Extra-pair Paternity Research Articles

Nest-site selection and nest predation in a tropical passerine in relation to food, friends, and foes

ABSTRACT Nest-site selection is an important determinant of avian reproductive success, mainly through its effect on predation risk. However, which environmental and social factors affect nest-site selection and predation risk remains less well understood. Optimal nest positioning may depend on the balance of many distinct factors such as nest predation, food availability, extra-pair mating opportunities, presence of helpers, and interactions with neighboring conspecifics. We investigated how these factors affect nest-site selection and nest survival in Acrocephalus sechellensis (Seychelles Warbler), a facultative cooperative-breeding passerine that defends stable territories year-round. We found that daily nest survival increased by ~1% for each meter higher in the canopy that a nest was placed. Nests were more likely to be located in food-rich parts of the territory, especially in territories with low overall densities of arthropods. Further, we found that nests in territories with helpers, which reduce nest predation in A. sechellensis, were built in areas with higher food availability, whereas nests in territories without helpers were built in areas with fewer nest predators. Finally, we found that females build their nests 0.5 m closer to the border for each year the nearest neighboring male was older than their partner. Our results suggest that nest-site selection in A. sechellensis is affected by nest predation, food availability, helper presence, and possibly, the female’s opportunity for extra-pair copulations. Clarifying the relative importance of these different selective factors is key to the understanding of optimal nest-site selection to maximize reproductive success.

Influence of genetic similarity and social setting on extra-pair parentage in prairie voles

Abstract Social monogamy is rare in mammals, but in those species in which it occurs, individuals frequently engage in extra-pair copulation (EPC). Numerous hypotheses have been proposed to explain EPC, but relatively few field studies have examined factors influencing EPC in socially monogamous mammals. Prairie voles (Microtus ochrogaster) are a socially monogamous rodent in which extra-pair paternity (EPP) is common. Using genetic data from a 3-year study of a natural population of prairie voles, we investigated whether the negative consequences of inbreeding and the structure of social units (male–female pairs vs. groups; adult sex ratio within groups) were factors affecting EPC. We found strong evidence that genetic similarity between males and females that produced offspring via EPC was less than that between social partners, as would be expected if avoiding inbreeding depression influenced the occurrence of EPC. Social unit structure was also a factor involved with extra-pair parentage. Contrary to our expectations, the greater the proportion of females in the group, the lower the chance of EPC resulting in offspring production by females, and, similarly, the chance of EPP by males declined as the proportion of males within the group increased. However, neither males nor females were more likely to produce offspring from EPC when they were living in pairs versus groups. One implication of these results is that EPC may be influenced more by female behaviors, such as mate choice, than male mate guarding. Overall, our results suggest that the proximate factors influencing EPC in prairie voles are complex but include the cost of inbreeding depression and the structure of social units.

Demographic drivers of reproductive failure in a threatened bird: Insights from a decade of data

Hatching failure affects up to 77% of eggs laid by threatened bird species, yet the true prevalence and drivers of egg fertilization failure versus embryo mortality as underlying mechanisms of hatching failure are unknown. Here, using ten years of data comprising 4,371 eggs laid by a population of a threatened bird, the hihi (Notiomystis cincta), we investigate the relative importance of infertility and embryo death as drivers of hatching failure and explore population-level factors associated with them. We show that of the 1,438 eggs that failed to hatch (33% of laid eggs) between 2010 and 2020, 83% failed due to embryo mortality, with the majority failing in the early stages of embryonic development. In the most comprehensive estimates of infertility rates in a wild bird population to date, we find that fertilization failure accounts for around 17% of hatching failure overall and is more prevalent in years where the population is smaller and more male biased. Male embryos are more likely to die during early development than females, but we find no overall effect of sex on the successful development of embryos. Offspring fathered by within-pair males have significantly higher inbreeding levels than extra-pair offspring; however, we find no effect of inbreeding nor extra-pair paternity on embryo mortality. Accurately distinguishing between infertility and embryo mortality in this study provides unique insight into the underlying causes of reproductive failure over a long-term scale and reveals the complex risks of small population sizes to the reproduction of threatened species.

Combined high rates of alternative breeding strategies unexpectedly found among populations of a solitary nesting raptor.

Social monogamy is the prevalent mating system in birds, but alternative strategies of extra-pair paternity (EPP) and conspecific brood parasitism (CBP) occur in many species. Raptors are virtually absent in discussions of broad taxonomic reviews regarding EPP and CBP likely because these strategies are mostly absent or at low frequency; CBP is unreported in solitary nesting raptors. In contrast, we found high frequencies of EPP (16%-31%) and CBP (15%-26%) nests among three populations of Cooper's Hawks (Accipiter cooperii) across the northern breeding range of this solitary nesting, socially monogamous species. EPP and CBP combined occurred in 42%-46% of all nests among populations and hence unexpectedly were nearly equivalent to proportions of genetically monogamous nests. Select covariates failed to predict presence of EPP and CBP in part because virtually all extra-pair adults were uncaught and likely were floaters. We found no support for the hypothesis that territorial females traded copulations for food to maximize energy intake for increased production. Our unique discoveries enhance knowledge of the extent and diversity of alternative breeding strategies among groups of avian and other animal species.

