Early arrival is not associated with more extra‐pair fertilizations in a long‐distance migratory bird

When assessing the benefits of early arrival date of migratory birds, a hidden and often ignored component of males’ fitness is the higher chance of early‐arriving birds to obtain extra‐pair fertilizations. Here we investigated how extra‐pair paternity might affect the relationship between male arrival date and number of fertilizations in a model study system, the European pied flycatcher Ficedula hypoleuca. For this purpose, we sampled and genotyped breeding pairs, unpaired males and offspring (including embryos from unhatched eggs when possible) of a Dutch pied flycatcher population. Detailed information on arrival date of males, egg laying date of their social mates and nest success was also recorded. Early‐arriving males had early‐laying females and males with early‐laying females had a higher probability of siring extra‐pair eggs and obtain more fertilizations. However, male arrival date alone did not correlate with the probability to gain extra‐pair paternity and neither to the amount of fertilized eggs. Both early‐ and late‐arriving males had a higher probability of losing paternity in their own nest compared to birds with an intermediate arrival date. Finally, late‐arriving males were more likely to remain unpaired but, interestingly, a few of these birds obtained paternity via extra‐pair copulations. Because earlier arrival date did not lead to more extra‐pair fertilizations and because such relationship seems to be driven mainly by the female's laying date, we conclude that the contribution of extra‐pair paternity to the overall fitness benefits of early male arrival date is relatively small.     

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.     

No evidence that genetic compatibility drives extra‐pair behavior in female blue‐footed boobies

The function of female birds' extra‐pair (EP) behavior has remained an unresolved question in ornithology and behavioral ecology for > 30 yr. The genetic compatibility hypothesis (GCH) proposes that females benefit by acquiring biological sires that yield more heterozygous, and therefore fitter, offspring than their social mates. We used ten polymorphic microsatellite loci to test GCH predictions and its assumption that fitness increases with heterozygosity in blue‐footed boobies Sula nebouxii, a long‐lived tropical seabird. Our predictions were not supported. Heterozygosity was uncorrelated with quality indicators (fledging probability, fledgling or adult body size or mass, adult ornamentation, mean breeding success). Females were no more likely to have EP behavior or chicks when their social mates were less heterozygous or compatible, nor were EP males more heterozygous or compatible than the males they cuckolded. Finally, EP chicks were no more heterozygous than within‐pair chicks overall or in half‐sib comparisons, nor were within‐pair chicks from all‐within‐pair nests more heterozygous that those with EP nest‐mates. There are both methodological and biological explanations for these consistently negative results. Inadequate sample size is possible but unlikely, since our samples were comparable or larger than those of similar studies with significant findings. Lack of identity disequilibrium (within‐individual heterozygosity correlation) among our marker loci could be responsible, and suggests either insufficient marker coverage or lack of inbreeding, bottleneck, and/or admixture. An independent social pedigree revealed infrequent inbreeding, suggesting that pressure on females to select sires that maximize offspring heterozygosity may be genuinely lax. Alternatively, it is possible that the GCH is only upheld when selection on young is strongest; this would not be detected in our sample, which was taken during an extremely productive year. Whatever their cause, our results expand the taxonomic breadth of avian EP behavior analyses and should be considered in future evaluations of the GCH.     

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.     

Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

Extra‐pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra‐pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra‐pair and within‐pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer‐winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer‐winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra‐pair and within‐pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.     

Experimental evidence that brighter males sire more extra‐pair young in tree swallows

Across taxa, extra‐pair mating is widespread among socially monogamous species, but few studies have identified male ornamental traits associated with extra‐pair mating success, and even fewer studies have experimentally manipulated male traits to determine whether they are related directly to paternity. As a consequence, there is little experimental evidence to support the widespread hypothesis that females choose more ornamented males as extra‐pair mates. Here, we conducted an experimental study of the relationship between male plumage colour and fertilization success in tree swallows (Tachycineta bicolor), which have one of the highest levels of extra‐pair mating in birds. In this study, we experimentally dulled the bright blue plumage on the back of males (with nontoxic ink markers) early in the breeding season prior to most mating. Compared with control males, dulled males sired fewer extra‐pair young, and, as a result, fewer young overall. Among untreated males, brighter blue males also sired more extra‐pair young, and in paired comparisons, extra‐pair sires had brighter blue plumage than the within‐pair male they cuckolded. These results, together with previous work on tree swallows, suggest that extra‐pair mating behaviour is driven by benefits to both males and females.     

