Extra-pair Males Research Articles

Genetic benefits of female from extra-pair paternity are context dependent within the socially monogamous Tree Sparrow

Females actively seek extra-pair paternity (EPP) to acquire a fitness advantage for their offspring. The “context-dependence hypothesis” posits that female extra-pair mate choice has plasticity in response to environmental conditions, and therefore magnitude of female genetic benefits from EPP depends on the environmental variation. Furthermore, chronic heavy metal pollution can cause adverse effects on fitness-related traits of wild birds. However, few studies were available on the interactions between heavy metal pollution and EPP. We selected an area that was contaminated by heavy metals for more than 60 years (Baiyin, BY), a relatively unpolluted area (Liujiaxia, LJX), and Tree Sparrows (Passer montanus) as study species to explore the response of female extra-pair mate choice and genetic benefits from EPP to heavy metal pollution in socially monogamous birds. The relatedness between social mates and extra-pair mates was investigated. Additionally, we compared the body size and heterozygosity of extra-pair offspring (EPO), within-pair offspring (WPO), social males and extra-pair males from the two Tree Sparrow populations. We found that at BY, female Tree Sparrows tended to choose extra-pair males with larger body size and lower genetic similarity, thereby producing higher heterozygosity and larger body size of EPO compared with those of WPO. However, no similar phenomenon was observed in the Tree Sparrow population from LJX. In addition, there was a significant interaction between population and paternity in the analyses of the fitness-related traits, suggesting that environmental variation could affect female genetic benefits from EPP. This study confirmed the existence of presumed interactions between environmental pollution and EPP within the natural population of socially monogamous Tree Sparrows. Our findings shed lights on the possible effects of long-term environmental stress on mating system in wild birds.

Low level of extra-pair paternity in an urban population of blackbirds

We studied extra-pair paternity in a socially monogamous bird, the European Blackbird (Turdus merula). The research was conducted in an urban park in Poland. We obtained genetic samples from 36 broods (123 nestlings) of 21 unique pairs. The proportion of broods with some extra-pair nestlings was 17.1% (6 broods), and overall, 13.1% (16 nestlings) of all nestlings were sired by extra-pair males. In one brood (2.8% of all the investigated broods), we found one egg laid by a female which did not have her own territory in the study area (brood parasitism). These figures are relatively low compared to other closely related passerines. We suggest that mate guarding in the studied population may effectively prevent females from engaging in extra-pair activity, and in the case of females, divorce and serial polygamy are better strategies for enhancing the genetic quality and genetic diversity of their offspring than infidelity.

Do female bluethroats without extra-pair offspring have more MHC-compatible social mates?

Genes of the major histocompatibility complex (MHC) are crucial for adaptive immunity in jawed vertebrates, and theory predicts that there should be mate choice for optimizing MHC constitution in the offspring. In a previous study, we demonstrated a non-random female choice of extra-pair males in the bluethroat (Luscinia svecica), yielding offspring that was closer to an intermediate MHC class II (MHCII) allele count than their within-pair halfsiblings. The present study tests whether social pairs with only within-pair young (WPY) in their brood, in the same study population, had a combined MHC-constitution closer to a presumed intermediate optimum, than social pairs with extra-pair young (EPY), with a corresponding pattern in their offspring. As expected, we found that WPY from pure WPY-broods were more MHC-optimal than WPY from mixed broods, but only in broods of young (second year) males. Correspondingly, there was a tendency for social pairs with only WPY in their brood to be more MHC-compatible than social pairs with EPY in their brood, when the male was young. Older bluethroat males have considerably larger testes than young males, and their higher sperm competitiveness could help them secure paternity in their own brood, also when they are not MHC-compatible. In other words, in the sexual conflict over paternity, females may be more likely to realise their preference for a MHC-compatible mate when paired to a young male. As a possible fitness indicator, immune responsiveness to an injected antigen (PHA) was elevated for offspring closer to “the golden mean” in MHCII allele count.Significance statementThis study contributes to our understanding of MHC-based mate choice in extra-pair mating systems, by showing that female bluethroats (Luscinia svecica) with an MHCII-compatible social mate tend to have no extra-pair young in their brood, but only when the social male is young. This elucidates a possible sexual conflict, in which older social males are able to override female preferences and prevent other males from gaining paternity in their brood through higher sperm production. Studying systems in which extra-pair paternity occurs offers an insight into the genetic benefits of mate choice, as extra-pair males, in contrast to social males, generally contribute only sperm. Further, the strict and thorough genotyping scheme applied in this study enabled us to demonstrate a preference for “the golden mean” in MHC-diversity in a species with one of the highest MHC class II-diversity known to date.

