Strategic female reproductive investment in response to male attractiveness in birds

Life-history theory predicts that individuals should adjust their reproductive effort according to the expected fitness returns on investment. Because sexually selected male traits should provide honest information about male genetic or phenotypic quality, females may invest more when paired with attractive males. However, there is substantial disagreement in the literature whether such differential allocation is a general pattern. Using a comparative meta-regression approach, we show that female birds generally invest more into reproduction when paired with attractive males, both in terms of egg size and number as well as food provisioning. However, whereas females of species with bi-parental care tend to primarily increase the number of eggs when paired with attractive males, females of species with female-only care produce larger, but not more, eggs. These patterns may reflect adaptive differences in female allocation strategies arising from variation in the signal content of sexually selected male traits between systems of parental care. In contrast to reproductive effort, female allocation of immune-stimulants, anti-oxidants and androgens to the egg yolk was not consistently increased when mated to attractive males, which probably reflects the context-dependent costs and benefits of those yolk compounds to females and offspring.

[1]  Female choice and the quality of parental care in the great tit Parus major , 1990, Behavioral Ecology and Sociobiology.

[2]  A. Cockburn,et al.  Reduced Egg Investment Can Conceal Helper Effects in Cooperatively Breeding Birds , 2007, Science.

[3]  Trevor Hastie,et al.  Regularization Paths for Generalized Linear Models via Coordinate Descent. , 2010, Journal of statistical software.

[4]  N. Burley The Differential-Allocation Hypothesis: An Experimental Test , 1988, The American Naturalist.

[5]  A. Cockburn Prevalence of different modes of parental care in birds , 2006, Proceedings of the Royal Society B: Biological Sciences.

[6]  N. Saino,et al.  Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks , 2005, Behavioral Ecology and Sociobiology.

[7]  C. Vleck,et al.  Maternal Effects Increase Within‐Family Variation in Offspring Survival , 2009, The American Naturalist.

[8]  H. Schwabl,et al.  Maternal testosterone in the avian egg enhances postnatal growth. , 1996, Comparative biochemistry and physiology. Part A, Physiology.

[9]  A. J. Moore,et al.  The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability , 2007, Proceedings of the National Academy of Sciences.

[10]  T. Amundsen,et al.  Is male plumage reflectance correlated with paternal care in bluethroats , 2001 .

[11]  T. Groothuis,et al.  Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  P. Lachenbruch Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[13]  T. Uller,et al.  Parental effects on carotenoid-based plumage coloration in nestling great tits, Parus major , 2006, Behavioral Ecology and Sociobiology.

[14]  P. Gowaty Reproductive compensation , 2008, Journal of evolutionary biology.

[15]  C. M. Lessells,et al.  Manipulative Signals in Family Conflict? On the Function of Maternal Yolk Hormones in Birds , 2007, The American Naturalist.

[16]  Miloš Krist Short- and long-term effects of egg size and feeding frequency on offspring quality in the collared flycatcher (Ficedula albicollis). , 2009, The Journal of animal ecology.

[17]  B. Sheldon,et al.  Differential allocation: tests, mechanisms and implications. , 2000, Trends in ecology & evolution.

[18]  D. Penn,et al.  Mate Choice for Genetic Benefits: Time to Put the Pieces Together , 2010 .

[20]  J. Balthazart,et al.  Sexual versus individual differentiation: the controversial role of avian maternal hormones , 2007, Trends in Endocrinology & Metabolism.

[21]  D. Altman,et al.  Measuring inconsistency in meta-analyses , 2003, BMJ : British Medical Journal.

[22]  H. Kokko Should advertising parental care be honest? , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  Ralph R. Miller,et al.  CHANGES IN AMBIENT TEMPERATURE TRIGGER YAWNING BUT NOT STRETCHING IN RATS. , 2011, Ethology : formerly Zeitschrift fur Tierpsychologie.

[24]  G. Hill Plumage coloration is a sexually selected indicator of male quality , 1991, Nature.

[25]  S. Alonzo,et al.  Does a trade‐off between current reproductive success and survival affect the honesty of male signalling in species with male parental care? , 2010, Journal of evolutionary biology.

[26]  Mark W. Lipsey,et al.  Practical Meta-Analysis , 2000 .

[27]  J. Graves,et al.  Male attractiveness and differential testosterone investment in zebra finch eggs. , 1999, Science.

[28]  J. Christians Avian egg size: variation within species and inflexibility within individuals , 2002, Biological reviews of the Cambridge Philosophical Society.

[29]  T. Clutton‐Brock,et al.  The Evolution of Parental Care , 2019 .

[30]  A. J. Moore,et al.  INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS: I. DIRECT AND INDIRECT GENETIC EFFECTS OF SOCIAL INTERACTIONS , 1997, Evolution; international journal of organic evolution.

[31]  T. Price,et al.  Maternal effects, paternal effects and sexual selection. , 2001, Trends in ecology & evolution.

[32]  W. E. Harris,et al.  Reproductive investment when mate quality varies: differential allocation versus reproductive compensation , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  P. Gowaty,et al.  Reproductive compensation for offspring viability deficits by female mallards, Anas platyrhynchos , 2004, Animal Behaviour.

[34]  D. Mock,et al.  Parental Feeding Rates in the House Sparrow, Passer domesticus: Are Larger‐Badged Males Better Fathers? , 2002 .