High frequency of extra‐pair paternity in an urban population of Cooper's Hawks

Raptors exhibit some of the highest rates of intra‐pair copulations among birds, perhaps in an attempt by males to reduce the risk of being cuckolded. Indeed, the frequency of extra‐pair fertilizations reported in studies of raptors to date is relatively low (0–11.2%). Socially monogamous Cooper's Hawks (Accipiter cooperii) exhibit one of the highest copulation rates among birds, yet there are no published accounts of extra‐pair copulations (or paternity). We studied a population of Cooper's Hawks in Milwaukee, Wisconsin, during three breeding seasons (2003, 2004, and 2007), examining the possible effects of age (1 yr old vs. ≥ 2 yr old), adult mass, and brood size on the frequency of extra‐pair paternity (EPP). We found that 19.3% of nestlings (N = 27/140) were extra‐pair young (EPY), and 34% of all broods (N = 15/44) had at least one EPY. The sires of the EPY in our study were identified for only two broods, suggesting that floater males may have engaged in extra‐pair copulations with territorial females. We found that brood size was a good predictor of the occurrence of EPP (EPP) in nests, but adult mass and female age were not. To our knowledge, these possible correlates of the occurrence of EPP in raptors had not previously been investigated. Male Cooper's Hawks provide food for females during the pre‐nesting period, and delivery of food is, in contrast to other raptor species, typically followed by copulation. Thus, one possible explanation of the relatively high rates of EPP in our study is that females might accept or even solicit extra‐pair copulations from males other than their mates as a means of maximizing energy intake for egg production. Such behavior might be particularly likely in our study area, i.e., a food‐rich urban setting with a high breeding density of Cooper's Hawks.     

Extra‐pair offspring are less heterozygous than within‐pair offspring in American redstarts Setophaga ruticilla

The vast majority of bird species are socially monogamous; however, extra‐pair paternity is nearly ubiquitous and a number of theories have been proposed to explain the prevalence of this mixed mating strategy. Here, we test the genetic compatibility hypothesis – the idea that females seek extra‐pair copulations with males whose genes are more compatible with her own. For this study, we examined eight years of paternity data (2004–2011) from a Nearctic‐Neotropical migratory bird, the American redstart Setophaga ruticilla, breeding in southeastern Ontario, Canada. We predicted that females paired with genetically similar males (higher relatedness) would be more likely to produce extra‐pair offspring and that extra‐pair offspring would have higher levels of heterozygosity than within‐pair offspring. Alternatively, because this population experiences high levels of immigration, females may produce extra‐pair offspring with more genetically similar males because of the potential for outbreeding depression. Using five highly variable microsatellite markers, we examined patterns of relatedness among social pairs as well as measures of offspring heterozygosity. In contrast to our predictions, we found no difference in relatedness between social pairs where the females produced extra‐pair offspring and social pairs where the females produced only within‐pair offspring. However, extra‐pair offspring were significantly less heterozygous than within‐pair offspring. Together, these findings suggest that females a) are not engaging in extra‐pair fertilizations based on relatedness to their social mate and b) appear to be mating with extra‐pair males that are more genetically similar to themselves. We suggest there may be benefits for females to mate with genetically similar extra‐pair males in highly outbred populations with high rates of immigration, such as for maintaining co‐adapted gene complexes or genes coding for local adaptations.     

Patterns of extra‐pair paternity in mountain chickadees

Extra‐pair paternity (EPP) is common in chickadees and often attributed to the good genes hypothesis. Females generally seek dominant males, who are typically larger, older and sing at higher rates than subordinate males, as extra‐pair sires. In other songbird species, habitat quality and urbanization have been found to influence EPP. Mountain chickadees commonly inhabit suburban habitat, and previous research on our population has shown urbanization may provide benefits to these adaptable songbirds. Here, we ask how individual condition and urbanization influence rates of EPP in mountain chickadees. Over three breeding seasons, we monitored mountain chickadee nests in urban and rural habitat, and determined parentage by genotyping adults and nestlings at six microsatellite loci. Extra‐pair paternity is common in mountain chickadees, with extra‐pair offspring (EPO) in 43.2% of nests and accounting for 17.9% of offspring. We found tenuous support for the good genes hypothesis with females tending to engage in EPCs with older males. However, we did not find an influence of male or female condition on the proportion of EPO in a nest. In addition, we did not find a significant effect of habitat on EPP rates, suggesting the impacts of urbanization on mountain chickadee reproduction may not extend to altering extra‐pair behaviour.     