A high level of extra-pair paternity in the Chestnut Thrush (Turdus rubrocanus)

Extra-pair copulation (EPC) can potentially maximize individual reproductive fitness, and this process may involve sexual selection of male and female traits that reflect individual quality. Previous studies have implied that adult characteristics are associated with the probability of extra-pair paternity (EPP), but it differs between species. Moreover, there are relatively few examples of the adaptive rationale for females’ engagement in EPCs based on an examination of these more traditionally recorded traits, in combination with female flight-mediated traits such as wing length. We investigated whether EPP existed in the wild Chestnut Thrush (Turdus rubrocanus) population during three breeding seasons (2019–2021), and whether paternity was related to morphological traits of males and females. Eight highly variable microsatellite loci were used to identify paternity, and generalized linear mixed models were used to analyze the relationship between paternity and morphological traits. We found that EPP existed in the Chestnut Thrush. 53.3% (N ​= ​41/77) of the broods contained at least one extra-pair offspring (EPO), and 34.6% (N ​= ​72/208) of the nestlings were EPO. We also found that male wing length was negatively associated with the probability of EPP and the proportion of EPO. Female body length was positively related to the probability of EPP. Both female body condition and mass were negatively associated with the proportion of EPO. While other traits of male and female did not relate to the probability of EPP or the proportion of EPO. Extra-pair males had better body condition compared to the males they cuckolded. EPO did not differ from their half-siblings in terms of body size or body condition. The results suggest that body size and body condition were associated with EPP in the Chestnut Thrush. This study provides fundamental information for further studies on the evolution and maintenance of EPP in the Chestnut Thrush, and it is also useful for the comparison of EPP among Turdus species.

Male aggressiveness during the female fertile phase in relation to extra-pair paternity, plumage ornaments and female traits

In many bird species, physical aggression between males become more frequent during the female’s fertile period, as female encounters with extra-pair males are more frequent and can entail paternity losses. Male aggressiveness during this stage has been proposed as crucial for ensuring male reproductive success. Thus, plumage ornaments could represent honest signals of individual quality that could reflect the aggressiveness of paired territorial males. Furthermore, male aggressiveness could be related to mate quality or defensive capacity. We quantified extra-pair paternity in the broods and investigated the association of male and female traits with the aggressive behaviour of territorial paired males in a Spanish population of Pied Flycatchers (Ficedula hypoleuca), where territorial intrusions were simulated during the female fertile period by placing a taxidermic male mount close to the nest. We predicted that (1) more aggressive males should better protect their mates from intruding males and thereby reduce their paternity losses, (2) males with larger white patches and higher UV reflectance of wing patches should respond more strongly to intrusions, and (3) that males should be more aggressive when mated with higher quality females. We found evidence that males that responded less intensely to a territorial intrusion suffered a higher paternity loss, which offers strong support to the basic tenet of the theory of territoriality as paternity defence. Moreover, both the level of male aggressiveness and control of the territory increased with male UV reflectance of wing patches. Finally, we found, contrary to our prediction, that males were less aggressive when mated with more ornamented females.