Extra-pair paternity and sperm length variation in a far northern Great Tit (Parus major) population

Extra-pair paternity and sperm length variation in a far northern Great Tit (Parus major) population

Extra-pair paternity in two passerine birds breeding in a gradient of urbanisation.

Urbanisation has been increasing worldwide in recent decades, driving environmental change and exerting novel selective pressures on wildlife. Phenotypic differences between urban and rural individuals have been widely documented in several taxa. However, the extent to which urbanisation impacts mating strategies is less known. Here, we investigated extra-pair paternity variation in great tits (Parus major) and blue tits (Cyanistes caeruleus) breeding in nestboxes set in a gradient of urbanisation in Warsaw, Poland, over three breeding seasons. Urbanisation was quantified as the amount of light pollution, noise pollution, impervious surface area (ISA) and tree cover within a 100-m radius around each nestbox. We obtained genotypes for 1213 great tits at 7344 SNP markers and for 1299 blue tits at 9366 SNP markers with a genotyping-by-sequencing method, and inferred extra-pair paternity by computing a genomewide relatedness matrix. We report higher extra-pair paternity in blue tits breeding in more urbanised areas, for example, with higher light pollution and ISA, and lower tree cover. However, no such trend was found in great tits. Late-stage survival of individual nestlings in both species was not associated with paternity or urbanisation proxies, thus we were not able to detect fitness benefits or drawbacks of being an extra-pair offspring in relation to urbanisation. Our results contribute to the growing body of knowledge reporting on the effects of urbanisation on avian ecology and behaviour, and confirm species-specific and population-specific patterns of extra-pair paternity variation.

Social and genetic relationships among individuals in urban kit fox social groups

Smaller canids, such as most foxes, individually hunt small prey, and therefore, social groups typically consist of just a mated pair. However, these smaller canids occasionally form groups in which the members have been presumed to be genetically or socially related. We studied social and genetic relationships among urban San Joaquin kit fox ( Vulpes macrotis mutica Merriam, 1902) groups in Bakersfield, California. Of 59 groups, 42.4% had extra adults in addition to the parents. Foxes were field classified as either mothers, fathers, helpers (extra adults), or pups. We then assessed relatedness of foxes within social groups using 11 microsatellites in DNA from tissue or hair samples. Mated pairs were significantly less related than mothers and helpers, with fathers and helpers being intermediate. Twelve pairs of females were mother–daughter dyads, but we also found two cases of sisters and two cases where the females were unrelated. Pups were always related to a female identified as their mother. Father–pup pairs were less related than mother–pup pairs, with helper–pup pairs being intermediate. The extra-pair paternity rate (multiple fathers per litter) was 39%. The social flexibility exhibited by kit foxes may increase their resiliency to marked fluctuations in resource availability, thereby reducing extinction risk.

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.

Benefits of Pair-Bond Duration on Reproduction in a Lifelong Monogamous Cooperative Passerine.

AbstractLong-term social and genetic monogamy is rare in animals except birds, but even in birds it is infrequent and poorly understood. We investigated possible advantages of monogamy in a colonial, facultative cooperatively breeding bird from an arid, unpredictable environment, the sociable weaver (Philetairus socius). We documented divorce and extrapair paternity of 703 pairs over 10 years and separated effects of pair duration from breeding experience by analyzing longitudinal and cross-sectional datasets. Parts of the colonies were protected from nest predation, thereby limiting its stochastic and thus confounding effect on fitness measures. We found that 6.4% of sociable weaver pairs divorced and 2.2% of young were extrapair. Longer pair-bonds were associated with more clutches and fledglings per season and with reproducing earlier and later in the season, when snake predation is lower, but not with increased egg or fledgling mass or with nestling survival. Finally, the number of helpers at the nest increased with pair-bond duration. Results were similar for protected and unprotected nests. We suggest that long-term monogamy is associated with a better capacity for exploiting a temporally unpredictable environment and helps to form larger groups. These results can contribute to our understanding of why long-term monogamy is frequently associated with unpredictable environments and cooperation.

Ultimate drivers of forced extra-pair copulations in birds lacking a penis: jackdaws as a case-study.

