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Is there indirect selection on female extra-pair reproduction through cross-sex genetic correlations with male reproductive fitness?

ABSTRACT: One key hypothesis explaining the evolution and persistence of polyandry, and resulting female extra-pair reproduction in socially monogamous systems, is that female propensity for extra-pair reproduction is positively genetically correlated with male reproductive fitness and consequently experiences positive cross-sex indirect selection. However, key genetic correlations have rarely been estimated, especially in free-living populations experiencing natural (co)variation in reproductive strategies and fitness. We used long-term life-history and pedigree data from song sparrows (Melospiza melodia) to estimate the cross-sex genetic correlation between female propensity for extra-pair reproduction and adult male lifetime reproductive success, and thereby test a key hypothesis regarding mating system evolution. There was substantial additive genetic variance in both traits, providing substantial potential for indirect selection on female reproductive strategy. However, the cross-sex genetic correlation was estimated to be close to zero. Such small correlations might arise because male reproductive success achieved through extra-pair paternity was strongly positively genetically correlated with success achieved through within-pair paternity, implying that the same successful males commonly sire offspring produced by polyandrous and monogamous females. Cross-sex indirect selection may consequently have limited capacity to drive evolution of female extra-pair reproduction, or hence underlying polyandry, in systems where multiple routes to paternity success exist.

SUBMITTER: Reid JM

PROVIDER: S-EPMC6121835 | biostudies-other | 2018 Jun

REPOSITORIES: biostudies-other

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Is there indirect selection on female extra-pair reproduction through cross-sex genetic correlations with male reproductive fitness?

Reid Jane M JM Wolak Matthew E ME

Evolution letters 20180615 3

One key hypothesis explaining the evolution and persistence of polyandry, and resulting female extra-pair reproduction in socially monogamous systems, is that female propensity for extra-pair reproduction is positively genetically correlated with male reproductive fitness and consequently experiences positive cross-sex indirect selection. However, key genetic correlations have rarely been estimated, especially in free-living populations experiencing natural (co)variation in reproductive strategi ...[more]

PMID: 30283673

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Project description:One hypothesis explaining extra-pair reproduction is that socially monogamous females mate with extra-pair males to adjust the coefficient of inbreeding (f) of extra-pair offspring (EPO) relative to that of within-pair offspring (WPO) they would produce with their socially paired male. Such adjustment of offspring f requires non-random extra-pair reproduction with respect to relatedness, which is in turn often assumed to require some mechanism of explicit pre-copulatory or post-copulatory kin discrimination. We propose three demographic processes that could potentially cause mean f to differ between individual females' EPO and WPO given random extra-pair reproduction with available males without necessarily requiring explicit kin discrimination. Specifically, such a difference could arise if social pairings formed non-randomly with respect to relatedness or persisted non-randomly with respect to relatedness, or if the distribution of relatedness between females and their sets of potential mates changed during the period through which social pairings persisted. We used comprehensive pedigree and pairing data from free-living song sparrows (Melospiza melodia) to quantify these three processes and hence investigate how individual females could adjust mean offspring f through instantaneously random extra-pair reproduction. Female song sparrows tended to form social pairings with unrelated or distantly related males slightly less frequently than expected given random pairing within the defined set of available males. Furthermore, social pairings between more closely related mates tended to be more likely to persist across years than social pairings between less closely related mates. However, these effects were small and the mean relatedness between females and their sets of potential extra-pair males did not change substantially across the years through which social pairings persisted. Our framework and analyses illustrate how demographic and social structuring within populations might allow females to adjust mean f of offspring through random extra-pair reproduction without necessarily requiring explicit kin discrimination, implying that adjustment of offspring f might be an inevitable consequence of extra-pair reproduction. New theoretical and empirical studies are required to explore the general magnitude of such effects and quantify the degree to which they could facilitate or constrain long-term evolution of extra-pair reproduction.

Dataset Information

Is there indirect selection on female extra-pair reproduction through cross-sex genetic correlations with male reproductive fitness?

Publications

Is there indirect selection on female extra-pair reproduction through cross-sex genetic correlations with male reproductive fitness?

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