Combined roles for breeding synchrony, habitat and scale as predictors of extrapair paternity

Despite extensive research on passerine reproduction, it remains difficult to predict which traits of individuals, nesting populations and landscapes drive extrapair paternity (EPP). Two broad categories of drivers, habitat structure and population level factors, have been considered separately or at a single spatial or temporal scale. We used a 6-year nesting data set of scissor-tailed flycatcher, Tyrannus forficatus , which have high rates of cuckoldry (73% of nests, 59% of nestlings), to explore how nest density, breeding synchrony, habitat structure and clutch initiation date affect EPP rates. We further considered synchrony at two temporal and habitat structure at two spatial scales. We predicted that visual occlusion from vertical habitat structuring on breeding territories would allow extrapair males to go unnoticed and provide cover for extrapair copulations. Predictions for effects of nest density and fertility synchrony were double-edged: EPP may either increase as extrapair mate availability and ease of comparison with social mates increases or decrease as social mates increase their efforts to assure paternity. Using Bayesian techniques, we found a combination of population level factors and habitat structure, including interactions among the latter, at different scales best accounted for variation in EPP. EPP declined with increasing population synchrony. Variation in EPP was also explained by fine-scale habitat measures, decreasing with increasing nest tree diameter at breast height and woody vegetation cover but increasing with tree density. Notably, EPP increased with a coarse-scale habitat measure, linear extent of fence or powerline, suggesting a role for human alteration of habitat. Fences are used as communal perches by neighbours and floater males, potentially increasing interactions between asynchronous individuals. Our study demonstrates that breeding synchrony influences the probability of EPP and that habitat structure on individual territories is a strong predictor of paternity that acts independently of breeding density or synchrony at our scale of measurement. • We explore factors influencing cuckoldry in scissor-tailed flycatchers across 6 years. • Cuckoldry increased with populationwide fertility synchrony. • Cuckoldry was not related to spatial distribution of nests. • Cuckoldry increased with tree number and powerline/fence length and low shrub cover. • These correlates may impact cuckoldry via their effects on male mate guarding.

Experimental extra-pair copulations provide proof of concept for fertility insurance in a socially monogamous bird.

Extra-pair paternity is common among socially monogamous birds, but whether females benefit from having extra-pair copulations remains unresolved. In this study, I staged single extra-pair copulations in captive pairs of socially monogamous Japanese quail (Coturnix japonica) and used extra-pair males of a different colour to identify extra-pair fertilizations. This eliminated among-female variation in extra-pair copulations as a source of variation in extra-pair fertilizations and tested whether a single extra-pair copulation would insure against infertility of the social male. Overall, the probability of extra-pair fertilization was 0.46 for the first egg that was fertilized after extra-pair copulation, but this rapidly declined over consecutive eggs in the laying sequence. However, a single extra-pair copulation was effective in ensuring fertilization of the majority of a typical clutch in the few cases where the social male was completely infertile. Hence, my results show that variation in extra-pair paternity can be independent from variation in extra-pair copulation behaviour and that a single, strategically timed, extra-pair copulation can largely insure against social male infertility. Among-female variation in extra-pair fertilizations, and their declining probability over the laying sequence, as typical for many bird species, can thus, in principle, be parsimoniously explained by a uniform female fertility insurance strategy.

Microsatellite markers yield new insight into extra-pair paternity in Bobolinks (Dolichonyx oryzivorus)

Since the mid-1980s, our understanding of avian reproductive strategies has shifted as new molecular technologies have revealed how common promiscuity is in many monogamous avian species. However, the prevalence and importance of extra-pair paternity in polygynous species is less well studied. We used microsatellite loci from related icterid species to identify the extra-pair paternity rate in a polygynous population of Bobolinks (Dolichonyx oryzivorus) that bred in the Champlain Valley of Vermont from 2002 to 2018. We assigned paternity for 120 nestlings and found that 42% of nestlings were sired by extra-pair males. These results highlight the importance of extra-pair paternity in the reproductive behavior of Bobolinks that breed in agricultural habitats.

Extra-pair paternity in the wood-feeding cockroach Cryptocercus punctulatus Scudder: Social but not genetic monogamy.

