Extra-pair Sires Research Articles

Removal of older males increases extra-pair siring success of yearling males.

In animals, reproductive performance typically improves over time early in life. Several ultimate and proximate mechanisms may contribute to such an age-related improvement and these mechanisms can act in a relative or in an absolute sense. Low performance of young individuals may be the consequence of a comparison or competition with older individuals (relative), or it may be due to specific traits of young individuals and be unrelated to the presence of older competitors (absolute). Here, we perform a test to disentangle whether the effect of age class (yearling or older) on male extra-pair siring success is relative or absolute. Male age is the most consistent predictor of male extra-pair siring success across bird species, yet the mechanisms underlying this pattern are not well understood. Low extra-pair siring success of yearling males may be a consequence of the presence of older ("adult") males (hypothesis 1), because adult males are more successful in intra- and intersexual interactions or because females prefer to copulate with adult males when available (relative preference). Alternatively, low extra-pair siring success of yearlings may be independent of the presence of adult males (hypothesis 2), for example, if yearling males on average invest less in extra-pair behavior or if females avoid them as extra-pair mates, independent of the availability of older males (absolute preference). To distinguish between these 2 hypotheses, we experimentally manipulated the age structure of a nest-box-breeding population of blue tits (Cyanistes caeruleus) by removing almost all adult males, and compared patterns of extra-pair paternity in the experimental year with those from the preceding 15 "control" years. Removal of adult males resulted in a substantial increase in the extra-pair siring success of yearling males compared to the "control" years, but did not affect the population-level frequency of extra-pair paternity or its spatial patterns. Our results provide clear evidence that extra-pair siring success of yearlings can increase and that it depends on the presence of older males in the population, indicating a relative effect of age on reproductive performance. These results suggest that older males outcompete yearling males in direct or indirect interactions, in sperm competition or as a result of differences in attractiveness to females.

Age trajectories in extra-pair siring success suggest an effect of maturation or early-life experience.

Across birds, male age is the most consistent predictor of extra-pair siring success, yet little is known about age effects on paternity over the lifetime of individuals. Here, we use data from a 13-year study of a population of blue tits (Cyanistes caeruleus) to investigate how extra-pair siring success changes with age within individuals. Our results indicate that extra-pair siring success does not continuously increase with male age. Instead, siring success was related to male age in a threshold fashion, whereby yearling males were less likely to gain paternity than older males. This effect was independent of the age of the social partner, but influenced by the age of the extra-pair female: success of yearlings at siring extra-pair young (EPY) with older females was even lower. Among males that sired at least one EPY, the number of extra-pair mates and the proportion of EPY sired were unrelated to male age. We found no evidence for an influence of selective disappearance on extra-pair reproduction. Senescence, if anything, only occurs at ages blue tits rarely reach. A literature review indicates that an effect of male age on extra-pair siring success may be limited to the switch from yearling to older in many species. Thus, the generally observed age effect on male extra-pair siring success may be linked to age class rather than continuous ageing. This suggests that lack of experience or not fully completed maturation are important drivers of age patterns in extra-pair paternity.

Experimentally advancing morning emergence time does not increase extra-pair siring success in blue tit males.

Extra-pair paternity occurs frequently in socially monogamous birds, but there is substantial variation in extra-pair siring success among males. Several studies have shown that siring success relates to the timing of morning activity, with the earliest active males being more successful, suggesting that early activity is important for acquiring extra-pair copulations. However, these studies are correlational, and it, therefore, remains unclear whether the relationship between timing and extra-pair siring success is causal. An alternative explanation is that successful extra-pair sires tend to be active earlier (e.g., because they are of high quality or in good condition), but that early activity in itself does not increase siring success. We experimentally advanced the emergence time of male blue tits by exposing them to light about half an hour before their natural emergence time. Although males that were exposed to the light treatment emerged from their roost substantially earlier than males that were exposed to a control treatment, light-treated males were not more likely to sire extra-pair offspring. Furthermore, whereas control males showed the expected relation between emergence time and siring success (although not statistically significant), there was no relation between emergence time and extra-pair siring success among light-treated males. Our results suggest that the timing of emergence from the roost is not an important factor underlying extra-pair siring success.

