Female Extra-pair Reproduction Research Articles

Indirect genetic effects increase heritability estimates for male and female extra-pair reproduction.

The question of why females engage in extra-pair behaviours is long-standing in evolutionary biology. One suggestion is that these behaviours are maintained through pleiotropic effects on male extra-pair behaviors (genes controlling extra-pair reproduction are shared between sexes, but only beneficial to one sex, in this case, males). However, for this to evolve extra-pair reproduction must be both heritable and positively genetically correlated between sexes. Previous studies have suggested low heritability with no evidence for between-sex genetic correlations in extra-pair reproduction. However, these have not considered indirect genetic effects (derived from the behaviour of others, IGEs) from the social partner, the influence of the social partner's genotype on the phenotype of an individual, despite the potential of IGEs to uncover hidden heritable variation. Using data from a closed house sparrow population with a genetic pedigree spanning two decades, we tested the influence of social partner IGEs on heritable variation and genetic correlation estimates of extra-pair reproduction. We found that the inclusion of IGEs resulted in larger heritable genetic variance for both male and female extra-pair heritability. While IGEs did not change between-sex genetic correlations, we found they reduced uncertainty in those estimates. Future studies should consider the effect of IGEs on the mechanisms of sex specific extra-pair reproduction.

Complex effects of helper relatedness on female extrapair reproduction in a cooperative breeder

AbstractIn cooperatively breeding species, the presence of male helpers in a group often reduces the breeding female’s fidelity to her social partner, possibly because there is more than one potential sire in the group. Using a long-term study of cooperatively breeding superb fairy-wrens (Malurus cyaneus) and records of paternity in 1936 broods, we show that the effect of helpers on rates of extrapair paternity varied according to the helpers’ relatedness to the breeding female. The presence of unrelated male helpers in a group increased average rates of extrapair paternity, from 57% for groups with no unrelated helpers, to 74% with one unrelated helper, to 86% with 2+ unrelated helpers. However, this increase was due in equal part to helpers within the group and males in other groups achieving increased paternity. In contrast, helpers who were sons of the breeding female did not gain paternity, nor did they affect the level of extra-group paternity (which occurred at rates of 60%, 58%, 61% in the presence of 0, 1, 2+ helper sons, respectively). There was no evidence of effects of helpers’ relatedness to the female on nest productivity or nestling performance. Because the presence of helpers per se did not elevate extrapair reproduction rates, our results undermine the “constrained female hypothesis” explanation for an increase in extrapair paternity with helper number in cooperative breeders. However, they indicate that dominant males are disadvantaged by breeding in “cooperative” groups. The reasons why the presence of unrelated helpers, but not of helper-sons, results in higher rates of extra-group reproduction are not clear.

Recent immigrants alter the quantitative genetic architecture of paternity in song sparrows.

Quantifying additive genetic variances and cross‐sex covariances in reproductive traits, and identifying processes that shape and maintain such (co)variances, is central to understanding the evolutionary dynamics of reproductive systems. Gene flow resulting from among‐population dispersal could substantially alter additive genetic variances and covariances in key traits in recipient populations, thereby altering forms of sexual conflict, indirect selection, and evolutionary responses. However, the degree to which genes imported by immigrants do in fact affect quantitative genetic architectures of key reproductive traits and outcomes is rarely explicitly quantified. We applied structured quantitative genetic analyses to multiyear pedigree, pairing, and paternity data from free‐living song sparrows (Melospiza melodia) to quantify the differences in mean breeding values for major sex‐specific reproductive traits, specifically female extra‐pair reproduction and male paternity loss, between recent immigrants and the previously existing population. We thereby quantify effects of natural immigration on the means, variances, and cross‐sex covariance in total additive genetic values for extra‐pair paternity arising within the complex socially monogamous but genetically polygynandrous reproductive system. Recent immigrants had lower mean breeding values for male paternity loss, and somewhat lower values for female extra‐pair reproduction, than the local recipient population, and would therefore increase the emerging degree of reproductive fidelity of social pairings. Furthermore, immigration increased the variances in total additive genetic values for these traits, but decreased the magnitudes of the negative cross‐sex genetic covariation and correlation below those evident in the existing population. Immigration thereby increased the total additive genetic variance but could decrease the magnitude of indirect selection acting on sex‐specific contributions to paternity outcomes. These results demonstrate that dispersal and resulting immigration and gene flow can substantially affect quantitative genetic architectures of complex local reproductive systems, implying that comprehensive theoretical and empirical efforts to understand mating system dynamics will need to incorporate spatial population processes.

