parasitism in eastern bluebirds revealed by DNA fingerprinting , 1994 .

[39]  M. Willson,et al.  The Influence of Habitats on Mating Systems of North American Passerine Birds , 1966 .

[40]  J. Crook.  The adaptive significance of avian social organisations , 1964 .

[41]  R. Montgomerie,et al.  DNA fingerprinting reveals relation between tail ornaments and cuckoldry in barn swallows, Hirundo rustica , 1991 .

[42]  D. Westneat,et al.  To Guard Mates or Go Forage: Conflicting Demands Affect the Paternity of Male Red-Winged Blackbirds , 1994, The American Naturalist.

[43]  D. Westneat.  Extra-pair fertilizations in a predominantly monogamous bird: genetic evidence , 1987, Animal Behaviour.

[44]  N. Burley,et al.  Sexual selection and extrapair fertilization in a socially monogamous passerine, the zebra finch (Taeniopygia gullata) , 1996 .

[45]  S. Yezerinac,et al.  Reproductive synchrony and extra-pair mating strategy in a socially monogamous bird, Dendroica petechia , 1997, Animal Behaviour.

[46]  A. Møller.  Frequency of Female Copulations with Multiple Males and Sexual Selection , 1992, The American Naturalist.

[47]  R. Meldola.  Sexual Selection , 1871, Nature.

[48]  Gwenn W. Gröndal,et al.  Meta-analytic procedures for social research , 1993 .

[49]  C. R. Freeman-Gallant.  Extra-pair paternity in monogamous and polygynous Savannah sparrows, Passerculus sandwichensis , 1997, Animal Behaviour.

[50]  J. Lifjeld.  Do female house sparrows copulate with extra-pair mates to enhance their fertility? , 1994 .

[51]  G. Orians.  On the Evolution of Mating Systems in Birds and Mammals , 1969, The American Naturalist.

[52]  S. Bensch,et al.  Low frequency of extrapair paternity in the polygynous great reed warbler, Acrocephalus arundinaceus , 1995 .

[53]  R. Wagner.  The Pursuit of Extra-pair Copulations by Female Birds: A New Hypothesis of Colony Formation , 1993 .

[54]  P. Boag,et al.  Cuckoldry and lack of parentage-dependent paternal care in yellow warblers: a cost–benefit approach , 1996, Animal Behaviour.

[55]  B. Kempenaers,et al.  Genetic similarity, inbreeding and hatching failure in blue tits: are unhatched eggs infertile? , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  D. Westneat.  Paternity and paternal behaviour in the red-winged blackbird, Agelaius phoeniceus , 1995, Animal Behaviour.

[57]  J. Manning.  Choosy females and correlates of male age , 1985 .

[58]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[59]  Hanna Kokko,et al.  Evolutionarily stable strategies of age-dependent sexual advertisement , 1997, Behavioral Ecology and Sociobiology.

[60]  E. M. Gray.  Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus) , 1996, Behavioral Ecology and Sociobiology.

[61]  K. Bollmann,et al.  Ecological determinants of extrapair fertilizations and egg dumping in Alpine water pipits (Anthus spinoletta) , 1997 .

[62]  T. Birkhead.  Sperm competition in birds. , 1998, Reviews of reproduction.

[63]  L. Hedges,et al.  Statistical Methods for Meta-Analysis , 1987 .

[64]  R. J. Robertson,et al.  Extra-pair paternity in polygynous tree swallows , 1993, Animal Behaviour.

[65]  B. Stutchbury,et al.  Correlates of extra-pair fertilization success in hooded warblers , 1997, Behavioral Ecology and Sociobiology.

[66]  R. Wagner,et al.  Condition-dependent control of paternity by female purple martins: implications for coloniality , 1996, Behavioral Ecology and Sociobiology.

[67]  N. Davies,et al.  The polygynandrous mating system of the alpine accentor, Prunella collaris. II. Multiple paternity and parental effort , 1995, Animal Behaviour.

[68]  M. Eens,et al.  Extra-pair paternity and intraspecific brood parasitism in the European starling, Sturnus vulgaris: evidence from DNA fingerprinting , 1993, Animal Behaviour.

[69]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[70]  S. Emlen,et al.  Ecology, sexual selection, and the evolution of mating systems. , 1977, Science.

[71]  A. P. Møller,et al.  THE EVOLUTION OF PLUMAGE BRIGHTNESS IN BIRDS IS RELATED TO EXTRAPAIR PATERNITY , 1994, Evolution; international journal of organic evolution.

[72]  B. Stutchbury,et al.  Extrapair paternity in hooded warblers , 1994 .

[73]  John E. Hunter,et al.  Methods of Meta-Analysis: Correcting Error and Bias in Research Findings , 1991 .

[74]  B. Kempenaers,et al.  Extra-pair paternity results from female preference for high-quality males in the blue tit , 1992, Nature.

[75]  M. Braun,et al.  EXTRAPAIR FERTILIZATIONS AND THE EVOLUTION OF COLONIAL BREEDING IN PURPLE MARTINS , 1990 .

[76]  John C. Avise.  Molecular Markers, Natural History and Evolution , 1994, Springer US.

[77]  S. Yezerinac,et al.  Extra–pair mating, male plumage coloration and sexual selection in yellow warblers (Dendroica petechia) , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[78]  D. Westneat.  Extra-pair copulations in a predominantly monogamous bird: observations of behaviour , 1987, Animal Behaviour.

[79]  D. Westneat.  Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus) , 1993 .

[80]  G. Arnqvist,et al.  Meta-analysis: synthesizing research findings in ecology and evolution. , 1995, Trends in ecology & evolution.

[81]  H. Hoi,et al.  An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilizations , 1997 .

[82]  Gregg B. Jackson,et al.  Meta-Analysis: Cumulating Research Findings Across Studies , 1982 .

[83]  H. Ellegren,et al.  AN EXPERIMENTAL STUDY OF PATERNITY AND TAIL ORNAMENTATION IN THE BARN SWALLOW (HIRUNDO RUSTICA) , 1997, Evolution; international journal of organic evolution.

[84]  M. Petrie,et al.  The degree of extra-pair paternity increases with genetic variability. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[85]  A. Møller,et al.  Paternity and Multiple Signaling: Effects of a Secondary Sexual Character and Song on Paternity in the Barn Swallow , 1998, The American Naturalist.

[86]  S. Perreault,et al.  Patterns and correlates of extrapair paternity in American redstarts (Setophaga ruticilla) , 1997 .

[87]  S. J. Arnold,et al.  The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence , 1980, Animal Behaviour.

[88]  P. Sherman,et al.  Density and extra-pair fertilizations in birds: a comparative analysis , 1997, Behavioral Ecology and Sociobiology.

[89]  L. Hedges,et al.  The Handbook of Research Synthesis , 1995 .

[90]  B. Stutchbury,et al.  The Effect of Breeding Synchrony On Extra-Pair Mating Systems in Songbirds , 1995 .

[91]  T. Burke,et al.  Paternal investment inversely related to degree of extra-pair paternity in the reed bunting , 1994, Nature.

[92]  H. Lisle Gibbs,et al.  Realized Reproductive Success of Polygynous Red-Winged Blackbirds Revealed by DNA Markers , 1990, Science.

[93]  R. Robertson,et al.  Temporary male removal increases extra-pair paternity in eastern bluebirds , 1996, Animal Behaviour.

[94]  T. Amundsen,et al.  Paternity and paternity assurance behaviour in the bluethroat, Luscinias.svecica , 1996, Animal Behaviour.