Subsocial Cryptocercus cockroaches are the sister group to termites and considered to be socially monogamous. Because genetic monogamy is a suggested requirement for evolution of cooperative breeding/eusociality, particularly in hymenopterans, clarification of the mating biology of Cryptocercus would help illuminate evolutionary trends in eusocial insects. To investigate possible extra-pair paternity in C.punctulatus, microsatellite markers were used to analyse offspring parentage, the stored sperm in females and results of experimental manipulation of sperm competition. Extra-pair paternity was common in field-collected families, but a lack of maternal alleles in several nymphs suggests sampling error or adoption. Isolating prereproductive pairs and assaying subsequently produced nymphs confirmed that nymphs lacked alleles from the pair male in 40% of families, with extra-pair male(s) siring 27%-77% of nymphs. Sperm of extra-pair males was detected in the spermatheca of 51% of paired prereproductive females. Mate switching and surgical manipulation of male mating ability indicated a tendency towards last male sperm precedence. Overall, the results demonstrate that about half of young females are serially monogamous during their maturational year, but bond, overwinter and produce their only set of offspring in company of the last mated male (=pair male). Repeated mating by the pair male increases the number of nymphs sired, but because many females use stored sperm of previous copulatory partners to fertilize eggs, pair males extend parental care to unrelated nymphs. The results suggest that genetic monogamy either developed in the termite ancestor after splitting from the Cryptocercus lineage, or that genetic monogamy may not be a strict prerequisite for the evolution of termite eusociality.

Should females prefer old males?

Whether females should prefer to mate with old males is controversial. Old males may sire offspring of low quality because of an aging germline, but their proven ability to reach an old age can also be an excellent indicator of superior genetic quality, especially in natural populations. These genetic effects are, however, hard to study in nature, because they are often confounded with direct benefits offered by old males to the female, such as experience and high territory quality. We, therefore, used naturally occurring extra‐pair young to disentangle different aspects of male age on female fitness in a natural population of collared flycatchers because any difference between within‐ and extra‐pair young within a nest should be caused by paternal genetic effects only. Based on 18 years of long‐term data, we found that females paired with older males as social partners experienced an overall reproductive advantage. However, offspring sired by old males were of lower quality as compared to their extra‐pair half‐siblings, whereas the opposite was found in nests attended by young males. These results imply a negative genetic effect of old paternal age, given that extra‐pair males are competitive middle‐age males. Thus, offspring may benefit from being sired by young males but raised by old males, to maximize both genetic and direct effects. Our results show that direct and genetic benefits from pairing with old males may act in opposing directions and that the quality of the germline may deteriorate before other signs of senescence become obvious.

Body size is associated with yearling breeding and extra-pair mating in the Island Scrub-Jay

Abstract Large body size is an important determinant of individual fitness in many animal species, especially in island systems where habitat saturation may result in strong intraspecific competition for mates and breeding territories. Here we show that large body size is associated with benefits to yearling breeding and extra-pair mating in the Island Scrub-Jay (Aphelocoma insularis), endemic to Santa Cruz Island, California. This species is ~20% larger than its mainland congener, consistent with the island syndrome, indicating that body size may be a trait under selection. From 2009 to 2013, we quantified the reproductive success of a marked population of Island Scrub-Jays, tracked which yearlings acquired a breeding territory and bred, and measured the occurrence of extra-pair paternity. Two potential contributors to fitness were positively related to body size. Larger yearling males were more likely to breed, possibly due to greater behavioral dominance during aggressive encounters. Larger males were also less likely to lose paternity to extra-pair males and, anecdotally, extra-pair males were larger than the social male cuckolded. This study provides evidence that larger males may have a fitness advantage over smaller males by breeding earlier and avoiding paternity loss, but estimates of lifetime reproductive success are ultimately needed for Island Scrub-Jays and other long-lived species.

Loss of Extra-pair Paternity is not Associated with Decreased Paternal Investment in Mixed-paternity Broods or Unrelated Nestlings in the Varied Tit, Parus varius

Males of socially monogamous bird species may be faced with providing costly care for unrelated offspring when nests have extra-pair young (EPY). Theoretical models predict that cuckolded males should lower their parental investment as the likelihood of paternity decreases. However, empirical data are not always in support of this prediction. Here, we explore parental behaviours within the context of extra-pair patenity (EPP) in a population of the varied tit Parus varius in China. The results showed that 39.5% of nests were cuckolded and 16.4% of chicks were sired by extra-pair males. We found no evidence that male and female varied tits reduced their feeding rates or relative feeding effort to EPP broods, or that they decreased provisioning for EPY in mixed broods. There was also no direct effect of EPP on the reproductive success of breeding adults and the body condition nestlings near fledging. The lack of reliable cues of EP copulations (EPC)s by social mates available for the males, and/or the absence of strictly environmental pressure on males that would favor discrimination may account for a lack of an adjustment in feeding effort. The absence of discrimination between own and EPP chicks in parental care suggests that females pay no fitness cost as a result of EPCs, which may explain the high frequency of EPY in nests.