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

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.

Variation in parent-offspring kinship in socially monogamous systems with extra-pair reproduction and inbreeding.

Female extra‐pair reproduction in socially monogamous systems is predicted to cause cuckolded socially‐paired males to conditionally reduce paternal care, causing selection against extra‐pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially‐paired female and/or to her extra‐pair mate, and therefore be related to extra‐pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra‐pair reproduction, might then be weakened. We derive metrics that quantify allele‐sharing between within‐pair and extra‐pair offspring and their mother and her socially‐paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra‐pair reproduction and inbreeding on a brood's total allelic value to its socially‐paired parents. Cuckolded male song sparrows were almost always detectably related to extra‐pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra‐pair reproduction, this decrease was reduced by within‐pair and extra‐pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra‐pair reproduction, parental care, and inbreeding.

Double decomposition: decomposing the variance in subcomponents of male extra-pair reproductive success.

1. Extra-pair reproductive success (EPRS) is a key component of male fitness in socially monogamous systems and could cause selection on female extra-pair reproduction if extra-pair offspring (EPO) inherit high value for EPRS from their successful extra-pair fathers. However, EPRS is itself a composite trait that can be fully decomposed into subcomponents of variation, each of which can be further decomposed into genetic and environmental variances. However, such decompositions have not been implemented in wild populations, impeding evolutionary inference. 2. We first show that EPRS can be decomposed into the product of three life-history subcomponents: the number of broods available to a focal male to sire EPO, the male's probability of siring an EPO in an available brood and the number of offspring in available broods. This decomposition of EPRS facilitates estimation from field data because all subcomponents can be quantified from paternity data without need to quantify extra-pair matings. Our decomposition also highlights that the number of available broods, and hence population structure and demography, might contribute substantially to variance in male EPRS and fitness. 3. We then used 20 years of complete genetic paternity and pedigree data from wild song sparrows (Melospiza melodia) to partition variance in each of the three subcomponents of EPRS, and thereby estimate their additive genetic variance and heritability conditioned on effects of male coefficient of inbreeding, age and social status. 4. All three subcomponents of EPRS showed some degree of within-male repeatability, reflecting combined permanent environmental and genetic effects. Number of available broods and offspring per brood showed low additive genetic variances. The estimated additive genetic variance in extra-pair siring probability was larger, although the 95% credible interval still converged towards zero. Siring probability also showed inbreeding depression and increased with male age, while the numbers of available broods and offspring per brood did not. 5. Our results indicate that the probability that a male will sire an EPO in an available brood is the primary source of genetic variation in male EPRS, implying that the evolution of female extra-pair reproduction could be facilitated by genetic covariance with this subcomponent of EPRS.

Female and male genetic effects on offspring paternity: additive genetic (co)variances in female extra-pair reproduction and male paternity success in song sparrows (Melospiza melodia).

Ongoing evolution of polyandry, and consequent extra-pair reproduction in socially monogamous systems, is hypothesized to be facilitated by indirect selection stemming from cross-sex genetic covariances with components of male fitness. Specifically, polyandry is hypothesized to create positive genetic covariance with male paternity success due to inevitable assortative reproduction, driving ongoing coevolution. However, it remains unclear whether such covariances could or do emerge within complex polyandrous systems. First, we illustrate that genetic covariances between female extra-pair reproduction and male within-pair paternity success might be constrained in socially monogamous systems where female and male additive genetic effects can have opposing impacts on the paternity of jointly reared offspring. Second, we demonstrate nonzero additive genetic variance in female liability for extra-pair reproduction and male liability for within-pair paternity success, modeled as direct and associative genetic effects on offspring paternity, respectively, in free-living song sparrows (Melospiza melodia). The posterior mean additive genetic covariance between these liabilities was slightly positive, but the credible interval was wide and overlapped zero. Therefore, although substantial total additive genetic variance exists, the hypothesis that ongoing evolution of female extra-pair reproduction is facilitated by genetic covariance with male within-pair paternity success cannot yet be definitively supported or rejected either conceptually or empirically.