MHC‐dependent survival in a wild population: evidence for hidden genetic benefits gained through extra‐pair fertilizations

Females should prefer to be fertilized by males that increase the genetic quality of their offspring. In vertebrates, genes of the major histocompatibility complex (MHC) play a key role in the acquired immune response and have been shown to affect mating preferences. They are therefore important candidates for the link between mate choice and indirect genetic benefits. Higher MHC diversity may be advantageous because this allows a wider range of pathogens to be detected and combated. Furthermore, individuals harbouring rare MHC alleles might better resist pathogen variants that have evolved to evade common MHC alleles. In the Seychelles warbler, females paired with low MHC‐diversity males elevate the MHC diversity of their offspring to levels comparable to the population mean by gaining extra‐pair fertilizations. Here, we investigate whether increased MHC diversity results in higher life expectancy and whether there are any additional benefits of extra‐pair fertilizations. Our 10‐year study found a positive association between MHC diversity and juvenile survival, but no additional survival advantage of extra‐pair fertilizations. In addition, offspring with a specific allele (Ase‐ua4) had a fivefold longer life expectancy than offspring without this allele. Consequently, the interacting effects of sexual selection and pathogen‐mediated viability selection appear to be important for maintaining MHC variation in the Seychelles warbler. Our study supports the prediction that MHC‐dependent extra‐pair fertilizations result in genetic benefits for offspring in natural populations. However, such genetic benefits might be hidden and not necessarily apparent in the widely used fitness comparison of extra‐ and within‐pair offspring.     

Female collared flycatchers choose neighbouring and older extra‐pair partners from the pool of males around their nests

Extra‐pair copulation is common among passerine birds. Females might engage in this behavior to obtain direct or indirect benefits. They may choose extra‐pair males with larger ornaments, especially if they are costly to produce. Here we studied extra‐pair paternity in the collared flycatcher. Genetic analysis allowed us to identify the presence or absence of extra‐pair young in the focal nests, and to identify extra‐pair fathers. We also identified potential males available as extra‐pair sires around the nests of females who had extra‐pair young. First, we tested the relationship between paternity in own nest and ornament size (wing patch and/or forehead patch), morphological traits and age of social males and females. Second, we compared the same suite of traits among social mates, extra‐pair males and all potential extra‐pair mates. Finally, we investigated the effect of the size of ornaments on the distance between the social nest and that of nest the extra‐pair father. Contrary to our prediction, males with larger ornaments and longer wings lost more paternity in their nests. We also found that early breeders lost less paternity in their nests. Extra‐pair males were older and had longer wings than social and potential extra‐pair males. Females mainly obtained extra‐pair mates near their nests but the distance did not vary according to ornamentation. These results could potentially be explained by differences in mate guarding strategy as older males may be more experienced in guarding their mate and attract other females more easily. More data about mate guarding and prospecting are needed to increase our understanding of mechanisms underlying the extra‐pair paternity in birds.     

High rates of extra‐pair paternity in a socially monogamous beetle with biparental care

1. Nest construction and paternity assurance are predicted to favour biparental care in insects. The horned passalus (Odontotaenius disjunctus) is a socially monogamous beetle with biparental care that breeds in decaying logs. The genetic mating system of the horned passalus was investigated to determine if paternity assurance is likely to drive the evolution or maintenance of paternal care in this system. Parental time budgets were also examined to better understand the types and frequencies of behaviours performed by parents. 2. Genotyping‐by‐sequencing revealed high levels of extra‐pair paternity, with 54.8% of offspring sired by extra‐pair males and 70% of nests containing extra‐pair young. 3. More heterozygous social males were cuckolded less than more homozygous social males. Extra‐pair mating, however, seems unlikely to increase offspring genetic diversity as extra‐pair offspring were not more heterozygous than within‐pair offspring, and average brood heterozygosity did not increase with higher rates of extra‐pair paternity. 4. Behavioural observations demonstrated that parents spent on average 46.5% of their time processing the decaying wood resource for larval offspring. Because resource processing is a by‐product of feeding and provides shareable benefits for all larvae in the brood, this form of paternal care could be favoured despite low paternity.     

Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Rates of extra‐pair paternity (EPP) have frequently been associated with genetic relatedness between social mates in socially monogamous birds. However, evidence is limited in mammals. Here, we investigate whether dominant females use divorce or extra‐pair paternity as a strategy to avoid the negative effects of inbreeding when paired with a related male in meerkats Suricata suricatta, a species where inbreeding depression is evident for several traits. We show that dominant breeding pairs seldom divorce, but that rates of EPP are associated with genetic similarity between mates. Although extra‐pair males are no more distantly related to the female than social males, they are more heterozygous. Nevertheless, extra‐pair pups are not more heterozygous than within‐pair pups. Whether females benefit from EPP in terms of increased fitness of the offspring, such as enhanced survival or growth, requires further investigations.     

Extra‐pair paternity in relation to breeding synchrony in ground tits: an individual‐based approach

Previous studies thought that at the within‐population level, whether a female bird engages in extra‐pair (EP) mating depends on how synchronous she is in breeding time with all other females around her, presumably the synchronization might affect the female's opportunities to meet potential EP sires who socially pair with these other females. However, when females or males are choosy about EP partners and mate with one EP individual only, the probability of EP mating may be most influenced by breeding synchrony between the EP partners. In such a case, the ‘individual‐level’ synchrony should act to determine EP mating success. We test this idea in a socially monogamous passerine, the ground tit Parus humilis. Fifty‐five out of 172 sampled females produced 122 EP offspring, each mating with one EP sire in most cases (92%), usually her intermediately‐related kin. As expected, the broader‐scale synchrony did not predict the probability of EP paternity but the individual‐level did, for females having EP offspring bred more synchronously with their EP than with their nearest neighbors, and females without EP offspring were least synchronous with their nearest neighbors. We argue that this kind of individual‐based approaches will shine light on the synchrony‐EP mating relationship in birds.     

Male age and its association with reproductive traits in captive and wild house sparrows

Evolutionary theory predicts that females seek extra‐pair fertilizations from high‐quality males. In socially monogamous bird species, it is often old males that are most successful in extra‐pair fertilizations. Adaptive models of female extra‐pair mate choice suggest that old males may produce offspring of higher genetic quality than young males because they have proven their survivability. However, old males are also more likely to show signs of reproductive senescence, such as reduced sperm quality. To better understand why old males account for a disproportionally large number of extra‐pair offspring and what the consequences of mating with old males are, we compared several sperm traits of both captive and wild house sparrows, Passer domesticus. Sperm morphological traits and cloacal protuberance volume (a proxy for sperm load) of old and young males did not differ substantially. However, old males delivered almost three times more sperm to the female's egg than young males. We discuss the possibility of a post‐copulatory advantage for old over young males and the consequences for females mated with old males.     

Age‐dependent trajectories differ between within‐pair and extra‐pair paternity success

Reproductive success is associated with age in many taxa, increasing in early life followed by reproductive senescence. In socially monogamous but genetically polygamous species, this generates the interesting possibility of differential trajectories of within‐pair and extra‐pair siring success with age in males. We investigate these relationships simultaneously using within‐individual analyses with 13 years of data from an insular house sparrow (Passer domesticus) population. As expected, we found that both within‐ and extra‐pair paternity success increased with age, followed by a senescence‐like decline. However, the age trajectories of within‐ and extra‐pair paternity successes differed significantly, with the extra‐pair paternity success increasing faster, although not significantly, in early life, and showing a delayed decline by 1.5 years on average later in life compared to within‐pair paternity success. These different trajectories indicate that the two alternative mating tactics should have age‐dependent pay‐offs. Males may partition their reproductive effort between within‐ and extra‐pair matings depending on their current age to reap the maximal combined benefit from both strategies. The interplay between these mating strategies and age‐specific mortality may explain the variation in rates of extra‐pair paternity observed within and between species.     