Forced copulation is common, presumably because it can increase male reproductive success. Forced extra-pair copulation (FEPC) occurs in birds, even though most species lack a penis and are widely thought to require female cooperation for fertilization. How FEPC persists, despite a presumed lack of siring success and likely non-negligible costs to the male, is unknown. Using the jackdaw (Corvus monedula) as a case study, we use SNPs to quantify the extra-pair paternity rate through FEPC and evaluate explanations for the persistence of FEPC in species without a penis. We then collate evidence for FEPC across penis-lacking birds. Combining genetic and behavioural analyses, our study suggests that the most likely explanations for the maintenance of FEPC in jackdaws are that it provides a selective advantage to males or it is a relic. Our literature review shows that across birds lacking a penis, FEPC is taxonomically widespread, and yet, little is known about its evolution. A broader implementation of the approach used here, combining both genetic and behavioural data, may shed light on why this widespread sexual behaviour persists. Additional work is necessary to understand whether a penis is needed for paternity through forced copulation and to quantify the costs of FEPC.

The cuckoldry conundrum.

Concerns about cuckoldry are a dominant theme in evolutionary studies of mating, frequently used to explain sex differences in reproductive strategies. However, studies in nonhuman species have shown that cuckoldry can be associated with important benefits. These insights have not been well integrated with the human literature, which continues to focus on anticuckoldry tactics and negative repercussions for men. I evaluate two key assumptions central to human models of cuckoldry: (1) men are being tricked into investing in nonbiological offspring and (2) investment in nonbiological offspring is wasted. The ethnographic data on fatherhood shows that the concepts of pater and genitor are complex and locally constructed ideas that often include explicit knowledge of extra-pair paternity, countering the idea that nonpaternity results from trickery. Furthermore, rather than being a "waste," paternity loss can be associated with important gains for men, helping to explain why men invest in nonbiological offspring.

Extra‐pair paternity enhances the reproductive fitness of urban Chinese blackbird

Urbanization is a human‐induced process of rapid habitat change that can affect the reproductive success of animals. The occurrence of extra‐pair paternity (EPP) may be sensitive to changes in urban ecological conditions. In this study, the Chinese blackbird Turdus mandarinus, a common breeding bird in southern Chinese cities, was selected as the focus species to explore the EPP patterns of monogamous birds in developing cities and the relationship between pairs. Over four breeding seasons, 316 Chinese blackbird nestlings and 20 adults in both urban and rural areas were monitored and genotyped for 11 microsatellite loci to determine progeny affinity. We confirmed that both the brood size and hatching rate of EPP nests were significantly larger than those of within‐pair paternity (WPP) nests. The body mass, beak length, head length, and body length of 12‐day age extra‐pair offspring (EPO) were significantly greater than those of within‐pair offspring (WPO), suggesting important benefits of EPP. However, in accordance with the analyses of nest ecological variables, we concluded that EPP occurs most often in areas with low urbanization levels, indicating some constraints for this reproductive strategy in cities. Our findings provide new insights about how this growing human‐induced landscape change affects mating behaviour in birds, an important aspect in avian ecology and evolution.

Extra-pair paternity in the Wood Warbler (Phylloscopus sibilatrix) in Central Russia

Extra-pair paternity is widespread in passerine birds. The number of extra-pair young (EPY) varies among different species and populations of the same species. We tested if it is a case for a small passerine bird with poly-territorial behaviour, the Wood Warbler (Phylloscopus sibilatrix). The results are based on the microsatellite analysis of seven loci and revealed a high level of EPY in Central Russia population of Wood Warbler (EPY in 41% of all nests, 16 of 39 nests; 25% of all young were EPY, 52 of 212 young). We did not find relationship between relatedness among mates in the pair and the presence of EPY. There was no difference in heterozygosity and body mass between EPY and within pair young (WPY). Possible causes of extra-pair paternity are discussed.

A possible case of offspring sex manipulation as result of a biased adult sex ratio

Although random meiosis should prevent the facultative adjustment of offspring sex ratio, theory predicts that females should produce more of the sex with the higher reproductive value. We reported a case of offspring sex ratio manipulation in grass wrens Cistothorus platensis. Males in better body condition would have higher reproductive value than females due to the potential for social polygyny and extra-pair fertilizations. On the other hand, local demography influences reproductive strategies in grass wrens as male abundance affects both social polygyny and extra-pair paternity frequencies. We evaluated whether females bias their brood sex ratio in response to adult sex ratio and nestling body condition (a proxy for female’s prospects of producing high-quality males). Females raised more male offspring when males were less abundant in the population (female-biased adult sex ratio). However, we found no relationship between nestling body condition and brood sex ratio, suggesting that females did not bias the brood sex ratio towards males when able to raise nestlings in better body condition. Taken together, our results provide the first suggestive evidence that female birds can manipulate their offspring sex ratio in response to the adult sex ratio.

