Extra-pair Offspring Research Articles

Experimental elevation of testosterone lowers fitness in female dark-eyed juncos

Testosterone (T) is often referred to as the “male hormone,” but it can influence aggression, parental behavior, and immune function in both males and females. By experimentally relating hormone-induced changes in phenotype to fitness, it is possible to ask whether existing phenotypes perform better or worse than alternative phenotypes, and hence to predict how selection might act on a novel or rare phenotype. In a songbird, the dark-eyed junco (Junco hyemalis), we have examined the effects of experimentally elevated T in females on fitness-related behaviors such as parental care. In this study, we implanted female juncos with exogenous T and examined its effect on fitness (survival, reproduction, and extra-pair mating) to assess whether T-altered phenotypes would prove to be adaptive or deleterious for females. Experimental elevation of T decreased the likelihood that a female would breed successfully, and T-implanted females had lower total reproductive success at every stage of the reproductive cycle. They did not, however, differ from control females in fledgling quality, extra-pair offspring production, survival, or reproduction in the following year. Previous work in this system has shown that experimental elevation of T in males alters behavior and physiology and decreases survival but increases the production of extra-pair offspring, leading to higher net fitness relative to control animals. Our results suggest that increased T has divergent effects on male and female fitness in this species, and that prevailing levels in females may be adaptive for them. These findings are consistent with sexual conflict.

Individual variation in sleep behaviour in blue tits Cyanistes caeruleus: assortative mating and associations with fitness‐related traits

Sleep is ubiquitous in animals, but there is great inter‐ and intraspecific variation in the daily amount of sleep that is needed. Chronic sleep curtailment or experimental sleep deprivation are known to impair health and performance of individuals, but not much is known about the fitness consequences of naturally occurring variation in sleep behaviour. Here we test for assortative mating in sleep behaviour and for correlations between sleep phenotypes and reproductive success and survival in a free‐living blue tit population. We found that partners of a social breeding pair were mated assortatively in regard to standardized awakening time, i.e. awakening time relative to that of other birds of the same sex in the population. We found no evidence for assortative mating for other sleep parameters. In female blue tits no sleep parameter that we measured was significantly correlated with lay date or clutch size. Females that had extra‐pair young in their brood did not differ in awakening time, or in any other sleep parameter, compared to females without extra‐pair young. In males, the probability of siring extra‐pair young was related to sleep onset and sleep duration, but not as predicted. Males that began to sleep earlier and slept longer were more likely to sire extra‐pair offspring. None of the sleep parameters were significantly correlated with local survival of first‐year birds. Our results suggest that there is no strong effect of variation in sleep behaviour on fitness in blue tits, at least under natural conditions. Such a relationship might only become evident when natural sleep patterns are experimentally disturbed, or when sleep quality is affected by anthropogenic noise or light pollution.

Extra-pair matings, context-dependence and offspring quality: a brood manipulation experiment in pied flycatchers

Extra-pair paternity (EPP) in socially monogamous species has been associated with the genetic benefits incurred by females through extra-pair mate choice. There is conflicting evidence in the literature concerning the importance of such benefits possibly due to their context-dependence. To ascertain if there are such context-dependent genetic benefits, we conducted a brood manipulation experiment in pied flycatchers (Ficedula hypoleuca) breeding in central Spain. We found that extra-pair mates (EPM) are frequently not nearest neighbours. Cuckolded males and EPM did not differ from other males in any measured trait, and were not different either when cuckolds and cuckolders were compared within broods. Within-pair offspring (WPO) and extra-pair offspring (EPO) did not differ with respect to heterozygosity and no association of heterozygosity of either offspring or males and females with EPP could be detected. Moreover, the competitive context in the nest induced by brood manipulations affected the growth of nestlings and showed an interaction with paternity differences in nestling mass but in the opposite direction to the prediction of context-dependence, i.e., EPO were lighter than WPO in enlarged broods but not in control broods. Furthermore, EPO had shorter tarsi than WPO in all treatments. Mortality in the nest showed an association with brood manipulation treatment, but not with paternity or its interaction with treatment. Thus, we have not found any evidence of genetic benefits, context-dependent or otherwise, of EPP in our study population. The evidence of poor quality EPO does not support a mixed reproductive strategy of females in our population.