MHC-Based Mate Choice in Wild Golden Snub-Nosed Monkeys.

The genes of the major histocompatibility complex (MHC) are an important component of the vertebrate immune system and play a significant role in mate choice in many species. However, it remains unclear whether female mate choice in non-human primates is based on specific functional genes and/or genome-wide genes. The golden snub-nosed monkey (Rhinopithecus roxellana) lives in a multilevel society, which consists of several polygynous one-male-several-female units. Although adult females tend to mainly socialize with one adult male, females often initiate extra-pair copulations with other males resulting in a high proportion of offspring being fathered by extra-pair males. We investigated the effects of adaptive MHC genes and neutral microsatellites on female mate choice in a wild R. roxellana population. We sequenced 54 parent-offspring triads using two MHC class II loci (Rhro-DQA1 and Rhro-DQB1) and 20 microsatellites from 3 years of data. We found that the paternities of offspring were non-randomly associated with male MHC compositions not microsatellite genotypes. Our study showed that the fathers of all infants had significantly less variance for several estimates of genetic similarity to the mothers compared with random males at both MHC loci. Additionally, the MHC diversity of these fathers was significantly higher than random males. We also found support for choice based on specific alleles; compared with random males, Rhro-DQA1∗ 05 and Rhro-DQB1∗ 08 were more common in both the OMU (one-male unit) males and the genetic fathers of offspring. This study provides new evidence for female mate choice for MHC-intermediate dissimilarity (rather than maximal MHC dissimilarity) and highlights the importance of incorporating multiple MHC loci and social structure into studies of MHC-based mate choice in non-human primates.

Female need for paternal care shapes variation in extra-pair paternity in a cooperative breeder

AbstractSocially monogamous females regularly mate with males outside the pair bond. The prevailing explanation for this behavior is that females gain genetic benefits resulting from increased fitness of extra-pair offspring. Furthermore, because of the risk of reduced paternal care in response to cuckoldry, females are expected to seek extra-pair copulations when they can rear offspring with little help from their social partner (“constrained female” hypothesis). We tested these hypotheses and analyzed variation in paternal care in the Afrotropical, facultative cooperative breeding placid greenbul (Phyllastrephus placidus). Overall, approximately 50% of the offspring resulted from extra-pair (and extra-group) mating. Identified extra-pair males were in most cases neighboring dominant males, yet never within-group subordinates. As predicted by the constrained female hypothesis, the occurrence of extra-pair paternity (EPP) increased with the number of cooperative helpers (and not with total group size). However, dominant males did not adjust their food provisioning rates in response to EPP. Although extra-pair males were more strongly related to the dominant female and less heterozygous than the latter’s social mate, this did not result in more inbred extra-pair offspring, likely because identified extra-pair males were not representative of the extra-pair male population. While earlier studies on EPP mainly focused on male genetic quality, results from this study provide evidence that female’s social context may affect extra-pair strategies too.

Does experimentally altered plumage brightness influence extra-pair mating success in female Tree Swallows (Tachycineta bicolor)?

Recent empirical evidence suggests that ornamental traits displayed by female birds may reflect aspects of their quality, and function during competitive interactions and (or) social mate attraction; however, less is known about how such traits influence extra-pair paternity. In Tree Swallows (Tachycineta bicolor (Vieillot, 1808)), plumage brightness of females signals their quality and may be related to extra-pair paternity if it enables them to invade the territories of other females to seek extra-pair copulations and (or) if potential extra-pair mates perceive their plumage brightness as attractive. Therefore, to examine whether the plumage brightness displayed by females influence rates of extra-pair paternity and the number of sires per brood, we experimentally enhanced and reduced the plumage brightness of females relative to controls. Our results showed that plumage brightness treatment of the female did not influence the number of extra-pair offspring in nests or the likelihood of a brood containing extra-pair offspring. Additionally, the number of extra-pair males siring offspring within the broods of females did not differ by plumage brightness treatment. Although extra-pair paternity has been shown to be beneficial for female Tree Swallows, our results suggest that plumage brightness of females does not influence their ability to engage in extra-pair mating.

