Sex-dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias.

Sex-dependent selection often leads to spectacularly different phenotypes in males and females. In species in which sexual dimorphism is not complete, it is unclear which benefits females and males derive from displaying a trait that is typical of the other sex. In barn owls (Tyto alba), females exhibit on average larger black eumelanic spots than males but members of the two sexes display this trait in the same range of possible values. In a 12-year study, we show that selection exerted on spot size directly or on genetically correlated traits strongly favoured females with large spots and weakly favoured males with small spots. Intense directional selection on females caused an increase in spot diameter in the population over the study period. This increase is due to a change in the autosomal genes underlying the expression of eumelanic spots but not of sex-linked genes. Female-like males produced more daughters than sons, while male-like females produced more sons than daughters when mated to a small-spotted male. These sex ratio biases appear adaptive because sons of male-like females and daughters of female-like males had above-average survival. This demonstrates that selection exerted against individuals displaying a trait that is typical of the other sex promoted the evolution of specific life history strategies that enhance their fitness. This may explain why in many organisms sexual dimorphism is often not complete.

[1]  D Gianola,et al.  Bayesian analysis of genetic change due to selection using Gibbs sampling , 1994, Genetics Selection Evolution.

[2]  J. Hadfield Estimating evolutionary parameters when viability selection is operating , 2008, Proceedings of the Royal Society B: Biological Sciences.

[3]  J. Leonard,et al.  Parallel processing in an identified neural circuit: the Aplysia californica gill‐withdrawal response model system , 2004, Biological reviews of the Cambridge Philosophical Society.

[4]  K. Burnham,et al.  Program MARK: survival estimation from populations of marked animals , 1999 .

[5]  A. Roulin Short- and long-term fitness correlates of rearing conditions in Barn Owls Tyto alba , 2002 .

[6]  E. Postma Implications of the difference between true and predicted breeding values for the study of natural selection and micro‐evolution , 2006, Journal of evolutionary biology.

[7]  S. J. Arnold,et al.  THE MEASUREMENT OF SELECTION ON CORRELATED CHARACTERS , 1983, Evolution; international journal of organic evolution.

[8]  T. Day,et al.  Intralocus Sexual Conflict Can Drive the Evolution of Genomic Imprinting , 2004, Genetics.

[9]  P. V. Tienderen,et al.  ELASTICITIES AND THE LINK BETWEEN DEMOGRAPHIC AND EVOLUTIONARY DYNAMICS , 2000 .

[10]  Res Altwegg,et al.  Age‐Specific Fitness Components and Their Temporal Variation in the Barn Owl , 2006, The American Naturalist.

[11]  H. Ellegren,et al.  Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus) , 2003, Journal of evolutionary biology.

[12]  J. Mank,et al.  Sex-Linkage of Sexually Antagonistic Genes is Predicted by Female, but Not Male, Effects in Birds , 2009, Evolution; international journal of organic evolution.

[13]  Alexandra Roulin The evolution, maintenance and adaptive function of genetic colour polymorphism in birds , 2004, Biological reviews of the Cambridge Philosophical Society.

[14]  A. Roulin Proximate basis of the covariation between a melanin-based female ornament and offspring quality , 2004, Oecologia.

[15]  J. Mank Sex Chromosomes and the Evolution of Sexual Dimorphism: Lessons from the Genome , 2008, The American Naturalist.

[16]  R. O’Hara,et al.  Bayesian approaches in evolutionary quantitative genetics , 2008, Journal of evolutionary biology.

[17]  D. Westneat,et al.  Sexual conflict as a partitioning of selection , 2009, Biology Letters.

[18]  S. Chenoweth,et al.  Intralocus sexual conflict. , 2009, Trends in ecology & evolution.

[19]  L. Kruuk,et al.  ESTIMATING SELECTION ON NEONATAL TRAITS IN RED DEER USING ELASTICITY PATH ANALYSIS , 2003, Evolution; international journal of organic evolution.

[20]  A. Roulin,et al.  Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl , 2003, Heredity.

[21]  N. Mundy A window on the genetics of evolution: MC1R and plumage colouration in birds , 2005, Proceedings of the Royal Society B: Biological Sciences.

[22]  A. Roulin,et al.  Breeding rate is associated with pheomelanism in male and with eumelanism in female barn owls , 2007 .

[23]  R. Nisbet,et al.  How should we define 'fitness' for general ecological scenarios? , 1992, Trends in ecology & evolution.

[24]  Henrik Jensen,et al.  Utilizing Gaussian Markov Random Field Properties of Bayesian Animal Models , 2010, Biometrics.

[25]  A. Ducrest,et al.  Extra-pair paternity, testes size and testosterone level in relation to colour polymorphism in the barn owl Tyto alba , 2004 .

[26]  Bradley P. Carlin,et al.  Bayesian measures of model complexity and fit , 2002 .

[27]  H. Ellegren Molecular evolutionary genomics of birds , 2007, Cytogenetic and Genome Research.

[28]  B. Sinervo,et al.  Within‐clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild , 2003, Journal of evolutionary biology.

[29]  W. Rice SEX CHROMOSOMES AND THE EVOLUTION OF SEXUAL DIMORPHISM , 1984, Evolution; international journal of organic evolution.

[30]  W. Rice,et al.  Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  L. Kruuk Estimating genetic parameters in natural populations using the "animal model". , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  A. Roulin,et al.  Variation and covariation in survival, dispersal, and population size in barn owls Tyto alba , 2003 .

[33]  Hans Ellegren,et al.  The evolution of sex-biased genes and sex-biased gene expression , 2007, Nature Reviews Genetics.

[34]  A. Roulin SHORT-AND LONG-TERM FITNESS CORRELATES OF REARING CONDITIONS IN BARN OWLS TYTO , 2002 .

[35]  Copenhagen,et al.  Bayesian inference in threshold models using Gibbs sampling , 1994 .

[36]  B. Sinervo,et al.  The effect of sexually antagonistic selection on adaptive sex ratio allocation , 2007 .

[37]  David R. Anderson,et al.  Modeling Survival and Testing Biological Hypotheses Using Marked Animals: A Unified Approach with Case Studies , 1992 .

[38]  Nicholas H. Barton,et al.  The Relative Rates of Evolution of Sex Chromosomes and Autosomes , 1987, The American Naturalist.

[39]  Jarrod D. Hadfield,et al.  The Misuse of BLUP in Ecology and Evolution , 2009, The American Naturalist.

[40]  I. Steinsland,et al.  Evolutionary Dynamics of a Sexual Ornament in the House Sparrow (Passer domesticus): The Role of Indirect Selection Within and Between Sexes , 2008, Evolution; international journal of organic evolution.

[41]  B. Sinervo,et al.  Uncoupling direct and indirect components of female choice in the wild , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. Roulin Nonrandom pairing by male barn owls (Tyto alba) with respect to a female plumage trait , 1999 .

[43]  L. Keller,et al.  Pleiotropy in the melanocortin system, coloration and behavioural syndromes. , 2008, Trends in ecology & evolution.

[44]  A. Roulin,et al.  Selection on a eumelanic ornament is stronger in the tropics than in temperate zones in the worldwide‐distributed barn owl , 2009, Journal of evolutionary biology.