Extrapair paternity in Parus major

Mating systems, as an evolutionary stable strategy, play an important role in animal reproductive process and result from an animal's adaption to their environment, including their inter-specific environment. In the 1980s, extrapair paternity (EPP) was first noted in the eurychoric species, the Great Tit, Parus major. As earlier studies indicated, morphology, physiology, behavior, ecological characteristics and mating systems of eurychoric species differ greatly between areas or populations. Accordingly, we analyzed the mating system of the Great Tit (P.m.minor) in Fairy Cave National Nature Reserve, Liaoning, China. We collected total parent-offspring blood samples from 22 broods. We used 8 hypervariable loci, which were selected from 11 reported microsatellite loci for paternity test. In conjunction with the known genetic pattern of the female parent, the accuracy of the paternity testing reached 99.98% with this genetic data. Results of paternity testing showed that 7 of 22 broods (31.8%) had extra-pair nestling, with 16 of 197 nestlings (8.12%) a result of extra-pair fertilizations. The EPP rate of the Great Tit we noted in Liaoning is obviously lower than those in other passerine forest birds (less than 10%). Though between 55.6% and 9.1% extrapair offspring were found among the different nests, we were, however, unable to find any explanatory rule.

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.

Reinterpreting Bateman gradients: multiple mating and selection in both sexes of a songbird species

Bateman’s principle, which states that male reproductive success should increase with multiple mating, whereas female reproductive success should not, has long been used to explain sex differences in behavior. The statistical relationship between mating success and reproductive success, or Bateman gradient, has been proposed as a way to quantify sex differences in sexual selection. We used a long-term data set on the distribution of paternity in the socially monogamous dark-eyed junco to examine the effect of multiple mating on lifetime reproductive success and to determine the relative contributions of within-pair and extra-pair mating. Both sexes exhibited a strong positive Bateman gradient, even when the number of breeding years was accounted for. Although theory suggests that this pattern indicates a strong potential for sexual selection in both sexes, we argue that the interpretation of strong Bateman gradients, particularly in females, has many potential complications. We discuss several alternative explanations for our results, none of which requires sexual selection acting on female traits, including targeting of inherently fecund females by males seeking extra-pair mates and increased power to detect extra-pair offspring as family size increases. Because neither of these explanations requires that increased mating success causes increased reproductive success, we conclude that using Bateman gradients to measure the potential for sexual selection may be misleading for some mating systems and life histories, such as the iteroparous social monogamy found in juncos.

Female Red-backed Fairy-Wrens (Malurus melanocephalus) do not appear to pay a cost for high rates of promiscuity

ABSTRACT. Males of monogamous species are expected to increase their overall fitness by engaging in extrapair copulations, but the fitness implications of this behavior for females are somewhat less clear. Numerous studies have examined the potential benefits of extrapair mating to females, but the costs of extrapair mating, which may be substantial, are less well studied. Quantifying these costs is critical to understanding the evolution of extrapair mating behavior in females. We examined the costs of extrapair paternity to female Red-backed Fairy-wrens (Malurus melanocephalus) using an 8-year data set that allowed us to examine both short-term and long-term costs. The variability of individual extrapair mating behavior in female Red-backed Fairy-wrens allowed us to compare the parental care, fecundity, and apparent survival of faithful and promiscuous females. We found no effect of the presence of extrapair offspring on the rate at which males provisioned broods. We also found that promiscuous and fait...

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.

The ecological–evolutionary interplay: density‐dependent sexual selection in a migratory songbird

Little is understood about how environmental heterogeneity influences the spatial dynamics of sexual selection. Within human-dominated systems, habitat modification creates environmental heterogeneity that could influence the adaptive value of individual phenotypes. Here, we used the gray catbird to examine if the ecological conditions experienced in the suburban matrix (SM) and embedded suburban parks (SP) influence reproductive strategies and the strength of sexual selection. Our results show that these habitats varied in a key ecological factor, breeding density. Moreover, this ecological factor was closely tied to reproductive strategies such that local breeding density predicted the probability that a nest would contain extra-pair offspring. Partitioning reproductive variance showed that while within-pair success was more important in both habitats, extra-pair success increased the opportunity for sexual selection by 39% at higher breeding densities. Body size was a strong predictor of relative reproductive success and was under directional selection in both habitats. Importantly, our results show that the strength of sexual selection did not differ among habitats at the landscape scale but rather that fine-scale variation in an ecological factor, breeding density, influenced sexual selection on male phenotypes. Here, we document density-dependent sexual selection in a migratory bird and hypothesize that coarse-scale environmental heterogeneity, in this case generated by anthropogenic habitat modification, changed the fine-scale ecological conditions that drove the spatial dynamics of sexual selection.

When should cuckolded males care for extra-pair offspring?

In socially monogamous species with bi-parental care, males suffer reduced reproductive success if their mate engages in extra-pair copulations (EPCs). One might therefore expect that males should refuse to care for a brood if they can detect that an EPC has occurred. Here, we use a game-theory model to study male brood care in the face of EPCs in a cooperatively breeding species in which offspring help to raise their (half-) siblings in their parents' next breeding attempt. We show that under certain conditions males are selected to care even for broods completely unrelated to themselves. This counterintuitive result arises through a form of pseudo-reciprocity, whereby surviving extra-pair offspring, when helping to rear their younger half-siblings, can more than compensate for the cost incurred by the male that raised them. We argue that similar effects may not be limited to cooperative breeders, but may arise in various contexts in which cooperation between (half-) siblings occurs.