Extra-pair mating in a passerine bird with highly duplicated major histocompatibility complex class II: Preference for the golden mean.

Genes of the major histocompatibility complex (MHC) are essential in vertebrate adaptive immunity, and they are highly diverse and duplicated in many lineages. While it is widely established that pathogen-mediated selection maintains MHC diversity through balancing selection, the role of mate choice in shaping MHC diversity is debated. Here, we investigate female mating preferences for MHC class II (MHCII) in the bluethroat (Luscinia svecica), a passerine bird with high levels of extra-pair paternity and extremely duplicated MHCII. We genotyped family samples with mixed brood paternity and categorized their MHCII alleles according to their functional properties in peptide binding. Our results strongly indicate that females select extra-pair males in a nonrandom, self-matching manner that provides offspring with an allelic repertoire size closer to the population mean, as compared to offspring sired by the social male. This is consistent with a compatible genes model for extra-pair mate choice where the optimal allelic diversity is intermediate, not maximal. This golden mean presumably reflects a trade-off between maximizing pathogen recognition benefits and minimizing autoimmunity costs. Our study exemplifies how mate choice can reduce the population variance in individual MHC diversity and exert strong stabilizing selection on the trait. It also supports the hypothesis that extra-pair mating is adaptive through altered genetic constitution in offspring.

Elevation affects extra-pair paternity but not a sexually selected plumage trait in dark-eyed juncos

Differences in environmental conditions are expected to generate distinct selective pressures favoring different phenotypes. For example, environmental conditions that affect the timing of breeding may influence opportunities for extra-pair copulations and thus the strength of sexual selection on males. To explore these relationships quantitatively, we compared breeding synchrony, rates of extra-pair paternity, and expression of a sexually selected plumage trait (the amount of white on the tail feathers) in populations of dark-eyed junco (Junco hyemalis) breeding at elevations from 1960 to 2660 m in California. Microsatellite parentage analysis revealed that extra-pair paternity rates varied by elevation, with intermediate elevations having the highest rate. Differences in breeding synchrony could not explain this variation. Extra-pair males had more tail white than the social males they cuckolded, consistent with tail white being a sexually selected trait. Although the observed differences in rates of extra-pair paternity suggested that sexually selected traits should also vary with elevation, there were no differences among elevations in the amount of white on male tails or in the correlation between tail white and proxies for male condition. Multiple factors may have contributed to this result, including persistent gene flow among elevations, which may counter the effects of local differences in selective pressures. These findings demonstrate the complexity of interactions among environmental conditions, selective pressures, and variation in phenotypic traits, and underscore the importance of assessing the impacts of sexual selection in the larger context of population genetic structure. SIGNIFICANCE STATEMENT: Environmental differences, such as those occurring along elevation gradients, can lead to differences in sexual selection. We found that juncos at mid elevations had higher rates of extra-pair paternity than juncos at high and low elevations. Our results also provide evidence that male tail plumage is sexually selected, as females preferred to copulate with males with more white on their tail plumage than the females’ social mates. This suggests that male tail white should differ among elevations, as the reproductive rewards of having an attractive tail would be greater at mid elevations. However, we found no differences in male tail white among elevations. This may be due to the birds breeding freely across elevations, as evidenced by a lack of genetic structure, i.e., gene flow swamping out any differences that might otherwise form.

