Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner's heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.

[1]  J. Aparicio,et al.  What should we weigh to estimate heterozygosity, alleles or loci? , 2006, Molecular ecology.

[2]  B. Kempenaers,et al.  A spatial genetic structure and effects of relatedness on mate choice in a wild bird population , 2006, Molecular ecology.

[3]  R. Mulder,et al.  Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  E Matthysen,et al.  A comparison of microsatellite‐based pairwise relatedness estimators , 2001, Molecular ecology.

[5]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .

[6]  V. Penteriani,et al.  A process of pair formation leading to assortative mating: passive age-assortative mating by habitat heterogeneity , 2003, Animal Behaviour.

[7]  A. Dhondt,et al.  Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches , 2005, Biology Letters.

[8]  Dispersal, kinship and inbreeding in an island population of the Great Tit , 1988 .

[9]  L. Sevensson Identification Guide to European Passerines , 1975 .

[10]  TIMOTHY R. FRASIER,et al.  STORM: software for testing hypotheses of relatedness and mating patterns , 2008, Molecular ecology resources.

[11]  J. Aparicio,et al.  Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population , 2007, Molecular ecology.

[12]  J. Sanz,et al.  Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus. , 2009, The Journal of animal ecology.

[13]  M. Kirkpatrick,et al.  The evolution of mating preferences and the paradox of the lek , 1991, Nature.

[14]  I. Cuthill,et al.  Ultraviolet Vision in Birds , 2000 .

[15]  E. Matthysen,et al.  Seasonal and lifetime reproductive consequences of inbreeding in the great tit Parus major , 2003 .

[16]  B. Charlesworth,et al.  The genetic basis of inbreeding depression. , 1999, Genetical research.

[17]  S. Bensch,et al.  No evidence for inbreeding avoidance in a great reed warbler population , 2007 .

[18]  B. Campbell Forces and Strategies in Evolution. (Book Reviews: Sexual Selection and the Descent of Man, 1871-1971) , 1972 .

[19]  D. W. Zeh,et al.  The evolution of polyandry I: intragenomic conflict and genetic incompatibility , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[21]  J. L. Tomkins,et al.  Mate choice or polyandry: reconciling genetic compatibility and good genes sexual selection , 2002 .

[22]  D E Weeks,et al.  Similarity of DNA fingerprints due to chance and relatedness. , 1993, Human heredity.

[23]  J. Ott Genetic data analysis II , 1997 .

[24]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

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

[26]  Susan C. Roberts,et al.  Genetic similarity and quality interact in mate choice decisions by female mice , 2003, Nature Genetics.

[27]  H. Kokko,et al.  Evolution of Mate Choice for Genome-Wide Heterozygosity , 2009, Evolution; international journal of organic evolution.

[28]  J. Aparicio,et al.  Egg production and individual genetic diversity in lesser kestrels , 2007, Molecular ecology.

[29]  Rauno V. Alatalo,et al.  Good-genes effects in sexual selection , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  Staffan Andersson,et al.  Ultraviolet sexual dimorphism and assortative mating in blue tits , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  E Matthysen,et al.  Natal dispersal and parental escorting predict relatedness between mates in a passerine bird , 2006, Molecular ecology.

[32]  B. Kempenaers Mate Choice and Genetic Quality: A Review of the Heterozygosity Theory , 2007 .

[33]  A. Gosler,et al.  Inheritance and variation in eggshell patterning in the great tit Parus major , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  G. Hill,et al.  Choosing mates: good genes versus genes that are a good fit. , 2004, Trends in ecology & evolution.

[35]  James N. M. Smith,et al.  Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia) , 2005, Proceedings of the Royal Society B: Biological Sciences.

[36]  E. G. Cothran,et al.  Correlation between the individual heterozygosity of parents and their offspring , 1993, Heredity.

[37]  J. Reid Secondary sexual ornamentation and non-additive genetic benefits of female mate choice , 2007, Proceedings of the Royal Society B: Biological Sciences.

[38]  J. L. Tomkins,et al.  On the resolution of the lek paradox. , 2008, Trends in ecology & evolution.

[39]  W. Amos,et al.  Female fur seals show active choice for males that are heterozygous and unrelated , 2007, Nature.

