Extra-pair Reproductive Success Research Articles

Female differential allocation in response to extrapair offspring and social mate attractiveness.

Renewed debate over what benefits females might gain from producing extra‐pair offspring emphasizes the possibility that apparent differences in quality between within‐pair and extra‐pair offspring are confounded by greater maternal investment in extra‐pair offspring. Moreover, the attractiveness of a female's social mate can also influence contributions of both partners to a reproductive attempt. Here, we explore the complexities involved in parental investment decisions in response to extra‐pair offspring and mate attractiveness with a focus on the female point of view. Adult zebra finches paired and reproduced in a colony setting. A male's early‐life diet quality and his extra‐pair reproductive success were used as metrics of his mating attractiveness. Females paired with males that achieved extra‐pair success laid heavier eggs than other females and spent less time attending their nests than their mates or other females. Extra‐pair nestlings were fed more protein‐rich hen's egg than within‐pair nestlings. Females producing extra‐pair offspring had more surviving sons than females producing only within‐pair offspring. Collectively, results show that females differentially allocate resources in response to offspring extra‐pair status and their social mate's attractiveness. Females may also obtain fitness benefits through the production of extra‐pair offspring.

Testosterone secretion in a socially monogamous but sexually promiscuous migratory passerine

The steroid hormone testosterone (T) influences a multitude of traits critical to reproduction in vertebrates. In birds, high male T supports territory establishment and mate attraction, but is thought to interfere with parental care. Interspecific comparisons indicate that migratory species with short, synchronous breeding seasons have the highest peak T, and that the seasonal profile of T exhibits a rapid decline with the onset of incubation by females. We describe the T profile of the migratory, socially monogamous, and biparental Eastern Kingbird (Tyrannus tyrannus) from the high desert of eastern Oregon, USA, where breeding occurs within a short 2–3month period. Eastern Kingbirds are socially monogamous but exhibit high rates of extra-pair paternity as ∼60% of broods contain extra-pair young. We therefore evaluate whether Eastern Kingbirds exhibit the “typical” T profile expected for a synchronously breeding migratory species, or whether T is maintained at a more constant level as would be predicted for a species with opportunities for mating that extend over a majority of the breeding season. Our samples were divided into six periods of the reproductive cycle from territory establishment to the feeding of fledglings. T did not change across stages of the nest cycle. Instead, T declined with sampling date and nest density, and increased with the number of fertile females in the population. Male kingbirds advertise their presence through song for most of the breeding season, and we suggest that T is maintained throughout most of the breeding season because male fitness is equally dependent on within- and extra-pair reproductive success.

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.

Genetic covariance between components of male reproductive success: within-pair vs. extra-pair paternity in song sparrows.

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra-pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within-pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra-pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade-off between male within-pair paternity success and extra-pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.

Spatial distribution of nests constrains the strength of sexual selection in a warbler

In socially monogamous species, extra-pair paternity may increase the strength of intersexual selection by allowing males with preferred phenotypes to monopolize matings. Several studies have found relationships between male signals and extra-pair mating, but many others fail to explain variation in extra-pair mating success. A greater appreciation for the role that ecological contingencies play in structuring behavioural processes may help to reconcile contradictory results. We studied extra-pair mating in a spatial context in the common yellowthroat (Geothlypis trichas), a territorial wood warbler. Over the course of 6 years, we observed 158 breeding attempts by 99 males, resulting in a total of 369 nests and 520 sampled nestlings. The spatial distribution of territories varied greatly, with males having between 0 and 10 close neighbours and between three and 39 neighbouring nestlings close enough to represent extra-pair siring opportunities. Both within-pair and extra-pair reproductive success increased with breeding density, but the opportunity for sexual selection and strength of selection varied with density. Total variance in reproductive success was highest at low density and was mostly explained by variation in within-pair success. In contrast, at high density, both within-pair and extra-pair successes contributed substantially to variance in reproductive success. The relationships between plumage and extra-pair mating also varied by density; plumage was under strong sexual selection via extra-pair mating success at high density, but no selection was detected at low density. Thus, ecological factors that structure social interactions can drive patterns of sexual selection by facilitating or constraining the expression of mating preferences.