[35]  D. Hasselquist,et al.  Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  A. Russell,et al.  Egg investment is influenced by male attractiveness in the mallard , 2000, Nature.

[37]  A. Badyaev,et al.  Context‐dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird , 2003, Journal of evolutionary biology.

[38]  G. Hill,et al.  Paternal care as a conditional strategy: Distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch , 2002 .

[39]  D. Gil Chapter 7 Hormones in Avian Eggs: Physiology, Ecology and Behavior , 2008 .

[40]  J. Partecke,et al.  Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows , 2008, Developmental neurobiology.

[41]  T. Mappes,et al.  Maternal effort and male quality in the bank vole, Clethrionomys glareolus , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  R. L. Young,et al.  Evolution of sex‐biased maternal effects in birds. IV. Intra‐ovarian growth dynamics can link sex determination and sex‐specific acquisition of resources , 2008, Journal of evolutionary biology.

[43]  D. Roff The evolution of life histories : theory and analysis , 1992 .

[44]  H. Schielzeth,et al.  Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males , 2009, Proceedings of the Royal Society B: Biological Sciences.

[45]  T. Clutton‐Brock,et al.  Helpers increase the reproductive potential of offspring in cooperative meerkats , 2007, Proceedings of the Royal Society B: Biological Sciences.

[46]  N. Hazon,et al.  Maternal effects due to male attractiveness affect offspring development in the zebra finch , 2006, Proceedings of the Royal Society B: Biological Sciences.

[47]  J. Matthias Starck,et al.  Avian growth and development : evolution within the altricial-precocial spectrum , 1998 .

[48]  N. Saino,et al.  Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rus , 1995 .

[49]  D. Roff Life History, Evolution of , 2001 .

[50]  L. Partridge,et al.  Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products , 1995, Nature.

[51]  A. Møller,et al.  Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[52]  I. Cuthill,et al.  Effect size, confidence interval and statistical significance: a practical guide for biologists , 2007, Biological reviews of the Cambridge Philosophical Society.

[53]  Wolf,et al.  The role of maternal and paternal effects in the evolution of parental quality by sexual selection , 1999 .

[54]  G. Hill,et al.  Evolution of sex‐biased maternal effects in birds: III. Adjustment of ovulation order can enable sex‐specific allocation of hormones, carotenoids, and vitamins , 2006, Journal of evolutionary biology.

[55]  Andrew Thomas,et al.  WinBUGS - A Bayesian modelling framework: Concepts, structure, and extensibility , 2000, Stat. Comput..

[56]  J. Komdeur,et al.  Maternal Effects Contribute to the Superior Performance of Extra-Pair Offspring , 2009, Current Biology.

[57]  N. Saino,et al.  Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow , 2002 .

[58]  J. Graves,et al.  Differential allocation and `good genes` , 2001 .

[59]  R. Ambrosini,et al.  Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow‐legged gull (Larus michahellis) chicks in relation to sex and laying order , 2008, Journal of evolutionary biology.

[60]  J. Hadfield,et al.  General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi‐trait models for continuous and categorical characters , 2010, Journal of evolutionary biology.

[61]  B. Sheldon,et al.  Environmental Sensitivity in Relation to Size and Sex in Birds: Meta‐Regression Analysis , 2009, The American Naturalist.

[62]  T. Groothuis,et al.  Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[63]  J. Prechl,et al.  Maternal immunoglobulin concentration in Collared Flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order , 2006 .

[64]  Miloš Krist Egg size and offspring quality: a meta‐analysis in birds , 2011, Biological reviews of the Cambridge Philosophical Society.

[65]  J. Komdeur,et al.  Differential deposition of antimicrobial proteins in blue tit (Cyanistes caeruleus) clutches by laying order and male attractiveness , 2010, Behavioral Ecology and Sociobiology.

[66]  H. Kokko,et al.  Differential allocation and compensation: who deserves the silver spoon? , 2010 .

[67]  C. Catchpole,et al.  Song as an indicator of male parental effort in the sedge warbler , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[68]  N. Burley Sexual Selection for Aesthetic Traits in Species with Biparental Care , 1986, The American Naturalist.

[69]  T. Groothuis,et al.  Balancing between costs and benefits of maternal hormone deposition in avian eggs , 2005, Biology Letters.

[70]  A. Houston,et al.  Conflict between parents over care. , 2005, Trends in ecology & evolution.

[71]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[72]  T. Groothuis,et al.  Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition , 2009 .

[73]  F. Vézina,et al.  Metabolic Costs of Egg Production in the European Starling (Sturnus vulgaris) , 2002, Physiological and Biochemical Zoology.

[74]  R. Ambrosini,et al.  Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant , 2011, Hormones and Behavior.

[75]  Jarrod D. Hadfield,et al.  MCMC methods for multi-response generalized linear mixed models , 2010 .

[76]  Bernd Leisler,et al.  Repertoire size, sexual selection, and offspring viability in the great reed warbler: changing patterns in space and time , 2004 .

[77]  T. Uller,et al.  Evolution of "determinants" in sex-determination: a novel hypothesis for the origin of environmental contingencies in avian sex-bias. , 2009, Seminars in cell & developmental biology.

[78]  T. Groothuis,et al.  Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study , 2003, Animal Behaviour.

[79]  G. Sorci,et al.  Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (Pavo cristatus) , 2007, Behavioral Ecology and Sociobiology.