Predicting evolutionary responses to selection on polyandry in the wild: additive genetic covariances with female extra-pair reproduction

The evolutionary forces that underlie polyandry, including extra-pair reproduction (EPR) by socially monogamous females, remain unclear. Selection on EPR and resulting evolution have rarely been explicitly estimated or predicted in wild populations, and evolutionary predictions are vulnerable to bias due to environmental covariances and correlated selection through unmeasured traits. However, evolutionary responses to (correlated) selection on any trait can be directly predicted as additive genetic covariances (covA) with appropriate components of relative fitness. I used comprehensive life-history, paternity and pedigree data from song sparrows (Melospiza melodia) to estimate covA between a female's liability to produce extra-pair offspring and two specific fitness components: relative annual reproductive success (ARS) and survival to recruitment. All three traits showed non-zero additive genetic variance. Estimates of covA were positive, predicting evolution towards increased EPR, but 95% credible intervals overlapped zero. There was therefore no conclusive prediction of evolutionary change in EPR due to (correlated) selection through female ARS or recruitment. Negative environmental covariance between EPR and ARS would have impeded evolutionary prediction from phenotypic selection differentials. These analyses demonstrate an explicit quantitative genetic approach to predicting evolutionary responses to components of (correlated) selection on EPR that should be unbiased by environmental covariances and unmeasured traits.

Offspring fitness varies with parental extra-pair status in song sparrows,Melospiza melodia

Numerous studies have tested for indirect selection on female extra-pair reproduction (EPR) by quantifying whether extra-pair young (EPY) are fitter than their within-pair young (WPY) maternal half-siblings. In contrast, the hypothesis that offspring of EPY and WPY (rather than the EPY and WPY themselves) differ in fitness has not been tested, even though inter-generational effects of parental extra-pair status on offspring fitness could alter the magnitude and direction of indirect selection on EPR. We tested whether offspring of EPY song sparrows, Melospiza melodia, were more likely to recruit or produce hatched or recruited offspring over their lifetimes than offspring of WPY. Hatchlings with one or two EPY parents were more likely to recruit and produce hatched offspring than hatchlings with two WPY parents. Furthermore, these relationships differed between maternal versus paternal extra-pair status. Hatchlings with EPY fathers were more likely to recruit and produce offspring than hatchlings with WPY fathers. In contrast, hatchlings with EPY mothers were as likely to recruit as hatchlings with WPY mothers and tended to be less likely to produce recruited offspring. Depending on the causal genetic and environmental mechanisms, such conflicting inter-generational relationships between parental extra-pair status and offspring fitness could substantially influence the evolutionary dynamics of EPR.

Are There Indirect Fitness Benefits of Female Extra-Pair Reproduction? Lifetime Reproductive Success of Within-Pair and Extra-Pair Offspring

The forces driving extra-pair reproduction by socially monogamous females, and the resulting genetic polyandry, remain unclear. A testable prediction of the hypothesis that extra-pair reproduction partly reflects indirect selection on females is that extra-pair young (EPY) will be fitter than their within-pair young (WPY) maternal half-siblings. This prediction has not been comprehensively tested in a wild population, requiring data on the lifetime reproductive success (LRS) of maternal half-sib EPY and WPY. We used 17 years of genetic parentage data from song sparrows, Melospiza melodia, to compare the LRS of hatched EPY and WPY maternal half-siblings measured as their lifetime number of hatched offspring, recruited offspring, and hatched grandoffspring. EPY hatchlings were not significantly fitter than WPY hatchlings for any of three measures of LRS. Furthermore, opposite to prediction, EPY hatchlings tended to have lower LRS than their maternal half-sibling WPY hatchlings on average. EPY also tended to be less likely to survive to hatch than their maternal half-sibling WPY. Taken together, these results fail to support one key hypothesis explaining the evolution of genetic polyandry by socially monogamous females and suggest there may be weak indirect selection against female extra-pair reproduction in song sparrows.