Decomposing variation in male reproductive success: age‐specific variances and covariances through extra‐pair and within‐pair reproduction

Age-specific variances and covariances in reproductive success shape the total variance in lifetime reproductive success (LRS), age-specific opportunities for selection, and population demographic variance and effective size. Age-specific (co)variances in reproductive success achieved through different reproductive routes must therefore be quantified to predict population, phenotypic and evolutionary dynamics in age-structured populations. While numerous studies have quantified age-specific variation in mean reproductive success, age-specific variances and covariances in reproductive success, and the contributions of different reproductive routes to these (co)variances, have not been comprehensively quantified in natural populations. We applied 'additive' and 'independent' methods of variance decomposition to complete data describing apparent (social) and realised (genetic) age-specific reproductive success across 11 cohorts of socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia). We thereby quantified age-specific (co)variances in male within-pair and extra-pair reproductive success (WPRS and EPRS) and the contributions of these (co)variances to the total variances in age-specific reproductive success and LRS. 'Additive' decomposition showed that within-age and among-age (co)variances in WPRS across males aged 2-4 years contributed most to the total variance in LRS. Age-specific (co)variances in EPRS contributed relatively little. However, extra-pair reproduction altered age-specific variances in reproductive success relative to the social mating system, and hence altered the relative contributions of age-specific reproductive success to the total variance in LRS. 'Independent' decomposition showed that the (co)variances in age-specific WPRS, EPRS and total reproductive success, and the resulting opportunities for selection, varied substantially across males that survived to each age. Furthermore, extra-pair reproduction increased the variance in age-specific reproductive success relative to the social mating system to a degree that increased across successive age classes. This comprehensive decomposition of the total variances in age-specific reproductive success and LRS into age-specific (co)variances attributable to two reproductive routes showed that within-age and among-age covariances contributed substantially to the total variance and that extra-pair reproduction can alter the (co)variance structure of age-specific reproductive success. Such covariances and impacts should consequently be integrated into theoretical assessments of demographic and evolutionary processes in age-structured populations.

EXTRA-PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra-pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males' apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free-living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within-pair reproductive success (WPRS) and extra-pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0-27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males' contributions to future generations, its impact on population-level parameters such as the opportunity for selection and effective population size was limited.

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.

Plumage color and reproduction in the red-backed fairy-wren: Why be a dull breeder?

Males of many species can breed in distinct alternative phenotypes; for example, in many birds some males breed in dull plumage while others breed in bright plumage. Because females often appear to prefer brighter males, it is unclear why some males breed in dull plumage. Males in dull plumage might enjoy enhanced within-pair reproductive success if they can gain access to better breeding territories, or they might have relatively high extrapair reproductive success if they are better able to intrude on the territories of other males. To test these possibilities, we examined the reproductive consequences of plumage color in the red-backed fairy-wren (Malurus melanocephalus), a species in which males can breed in either bright plumage or dull plumage or serve as nonbreeding auxiliaries. Male plumage color was distributed bimodally and was loosely associated with age, such that some males molted into bright plumage a year or more earlier than others. Both male phenotypes were cuckolded at similar rates, but bright males sired significantly more extrapair young than did dull males, and this effect was independent of age. Thus, 1-year-old males who bred in dull plumage had low seasonal reproductive success compared with same-aged males who bred in bright plumage. These results suggest that males may not reap any fitness benefits by breeding in dull coloration, compared with breeding in bright plumage, but rather may be constrained to breed in suboptimal plumage by the timing of plumage acquisition.

Extrapair paternity in chestnut-sided warblers is correlated with consistent vocal performance

The elaborateness of many bird songs is commonly presumed to have evolved under the influence of sexual selection by female mate choice. Thus, aspects of acoustic diversity, such as song repertoire size, are seen as likely targets of female choice. In many songbird species with song repertoires, however, the repertoires are small. In such species, female choice might be based on song features other than, or in addition to, song diversity. To investigate this conjecture, I assessed singing and paternity in a population of chestnut-sided warblers (Dendroica pensylvanica), a species in which song repertoires are of modest size. Twenty-two song traits were evaluated to determine which ones best predicted male extrapair reproductive success. The candidate traits encompassed measures of song diversity (e.g., song repertoire size), gross-scale song performance (e.g., singing rate), and fine-scale song performance (e.g., variability among songs in a bout). Regression analysis revealed that the best predictor of extrapair success was singing with little variability. In particular, the most successful males sang with consistent pitch and timing, as well as high pitch. The greater extrapair success of males with more consistent vocal performance may be due to female preference for such performance, which could be an indicator of male quality. Copyright 2007.