Inclusive fitness benefits mitigate costs of cuckoldry to socially paired males

BackgroundIn socially monogamous species, reproduction is not always confined to paired males and females. Extra-pair males commonly also reproduce with paired females, which is traditionally thought to be costly to the females’ social partners. However, we suggest that when the relatedness between reproducing individuals is considered, cuckolded males can suffer lower fitness losses than otherwise expected, especially when the rate of cuckoldry is high. We combine theoretical modeling with a detailed genetic study on a socially monogamous wild fish, Variabilichromis moorii, which displays biparental care despite exceptionally high rates of extra-pair paternity.ResultsWe measured the relatedness between all parties involved in V. moorii spawning events (i.e. between males and females in social pairs, females and their extra-pair partners, and paired males and their cuckolders), and we reveal that males are on average more related to their cuckolders than expected by chance. Queller–Goodnight estimates of relatedness between males and their cuckolders are on average r = 0.038 but can range up to r = 0.64. This also increases the relatedness between males and the extra-pair offspring under their care. These intriguing results are consistent with the predictions of our mathematical model, which shows that elevated relatedness between paired males and their cuckolders can be adaptive for both parties when competition for fertilizations is strong.ConclusionsOur results show how cuckoldry by relatives can offset males’ direct fitness losses with inclusive fitness gains, which can be substantial in systems where males face almost certain paternity losses.

Extra-pair paternity in socially monogamous Streaked Shearwaters: forced copulation or female solicitation?

Seabirds are long-lived birds that invest in offspring at very high levels, for which male parental care is indispensable. These characteristics are thought to explain seabirds’ generally low level of extra-pair paternity (EPP). Although the Streaked Shearwater (Calonectris leucomelas) is a socially monogamous seabird, it is known to copulate outside its social pair bond, which implies the frequent occurrence of EPP. In the closely related Cory’s Shearwater Calonectris borealis, cuckoldry is related to body size of the social male. To determine whether body-size-related EPP occurs among Streaked Shearwaters, we established 39 new microsatellite markers for parentage analysis and compared body size between cuckolded and non-cuckolded males. With the new markers, we found that extra-pair males sired 17 (15.0%) of 113 offspring during the 2014–2016 study period, which included three 1.5-month chick-rearing periods. This percentage is among the highest recorded for seabirds. We also found the bill and wing length of cuckolded males to be significantly shorter than those of non-cuckolded males, and that females can reject attempted copulations. These observations imply that EPP in this species is size related and involves female acceptance.

Association between extra-pair paternity and nestling sex and condition in the barn swallow

Parents should differentially allocate resources to the production of offspring of either sex depending on their expected fitness return. In sexually promiscuous females, offspring sex ratio should be affected by the sexual attractiveness of biological fathers because sons, but not daughters, will benefit from inheriting genes for sexual attractiveness. Females may acquire benefits for the offspring if the extra-pair male is of superior genetic quality as compared to the social mate, if it carries compatible genes or genes that enhance offspring genetic diversity. If sexually selected ornaments reflect male quality, extra-pair offspring should be more frequently males and of higher quality compared to their half-siblings. Furthermore, the probability of extra-pair offspring to be male should increase with an increasing difference in sexual ornamentation between the extra-pair and the social mate. In this study, we tested if barn swallow offspring sex ratio depends on paternity and on sexual ornamentation of the extra-pair father, and whether paternity predicts offspring phenotypic quality. The results partially fulfilled our prediction. We did not provide support for the hypothesis of a differential sex allocation to the production of male offspring by promiscuous females, both at the individual and at the within-brood level. Moreover, the difference in the ornamentation of the extra-pair and the social male did not affect the sex ratio of individual offspring. However, in accordance with the good genes and the genetic compatibility hypotheses, extra-pair offspring were of superior quality as compared to their half-sibling, in terms of body size and feather growth. In sexually promiscuous species, females should differentially allocate resources to the production of offspring of either sex depending on paternity or sexual ornamentation of the social or the extra-pair mate. Moreover, extra-pair offspring may be of superior quality compared to their within-pair half-siblings. In the present study of the barn swallow, paternity and the differences in sexual ornamentation between the social and the extra-pair mate did not affect offspring sex ratio. In addition, according to the good genes and the genetic compatibility hypotheses, we found that extra-pair offspring are of superior quality as compared to their within-pair siblings. Despite we failed to provide support to the sex allocation theory, the present study emphasizes the importance of “negative” results to better estimate the generality of the occurrence of adaptive sex allocation strategies in the context of sexual selection studies.