Abstract

Inclusive fitness theory predicts that parental care will vary with relatedness between potentially caring parents and offspring, potentially shaping mating system evolution. Systems with extra-pair paternity (EPP), and hence variable parent–brood relatedness, provide valuable opportunities to test this prediction. However, existing theoretical and empirical studies assume that a focal male is either an offspring's father with no inbreeding, or is completely unrelated. We highlight that this simple dichotomy does not hold given reproductive interactions among relatives, complicating the effect of EPP on parent–brood relatedness yet providing new opportunities to test inclusive fitness theory. Accordingly, we tested hierarchical hypotheses relating parental feeding rate to parent–brood relatedness, parent kinship and inbreeding, using song sparrows (Melospiza melodia) experiencing natural variation in relatedness. As predicted, male and female feeding rates increased with relatedness to a dependent brood, even controlling for brood size. Male feeding rate tended to decrease as paternity loss increased, and increased with increasing kinship and hence inbreeding between socially paired mates. We thereby demonstrate that variation in a key component of parental care concurs with subtle predictions from inclusive fitness theory. We additionally highlight that such effects can depend on the underlying social mating system, potentially generating status-specific costs of extra-pair reproduction.

Highlights

  • A central ambition in evolutionary ecology is to understand how ‘altruistic’ behaviours, which cost actors but benefit recipients, evolve as functions of interactions among relatives [1,2,3,4]

  • Paternal care is predicted to increase with a male’s paternity success and resulting male–brood relatedness, defined as the total number of copies of an allele that is present in focal male i that is expected to be present in the brood [5,12,13,14,15]

  • Patterns of variation in parental feeding rates observed in song sparrows experiencing considerable natural variation in parent–brood relatedness, resulting from combinations of extra-pair paternity (EPP), mate kinship and individual coefficient of inbreeding, broadly concurred with key predictions of inclusive fitness theory

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Summary

Introduction

A central ambition in evolutionary ecology is to understand how ‘altruistic’ behaviours, which cost actors but benefit recipients, evolve as functions of interactions among relatives [1,2,3,4]. Systems where relatedness between potentially caring adults and dependent offspring varies among family groups offer interesting opportunities to test this prediction, and to examine the degree to which adaptive plastic responses in parental care can arise and potentially shape mating system evolution Such variation in adult–offspring relatedness is commonplace in socially monogamous systems with variable extra-pair paternity (EPP) [7,8,9,10,11]. Because a potentially caring male’s relatedness to an EPO may not be zero, the decrease in TAVi resulting from EPP no longer equals 1⁄2BS PEPO Rather, this difference (hereafter ‘lost allelic value’, LAV) can be calculated as LAV = PAV − TAVi, where PAV is the ‘potential allelic value’ of the brood to the male if he had sired the entire brood (electronic supplementary material, appendix S1). Predicted response by males paternal feeding rate will increase with increasing TAV more tightly than with increasing BS paternal feeding rate will increase with increasing TAV after controlling for BS paternal feeding rate will decrease with increasing LAV and PEPO paternal feeding rate will increase with increasing kij paternal feeding rate will not vary with fi predicted response by females maternal feeding rate will increase with increasing TAV more tightly than with increasing BS maternal feeding rate will increase with increasing TAV after controlling for BS maternal feeding rate will not vary directly with LAV or PEPO maternal feeding rate will increase with increasing kij maternal feeding rate will not vary with fj

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