Extra‐group mating increases inbreeding risk in a cooperatively breeding bird

In many cooperatively breeding species, females mate extra‐group, the adaptive value of which remains poorly understood. One hypothesis posits that females employ extra‐group mating to access mates whose genotypes are more dissimilar to their own than their social mates, so as to increase offspring heterozygosity. We test this hypothesis using life history and genetic data from 36 cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali) groups. Contrary to prediction, a dominant female's relatedness to her social mate did not drive extra‐group mating decisions and, moreover, extra‐group mating females were significantly more related to their extra‐group sires than their social mates. Instead, dominant females were substantially more likely to mate extra‐group when paired to a dominant male of low heterozygosity, and their extra‐group mates (typically dominants themselves) were significantly more heterozygous than the males they cuckolded. The combined effects of mating with extra‐group males of closer relatedness, but higher heterozygosity resulted in extra‐group‐sired offspring that were no more heterozygous than their within‐group‐sired half‐siblings. Our findings are consistent with a role for male–male competition in driving extra‐group mating and suggest that the local kin structure typical of cooperative breeders could counter potential benefits to females of mating extra‐group by exposing them to a risk of inbreeding.     

Lack of evidence for improved immune response of extra‐pair nestlings in collared flycatcher Ficedula albicollis

Extra‐pair paternity is common in many socially monogamous bird species. Increasing evidence suggests that extra‐pair copulations are female‐driven, but benefits for females mating outside social pair‐bonds are still poorly understood. The most influential explanation, “good genes” hypothesis, states that females mated socially with low quality males, engage in extra‐pair copulations to obtain genetic benefits for their progeny. According to this model, enhanced performance of extra‐pair offspring is expected. Here, based on 4‐year study of collared flycatcher Ficedula albicollis, we compared the condition of extra‐pair and within‐pair young. We found no difference in immune response and body size between maternal half‐siblings raised in the same nests. Additionally sex ratio was not biased among extra‐pair nestlings, and paternity was not associated with hatching rank. Our results failed to reveal “good genes” effects in the studied population. These effects might be hard to detect, but other hypotheses should also be studied more thoroughly in the future.     

Malaria infection status predicts extra‐pair paternity in the blue tit

Extra‐pair matings comprise a common reproductive strategy among socially monogamous bird species. However, it remains unclear why females decide to mate with extra‐pair males. Indirect benefits in terms of improving offspring genetic quality are usually invoked to explain this phenomenon. Parasite resistance genes are often considered as a female target of seeking extra‐pair matings, but the direct test of this hypothesis is generally lacking. Here, we report on a relationship between the status of infection with malaria parasites (Plasmodium and Haemoproteus) and occurrence of extra‐pair paternity in a wild population of the blue tit Cyanistes caeruleus inhabiting Gotland (Sweden). We found that the probability of extra‐pair paternity is significantly related to the infection status of social parents. Infected males showed higher probability of being cuckolded than uninfected ones. However, this was observed only among males mated to uninfected females. Thus, avian malaria may potentially contribute to explanation of extra‐pair mating behaviour.     

True deception during extra‐pair courtship feeding: cheating whiskered tern Chlidonias hybrida females perform better

Males of many bird species feed their mates during the pre‐incubation period. The food provisioned by males during these courtship feedings (CFs) represents the key source of energy for the female during egg formation. Non‐pair males may trade food for extra pair copulations (EPC) with females during extra pair courtship feeding (EPCF), while females may trade copulations for food with non‐pair males to obtain additional resources. Because EPCs can be costly to the females, they are expected to behave in ways that will deceive non‐pair males to obtain additional resources at no cost to themselves. We investigated EPCFs in whiskered terns Chlidonias hybrida breeding in food‐rich conditions, on carp ponds in southern Poland. Almost all CFs (n = 2751) took place during the female's fertile period and peaked just before clutch initiation. 10% of all CFs were performed by non‐pair males. Females tried to obtain food from the non‐pair male during 39% of EPCFs, by swindling (the female solicits a non‐social male for copulation and tries to swindle food with no cloacal contact) or by snatching (the female tries to take the gift without engaging in copulation). In the remaining 61% of EPCFs, females did not react or chased the visiting male away. The probability of a female's obtaining food during EPCF was much higher (0.69, 95% CI: 0.47–0.85) if she swindled rather than snatched (0.08, 95% CI: 0.02–0.22). Only 0.7% of EPCFs were followed by EPCs. The high availability of food in the study area allows males to perform frequent EPCFs, despite the very low probability of obtaining EPCs. This is the first time that ‘true deception’ during EPCFs has been reported in birds: swindling females obtain food from non‐pair males at no immediate detectable cost to themselves.