Declining extra-pair paternity with laying order associated with initial incubation behavior, but independent of final clutch size in the blue tit

Although functional explanations for female engagement in extra-pair copulation have been studied extensively in birds, little is known about how extra-pair paternity is linked to other fundamental aspects of avian reproduction. However, recent studies indicate that the occurrence of extra-pair offspring may generally decline with laying order, possibly because stimulation by eggs induces incubation, which may suppress female motivation to acquire extra-pair paternity. Here we tested whether experimental inhibition of incubation during the laying phase, induced by the temporary removal of eggs, resulted in increased extra-pair paternity, in concert with a later cessation of laying, in blue tits (Cyanistes caeruleus). As expected, experimental females showed a more gradual increase in nocturnal incubation duration over the laying phase and produced larger clutches than controls. Moreover, incubation duration on the night after the first egg was laid predicted how extra-pair paternity declined with laying order, with less incubation being associated with more extra-pair offspring among the earliest eggs in the clutch. However, incubation duration on this first night was unrelated to our experimental treatment and independent of final clutch size. Consequently, the observed decline in extra-pair paternity with laying order was unaffected by our manipulation and larger clutches included proportionally fewer extra-pair offspring. We suggest that female physiological state prior to laying, associated with incubation at the onset of laying, determines motivation to acquire extra-pair paternity independent of final clutch size. This decline in proportion of extra-pair offspring with clutch size may be a general pattern within bird species.

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.

Effects of known age on male paternity in a migratory songbird

Many avian studies have shown that reproductive performance improves with age, but little is known about how key components of male fitness, extrapair and within pair paternity, vary across life spans. We tested for age effects on male paternity in purple martins (Progne subis) using cross-sectional analyses of known-aged males (1–9 years old) and longitudinal analyses of individuals sampled in 2 successive years. Microsatellite analyses found that 137 of 297 (46%) nests contained extrapair offspring and 273 of 1235 (22%) offspring were extrapair. Using a subsample of unique known-aged males (n = 160), we found significant linear and nonlinear effects of male age on the number of within pair offspring and, to a lesser extent, on the number of extrapair offspring sired. Male genetic reproductive success increased with age to 3 years and then leveled off. In longitudinal comparisons of known age males sampled in successive years (n = 41), within pair offspring increased with age, even for males ≥2 years old. Paired comparisons (n = 74) found that extrapair sires were older than the males they cuckolded, and that first-year males were significantly underrepresented as extrapair sires given the known age distribution in the population. Poor genetic reproductive performance in younger males is likely constrained through male–male competition during mate guarding and female choice for older males.

Experimental manipulation shows that the white wing patch in collared flycatchers is a male sexual ornament

Descriptive analysis suggests that a conspicuous white wing patch in dichromatic (black and white) pied and collared flycatchers is under sexual selection. Here, we use an experimental approach to test whether this trait is indeed the target of selection. We caught 100 collared flycatcher Ficedula albicollis males soon after their arrival on the breeding site. We reduced (blackened) part of the white wing patch in half of these males and recorded their mating success and within and extra-pair offspring production. Reduction of the size of the white wing patch lowered a male's probability to attract a secondary social female, but not a primary female. However, primary females paired to males with a reduced wing patch were smaller (in tarsus), suggesting that male choice of partner or female–female competition over mates occurs in this species. The probability of pairing with a primary female (but not other components of male reproductive success) declined with arrival time (proxied by the date of capture). Males with a reduced wing patch size tended to sire less extra-pair offspring, although this relationship was reversed in one of the three study plots, suggesting that mating dynamics are context dependent. While our findings show that wing patch size is the target of sexual selection, the pathways and the strength of selection on this ornament differed markedly from a previous descriptive study. Nonexperimental studies of sexual selection in the wild may overestimate its importance because male fitness and ornamentation both depend positively on environmental conditions.

Superiority of extra-pair offspring: maternal but not genetic effects as revealed by a mixed cross-fostering design