Indirect selection on female extra-pair reproduction? Comparing the additive genetic value of maternal half-sib extra-pair and within-pair offspring

One specific hypothesis explaining the evolution of extra-pair reproduction (EPR) by socially monogamous females is that EPR is under indirect selection because extra-pair offspring (EPO) sired by extra-pair males have higher additive genetic value for fitness than the within-pair offspring (WPO) a female would have produced had she solely mated with her socially paired male. This hypothesis has not been explicitly tested by comparing additive genetic value between EPO and the WPO they replaced. We show that the difference in additive genetic breeding value (BV) between EPO and the WPO they replaced is proportional to the genetic covariance between offspring fitness and male net paternity gain through EPR, and estimate this covariance with respect to offspring recruitment in free-living song sparrows (Melospiza melodia). Recruitment and net paternity gain showed non-zero additive genetic variance and heritability, and negative genetic covariance. Opposite to prediction, EPO therefore had lower BV for recruitment than the WPO they replaced. We thereby demonstrate an explicit quantitative genetic approach to testing the hypothesis that EPR allows polyandrous females to increase offspring additive genetic value, and suggest that there may be weak indirect selection against female EPR through reduced additive genetic value for recruitment of EPO versus WPO in song sparrows.

Sex-specific differential survival of extra-pair and within-pair offspring in song sparrows,Melospiza melodia

It is widely hypothesized that the evolution of female extra-pair reproduction in socially monogamous species reflects indirect genetic benefits to females. However, a critical prediction of this hypothesis, that extra-pair young (EPY) are fitter than within-pair young (WPY), has rarely been rigorously tested. We used 18 years of data from free-living song sparrows, Melospiza melodia, to test whether survival through major life-history stages differed between EPY and WPY maternal half-siblings. On average, survival of hatched chicks to independence from parental care and recruitment, and their total lifespan, did not differ significantly between EPY and WPY. However, EPY consistently tended to be less likely to survive, and recruited EPY survived for significantly fewer years than recruited WPY. Furthermore, the survival difference between EPY and WPY was sex-specific; female EPY were less likely to survive to independence and recruitment and lived fewer years than female WPY, whereas male EPY were similarly or slightly more likely to survive and to live more years than male WPY. These data indicate that extra-pair paternity may impose an indirect cost on females via their female offspring and that sex-specific genetic, environmental or maternal effects may shape extra-pair reproduction.

Additive Genetic Variance, Heritability, and Inbreeding Depression in Male Extra-Pair Reproductive Success

The hypothesis that female extra-pair reproduction in socially monogamous animals reflects indirect genetic benefits requires that there be additive and/or nonadditive genetic variance in fitness. However, the specific hypotheses that male extra-pair reproductive success (EPRS) shows additive genetic variance (V(A)), heritability (h2), or inbreeding depression, and hence that females could acquire indirect genetic benefits through increased EPRS of sons, have not been explicitly tested. We used comprehensive genetic pedigree data from song sparrows (Melospiza melodia) to estimate V(A), h2, and inbreeding depression in the number of extra-pair offspring a male sired per year and the probability that a male would sire any extra-pair offspring per year. Inbreeding depression was substantial: more inbred males sired fewer extra-pair offspring and were less likely to sire any extra-pair offspring. In contrast, estimates of V(A) and h2 were close to 0, although 95% credible intervals were relatively wide. These data suggest that females could accrue indirect genetic benefits, in terms of increased EPRS of outbred sons, by mating with unrelated social or extra-pair mates. In contrast, any indirect benefit of extra-pair reproduction in terms of producing sons with high additive genetic value for EPRS is most likely to be small.

Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia)

The forces driving the evolution of extra-pair reproduction in socially monogamous animals remain widely debated and unresolved. One key hypothesis is that female extra-pair reproduction evolves through indirect genetic benefits, reflecting increased additive genetic value of extra-pair offspring. Such evolution requires that a female's propensity to produce offspring that are sired by an extra-pair male is heritable. However, additive genetic variance and heritability in female extra-pair paternity (EPP) rate have not been quantified, precluding accurate estimation of the force of indirect selection. Sixteen years of comprehensive paternity and pedigree data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) showed significant additive genetic variance and heritability in the proportion of a female's offspring that was sired by an extra-pair male, constituting major components of the genetic architecture required for extra-pair reproduction to evolve through indirect additive genetic benefits. However, estimated heritabilities were moderately small (0.12 and 0.18 on the observed and underlying latent scales, respectively). The force of selection on extra-pair reproduction through indirect additive genetic benefits may consequently be relatively weak. However, the additive genetic variance and non-zero heritability observed in female EPP rate allow for multiple further genetic mechanisms to drive and constrain mating system evolution.

A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females

A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females