Start and end of daily activity predict extrapair siring success independently of age in male blue tits

Start and end of daily activity predict extrapair siring success independently of age in male blue tits

Extra-pair paternity explains cooperation in a bird species

In many social animals, females mate with multiple males, but the adaptive value of female extra-pair mating is not fully understood. Here, we tested whether male pied flycatchers (Ficedula hypoleuca) engaging in extra-pair copulations with neighboring females were more likely to assist their neighbors in antipredator defense. We found that extra-pair sires joined predator-mobbing more often, approached predators more closely, and attacked predators more aggressively than males without extra-pair offspring in the neighboring nest. Extra-pair mating may incentivize males to assist in nest defense because of the benefits that this cooperative behavior has on their total offspring production. For females, this mating strategy may help recruit more males to join in antipredator defense, offering better protection and ultimately improving reproductive success. Our results suggest a simple mechanism by which extra-pair mating can improve reproductive success in breeding birds. In summary, males siring extra-pair offspring in neighboring nests assist neighbors in antipredator defense more often than males without extra-pair offspring.

Mate choice for major histocompatibility complex (MHC) complementarity in the Yellow-rumped Flycatcher (Ficedula zanthopygia)

BackgroundGenes of the major histocompatibility complex (MHC) are an important component of the vertebrate immune system and play a significant role in mate choice in animal populations. However, the MHC genetic targets of female mate choice have not been clearly identified, and whether female mate choice is based on neutral genetic characteristics remains an open question. Here, we focus on the effects of morphological traits and genetic similarity among individuals in MHC class IIB (MHC IIB) exon 2 on mating in a sexually dimorphic songbird that exhibits social monogamy with extra-pair paternity (EPP).MethodsWe sequenced 64 parent–offspring triads sampled over a 3-year period using two MHC class II loci to detect disassortative mating in the Yellow-rumped Flycatcher (Ficedula zanthopygia).ResultsWe found that MHC similarity in social pairs was lower than that in random pairs. Extra-pair mate choice according to MHC IIB was observed, in which females’ extra-pair mates had fewer MHC alleles than their within-pair mates, but there was no significant band-sharing between extra-pair sires and potential extra-pair mates. However, the interaction between the MHC diversity of females and that of the social males affected the occurrence of EPP.ConclusionsOur results support the “optimality hypothesis” of MHC-based social and extra-pair choice. Female choice probably maintains a certain level of MHC diversity in offspring in the Yellow-rumped Flycatcher.

Analysis of within-individual variation in extrapair paternity in blue tits (Cyanistes caeruleus) shows low repeatability and little effect of changes in neighborhood.

Many studies investigated variation in the frequency of extrapair paternity (EPP) among individuals. However, our understanding of within-individual variation in EPP remains limited. Here, we comprehensively investigate variation in EPP at the within-individual level in a population of blue tits (Cyanistes caeruleus). Our study is based on parentage data comprising >10 000 genotyped offspring across 11 breeding seasons. First, we examined the repeatability of the occurrence of EPP, the number of extrapair offspring, the number of extrapair partners, and the occurrence of paternity loss using data from males and females that bred in multiple years. Second, we tested whether within-individual changes in EPP between breeding seasons relate to between-year changes in the local social environment. Repeatabilities were generally low but significant for the occurrence and number of extrapair young in females and for whether a male sired extrapair young or not. We found no evidence that the presence of the former social partner or changes in the proportion of familiar individuals or in phenotypic traits of the neighbors influenced changes in levels of EPP in females. However, in adult males, a decrease in the average body size of male neighbors was associated with higher extrapair siring success. If confirmed, this result suggests that the competitive ability of a male relative to its neighbors influences his extrapair mating success. We suggest that alternative hypotheses, including the idea that within-individual changes in EPP are due to “chance events” rather than changes in an individual’s social breeding environment, deserve more consideration.

Common Field Data Limitations Can Substantially Bias Sexual Selection Metrics.

Sexual selection studies widely estimate several metrics, but values may be inaccurate because standard field methods for studying wild populations produce limited data (e.g., incomplete sampling, inability to observe copulations directly). We compared four selection metrics (Bateman gradient, opportunity for sexual selection, opportunity for selection, and ) estimated with simulated complete and simulated limited data for 15 socially monogamous songbird species with extrapair paternity (4%-54% extrapair offspring). Inferring copulation success from offspring parentage creates nonindependence between these variables and systematically underestimates copulation success. We found that this introduces substantial bias for the Bateman gradient, opportunity for sexual selection, and . Notably, 47.5% of detected Bateman gradients were significantly positive for females, suggesting selection on females to copulate with multiple males, although the true Bateman gradient was zero. Bias generally increased with the extent of other sources of data limitations tested (nest predation, male infertility, and unsampled floater males). Incomplete offspring sampling introduced bias for all of the metrics except the Bateman gradient, while incomplete sampling of extrapair sires did not introduce additional bias when sires were a random subset of breeding males. Overall, our findings demonstrate how biases due to field data limitations can strongly impact the study of sexual selection.