[40]  J. Aparicio,et al.  Genetic consequences of natal dispersal in the colonial lesser kestrel , 2008, Molecular ecology.

[41]  F. Balloux,et al.  Does heterozygosity estimate inbreeding in real populations? , 2004, Molecular ecology.

[42]  K. Scribner,et al.  Environmental and Genetic Components of Antler Growth in White-Tailed Deer , 1989 .

[43]  Kaspar Delhey,et al.  Male sexual attractiveness and parental effort in blue tits: a test of the differential allocation hypothesis , 2005, Animal Behaviour.

[44]  J. Slate,et al.  MICROSATELLITE MEASURES OF INBREEDING: A META‐ANALYSIS , 2003, Evolution; international journal of organic evolution.

[45]  Jerram L. Brown A theory of mate choice based on heterozygosity , 1997 .

[46]  T. Pitcher,et al.  Genetic quality and sexual selection: an integrated framework for good genes and compatible genes , 2004, Molecular ecology.

[47]  R. Mauck,et al.  Asymmetrical incest avoidance in the choice of social and genetic mates , 2006, Animal Behaviour.

[48]  T. Clutton‐Brock Sexual selection in females , 2009, Animal Behaviour.

[49]  J. Pemberton Measuring inbreeding depression in the wild: the old ways are the best. , 2004, Trends in ecology & evolution.

[50]  R. Trivers Parental investment and sexual selection , 1972 .

[51]  T. Pitcher,et al.  Mate choice for non-additive genetic benefits: a resolution to the lek paradox. , 2008, Journal of theoretical biology.

[52]  J. Aparicio,et al.  Individual genetic diversity correlates with the size and spatial isolation of natal colonies in a bird metapopulation , 2008, Proceedings of the Royal Society B: Biological Sciences.

[53]  S. Washburn The evolution of man. , 1978, Scientific American.

[54]  B. Sheldon,et al.  Dispersal as a means of inbreeding avoidance in a wild bird population , 2008, Proceedings of the Royal Society B: Biological Sciences.

[55]  Susan C. Roberts,et al.  Correlations between heterozygosity and measures of genetic similarity: implications for understanding mate choice , 2006, Journal of evolutionary biology.

[56]  M. Milinski,et al.  Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism , 2001, Nature.

[57]  I. Cuthill,et al.  Preferences for ultraviolet partners in the blue tit , 1999, Animal Behaviour.

[58]  J. Slate,et al.  Does reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)? , 2006, Current Biology.

[59]  B. C. Glass,et al.  Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data , 2004, Heredity.

[60]  L. Kruuk,et al.  Severe inbreeding depression in collared flycatchers (Ficedula albicollis) , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[61]  C. Catchpole,et al.  Sexual selection and individual genetic diversity in a songbird , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  W. Amos,et al.  Inbreeding: Disease susceptibility in California sea lions , 2003, Nature.

[63]  B. Kempenaers,et al.  Females increase offspring heterozygosity and fitness through extra-pair matings , 2003, Nature.

[64]  J. Veiga,et al.  A test of the hypothesis of mate choice based on heterozygosity in the spotless starling , 2001, Animal Behaviour.

[65]  C. Eckert,et al.  A test of the good-genes-as-heterozygosity hypothesis using red-winged blackbirds , 1999 .

[66]  A. Magurran,et al.  Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots , 2003, Journal of evolutionary biology.

[67]  Helena Westerdahl,et al.  Complex Mhc-based mate choice in a wild passerine , 2006, Proceedings of the Royal Society B: Biological Sciences.

[68]  W. Hamilton,et al.  Heritable true fitness and bright birds: a role for parasites? , 1982, Science.

[69]  L. Keller,et al.  No Evidence for Inbreeding Avoidance in a Natural Population of Song Sparrows (Melospiza melodia) , 1998, The American Naturalist.

[70]  I. Cuthill,et al.  Blue tits are ultraviolet tits , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[71]  L. Bachmann,et al.  Female genetic heterogeneity affects the reproduction of great tits (Parus major L., 1758) in low-quality woodlands , 2007 .

[72]  Dafydd Gibbon,et al.  1 User’s guide , 1998 .

[73]  D. W. Zeh,et al.  The evolution of polyandry II: post–copulatory defenses against genetic incompatibility , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.