Extra-pair copulations (EPC) are the rule rather than an exception in socially monogamous birds, but despite widespread occurrences, the benefits of female infidelity remain elusive. Most attention has been paid to the possibility that females gain genetic benefits from EPC, and fitness comparisons between maternal half-siblings are considered to be a defining test of this hypothesis. Recently, it was shown that these comparisons may be confounded by within-brood maternal effects where one such effect may be the distribution of half-siblings in the laying order. However, this possibility is difficult to study as it would be necessary to detect the egg from which each chick hatched. In this study, we used a new approach for egg-chick assignment and cross-fostered eggs on an individual basis among a set of nests of the collared flycatcher Ficedula albicollis. After hatching, chicks were ascribed to mothers and therefore to individual eggs by molecular genetic methods. Extra-pair young predominated early in the laying order. Under natural conditions, this should give them a competitive advantage over their half-siblings, mediated by hatching asynchrony. However, we experimentally synchronized hatching, and after this treatment, extra-pair young did not outperform within-pair young in any studied trait including survival up to recruitment and several indicators of reproductive success and attractiveness. We obtained only modest sample sizes for the last two traits and did not test for extra-pair success of male offspring. Thus, we cannot exclude the possibility of advantages of extra-pair young during the adult phase of life. However, our data tentatively suggest that the more likely reason for females' EPCs is the insurance against the infertility of a social mate.

By any name, female-female competition yields differential mating success.

By any name, female-female competition yields differential mating success.

Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric

In cooperative breeders, the tension between the opposing forces of kin selection and kin competition is at its most severe. Although philopatry facilitates kin selection, it also increases the risk of inbreeding. When dispersal is limited, extra-pair paternity might be an important mechanism to avoid inbreeding, but evidence for this is equivocal. The red-winged fairy-wren is part of a genus of cooperative breeders with extreme levels of promiscuity and male philopatry, but is unique in that females are also strongly philopatric. Here, we test the hypothesis that promiscuity is an important inbreeding avoidance mechanism when both sexes are philopatric. Levels of extra-pair paternity were substantial (70% of broods), but did not arise through females mating with their helpers, but via extra-group mating. Offspring were more likely to be sired by extra-pair males when the social pair was closely related, and these extra-pair males were genetically less similar to the female than the social male and thus, inbreeding is avoided through extra-pair mating. Females were consistent in their choice of the extra-pair sire over time and preferred early moulting males. Despite neighbouring males often being close kin, they sired 37% of extra-pair offspring. However, females that gained paternity from neighbours were typically less related to them than females that gained paternity further away. Our study is the first to suggest that mating with both closely related social partners and neighbours is avoided. Such sophistication in inbreeding avoidance strategies is remarkable, as the extreme levels of promiscuity imply that social context may provide little cue to relatedness.

Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories

In birds, the number of sperm trapped between the perivitelline membranes around the ovum is an estimate of sperm numbers present at the time and place of fertilisation in the female reproductive tract. Sperm numbers may vary among species and between eggs in a clutch and can provide information about sperm utilisation and mechanisms of sperm competition. Here, we describe patterns of variation in sperm numbers through the egg-laying sequence in three passerines in which extra-pair paternity is common, but copulation behaviour differs. Sperm numbers showed no systematic change across the laying sequence in blue tits (Cyanistes caeruleus), but decreased significantly with laying order in bluethroat (Luscinia svecica) and tree swallow (Tachycineta bicolor) clutches. This is consistent with observations that blue tits regularly copulate throughout the laying sequence, while bluethroats stop mate guarding and tree swallows reduce their copulation frequency once the first egg is laid. Nevertheless, cases of a sudden increase in sperm numbers in clutches of bluethroats and tree swallows suggest that successful inseminations also occurred after laying started. In blue tits and bluethroats, sperm numbers were not higher on extra-pair sired eggs than on eggs sired by the social male, suggesting that extra-pair copulations are not timed to the period of peak fertility for each egg. More extra-pair offspring originated from eggs laid early in the sequence in blue tits, while there was no systematic bias in bluethroats. Our results suggest that copulations during the laying sequence are predominantly performed by within-pair males in our study species.

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.

Higher in vitro resistance to oxidative stress in extra‐pair offspring

Oxidative stress is considered to act as a universal physiological constraint in life-history evolution of animals. This should be of interest for extra-pair paternity behaviour, and we tested here the prediction that offspring arising from extra-pair matings of female great tits show higher resistance to oxidative stress than within-pair offspring. Resistance to oxidative stress, measured as the whole blood resistance to a controlled free-radical attack, was significantly higher for extra-pair offspring as predicted although these were not heavier or in better body condition than within-pair offspring. Since resistance to oxidative stress has been suggested to enhance survival and reproductive rates, extra-pair offspring with superior resistance to oxidative stress, be it through maternal effects or paternal inheritance, may achieve higher fitness and thus provide significant indirect fitness benefits to their mothers. In addition, because oxidative stress affects colour signals and sperm traits, females may also gain fitness benefits by producing sons that are more attractive (sexy-sons hypothesis) and have sperm of superior quality (sexy-sperm hypothesis). Heritability of resistance to oxidative stress as well as maternal effects may both act as proximate mechanisms for the observed result. Disentangling these two mechanisms would require an experimental approach. Future long-term studies should also aim at experimentally testing whether higher resistance to oxidative stress of EP nestlings indeed translates into fitness benefits to females.