Winter associations predict social and extra-pair mating patterns in a wild songbird.

Despite decades of research, our understanding of the underlying causes of within-population variation in patterns of extra-pair paternity (EPP) remains limited. Previous studies have shown that extra-pair mating decisions are linked to both individual traits and ecological factors. Here, we examine whether social associations among individuals prior to breeding also shape mating patterns, specifically the occurrence of EPP, in a small songbird, the blue tit. We test whether associations during the non-breeding period predict (1) future social pairs, (2) breeding proximity (i.e. the distance between breeding individuals) and (3) the likelihood that individuals have extra-pair young together. Individuals that were more strongly associated (those that foraged more often together) during winter tended to nest closer together. This, by itself, predicts EPP patterns, because most extra-pair sires are close neighbours. However, even after controlling for spatial effects, female–male dyads with stronger social associations prior to breeding were more likely to have extra-pair young. Our findings reveal a carry-over from social associations into future mating decisions. Quantifying the long-term social environment of individuals and studying its dynamics is a promising approach to enhance our understanding of the process of (extra-)pair formation.

Male-only care and cuckoldry in black coucals: does parenting hamper sex life?

Providing parental care often reduces additional mating opportunities. Paternal care becomes easier to understand if trade-offs between mating and caring remain mild. The black coucal Centropus grillii combines male-only parental care with 50% of all broods containing young sired by another male. To understand how much caring for offspring reduces a male's chance to sire additional young in other males' nests, we matched the production of extra-pair young in each nest with the periods during which potential extra-pair sires were either caring for offspring themselves or when they had no own offspring to care for. We found that males which cared for a clutch were not fully excluded from the pool of competitors for siring young in other males' nests. Instead, the relative siring success showed a temporary dip. Males were approximately 17% less likely to sire young in other males' nests while they were incubating, about 48% less likely to do so while feeding nestlings, followed by 26% when feeding fledglings, compared to the success of males that currently did not care for offspring. These results suggest that real-life care situations by males may involve trade-off structures that differ from, and are less strict than those frequently employed in theoretical considerations of operational sex ratios, sex roles and parenting decisions.

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 13years 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 1.5years 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.

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.

Effects of load-lightening and delayed extrapair benefits on the fitness consequences of helping behavior.

In most cooperative breeders, helping is directed at close kin, allowing helpers to gain indirect fitness benefits by increasing the reproductive success of close relatives, usually their parents. Extrapair paternity (EPP) occurs at high rates in some cooperative breeders, reducing the relatedness of helpers to the young they help raise. Even so, a son that helps is related to the brood by at least 0.25 through his mother and to within-pair young by 0.5, whereas a potential helper that has EPP in his own nest is related only to the offspring he sires and unrelated to any extrapair offspring. In birds, EPP often favors older males, which in the extreme case can result in sons being more closely related to young in their parents' nest than to young in their own nests. The fitness benefit of helping will thus be enhanced if helping lightens the workload and increases survival of helpers and their fathers, enabling them to become old, hyper-successful extrapair sires. Here, we develop and analyze a proof-of-concept model, grounded in the western bluebird (Sialia mexicana) system, demonstrating the conditions under which high population levels of EPP can generate inclusive fitness benefits of helping behavior that outweigh the costs. This model provides a new perspective on the relationship between EPP and helping behavior in cooperative breeders and suggests a strong need for empirical work to gather unprecedented data on paternity over the lifetime of helpers and their parents.

Timing of extrapair fertilizations: within-pair fertilization trade-offs or pair synchrony spillovers?

In socially monogamous species, male fertilization-related behaviors are expected to be tuned to the fertile cycle of their social female. How a male adjusts his fertilization-related behaviors to his social mate's fertile period is relatively well understood. However, the influence of the social mate's fertility stage on a male's extrapair siring success remains poorly studied. In this study, we tested 2 alternative hypotheses about how a male's extrapair siring success may vary in relation to his social mate's fertile cycle. The tradeoff avoidance hypothesis posits that males engage in extrapair fertilization-related behaviors when their social female is not fertile to avoid a potential trade-off between within-pair and extrapair reproduction. Alternatively, the pair synchrony hypothesis postulates that males are more likely to sire extrapair offspring when their social mate is fertile because male investment in fertilization- related behaviors during their social mate's fertile period aimed at increasing within-pair siring success will have positive spillover effects on their extrapair siring success. To assess the support for each of these 2 hypotheses, we studied a population of great tits (Parus major) for 4 consecutive years in 12 nest-box plots and quantified each male's extrapair siring success before, during, and after the fertile period of his social mate. After correcting for variation in the availability of fertile females, males gained more extrapair paternity during the fertile period of their social mate, supporting the pair synchrony hypothesis.

Increased extra-pair paternity in broods of aging males and enhanced recruitment of extra-pair young in a migratory bird.

Despite keen interest in extra-pair mating in birds, its adaptive significance remains unresolved. Here, we use a multi-year dataset to test whether traits of a female's social mate influence her propensity to produce extra-pair offspring in a population of house wrens, and whether producing extra-pair young has consequences for a female's fitness through effects on offspring survival. Females were most likely to produce extra-pair offspring when paired with old males and when paired with males on poor-quality territories, although this latter effect was marginally nonsignificant. Among offspring, the cutaneous immunity of within-pair young decreased as the age of their sires increased, but cutaneous immunity of extra-pair young was not affected by the age of their extra-pair sires or by the age of the males rearing them. Extra-pair offspring were more likely than within-pair offspring to return as breeding adults to the local population, with extra-pair sons being more likely to return as a breeder for multiple years. Our findings support the hypothesis that females produce extra-pair offspring to enhance their inclusive fitness beyond what they are capable of given the male with which they are socially paired.

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.

Extra-Pair Paternity Declines with Female Age and Wing Length in the Pied Flycatcher

Despite many studies of how male characteristics affect paternity in predominantly monogamous birds, relatively little attention has been given to the traits of females that may influence extra-pair paternity (EPP). However, the occurrence of EPP may be the result of behavioural interactions in which both male and female traits are important for determining the outcome. If EPP is driven mainly by female choice of extra-pair sires, older, more experienced or larger females would be better able to evade mate guarding tactics and more capable of selecting extra-pair mates and resisting unwanted suitors. This would be especially noticeable in females paired with unattractive mates. On the other hand, if EPP is driven mainly by male pursuit, we should expect that young, inexperienced or small females would be more exposed to coercive male approaches independently of social mate traits. In a study of an Iberian population of the pied flycatcher Ficedula hypoleuca, we found that EPP affected 38% of the broods and 17% of the nestlings. These values are relatively high, allowing a relatively large number of affected within-pair mates to be included. We found that EPP is related to both female and male traits although not to any interaction between male and female traits. EPP was higher at nests tended by both younger and short-winged females and by browner males. Older females may be more experienced and dominant while long-winged females may be faster fliers, these traits enabling them to avoid extra-pair copulations, while brown males are less aggressive towards male intruders. In our study population, EPP appears to be caused by male pursuit, which in some cases may overwhelm female attempts to avoid extra-pair copulations and their social partner's ability to prevent them.

Extra-pair mating and evolution of cooperative neighbourhoods.

A striking but unexplained pattern in biology is the promiscuous mating behaviour in socially monogamous species. Although females commonly solicit extra-pair copulations, the adaptive reason has remained elusive. We use evolutionary modelling of breeding ecology to show that females benefit because extra-pair paternity incentivizes males to shift focus from a single brood towards the entire neighbourhood, as they are likely to have offspring there. Male-male cooperation towards public goods and dear enemy effects of reduced territorial aggression evolve from selfish interests, and lead to safer and more productive neighbourhoods. The mechanism provides adaptive explanations for the common empirical observations that females engage in extra-pair copulations, that neighbours dominate as extra-pair sires, and that extra-pair mating correlates with predation mortality and breeding density. The models predict cooperative behaviours at breeding sites where males cooperate more towards public goods than females. Where maternity certainty makes females care for offspring at home, paternity uncertainty and a potential for offspring in several broods make males invest in communal benefits and public goods. The models further predict that benefits of extra-pair mating affect whole nests or neighbourhoods, and that cuckolding males are often cuckolded themselves. Derived from ecological mechanisms, these new perspectives point towards the evolution of sociality in birds, with relevance also for mammals and primates including humans.

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.

Extra-pair mating and sexual selection on male traits across populations

Research on sexually selected male traits has intensified over the last two decades and there are now many species of birds for which male traits associated with extra-pair mating success have been identified. Some of the more commonly studied species have been examined in multiple populations; however, there is often little consistency in results between studies. In paired analyses of Tree Swallows breeding in Wisconsin, we found that successful extra-pair sires were more experienced breeders, heavier, had fewer lice holes in their feathers, had longer wings and tended to be in better condition than the male they cuckolded. Our results are similar to those from a population of Tree Swallows studied in Ontario but differ from a population studied in British Columbia. Such variation among populations may arise if environmental heterogeneity influences the information content, reliability, or importance of particular male traits as signals of male quality. Taking these factors into consideration will help us understand how selection on male traits varies between populations and the role of extra-pair mating in sexual selection.