Alternative mating strategies in Eurasian Reed Warblers: extra-pair paternity and egg dumping

Alternative mating strategies, involving mating outside a social pair bond, have been studied intensively during the last few decades. However, we are still far from understanding what factors affect their frequencies in wild bird populations. In 2006–2011 we studied Eurasian Reed Warblers breeding in the nature reserve “Stawy Milickie” in SW Poland, and analysed the frequency of extra-pair paternity (EPP) and intra-specific brood parasitism (IBP). We genotyped a total of 786 nestlings from 259 nests. EPP offspring constituted 13.40% of all young (from 7.63% to 22.82% in different study years), and they were found in 21.62% of the broods (from 14.6% to 32.7% annually). The mean proportion of females with EPP young was 24.2% (from 16.2 to 41.7% annually). The proportion of EPP young in nests containing any EPP offspring ranged from 25% to 100% (on average 60%) and was not related to brood size. EPP young in one nest were sired usually by one or two males (92% of all cases), but we recorded one brood with three EPP fathers and one brood of four, where each young was sired by a different EPP male, and none by a social male. We found only one case of intra-specific brood parasitism (IBP). The brood with IBP constituted 0.39% of all examined broods, while the nestling that hatched from the dumped egg constituted 0.13% of all young whose parents were genotyped. We conclude that extra-pair paternity is a relatively common and regularly occurring alternative mating strategy in our study population of Reed Warblers, while intra-specific brood parasitism is extremely rare.

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.

Development and parentage analysis of SNP markers for Chestnut-vented Nuthatch (Sitta nagaensis) based on ddRAD-seq data

Extra-pair paternity (EPP) is commonly found in socially monogamous birds, especially in small passerine birds, and there are interspecific and intraspecific variations in the extent of EPP. The Chestnut-vented Nuthatch (Sitta nagaensis) is a socially monogamous passerine bird, and verifying whether this species has EPP relies on parentage testing—S. nagaensis is not known to have EPP. In this study, we developed SNP markers of this species that are informative for parentage analysis from double digest restriction site-associated DNA sequencing (ddRAD-seq) data. A panel consisting of 50 SNP markers, with a mean heterozygosity of 0.343, was used to resolve 95% of nestlings to fathers. The combined exclusion probabilities for the first parent and second parent were 0.991 and 0.9999, respectively. This panel of SNP markers is a powerful tool for parentage assignments in S. nagaensis. In addition, we found that three offspring (7.9%) from three nests (23.1%) were the result of extra-pair fertilization out of 38 offspring in 13 nests. Our study provided information on parentage analysis that has not been reported before in S. nagaensis. It also supplemented the understudied EPP behavior of birds in Asia, contributing to a general understanding of the EPP behaviors of birds.

Genomic data reveal unexpected relatedness between a brown female Eastern Bluebird and her brood.

Because plumage coloration is frequently involved in sexual selection, for both male and female mate choice, birds with aberrant plumage should have fewer mating opportunities and thus lower reproductive output. Here we report an Eastern Bluebird (Sialia sialis) female with a brown phenotype that raised a brood of four chicks to fledging. The brown female and her mate were only related to their social offspring to the second degree and one of the offspring was a half-sibling. We propose four family tree scenarios and discuss their implications (e.g., extra-pair paternity, conspecific brood parasitism). Regardless of the tree, the brown female was able to find a mate, which may have been facilitated by the bottleneck created by the severe snowstorms in February 2021.

The risk of brood parasitism does not affect levels of extrapair paternity in a cuckoo host

Abstract In socially monogamous bird species, extrapair paternity is common, but its level varies considerably within and among species. For hosts of brood parasites, the risk of brood parasitism may influence the costs of engaging in extrapair copulations (e.g., leaving the nest undefended) and the benefits of having extrapair young (e.g., spreading the risk of nest predation). However, whether brood parasitism risk affects extrapair behavior in host species has rarely been tested. We investigated whether variation in the risk of brood parasitism affected levels of extrapair paternity in Daurian redstarts, a socially monogamous passerine. As a common host of the common cuckoo, the redstart is unique in that its first clutch of the year takes place before the arrival of cuckoos. As a consequence, redstarts experience large seasonal variation in cuckoo parasitism risk, with no parasitism in the first egg-laying period and a high risk in the second period. We genotyped 995 nestlings (and unhatched eggs) from 181 broods and found moderate levels of extrapair paternity, with 34.8% of broods containing at least one extrapair young and 11.7% of all offspring being sired by an extrapair male. However, levels of extrapair paternity did not differ between the first and the second egg-laying period. Also, experimentally simulating parasitism risk during the first egg-laying period by broadcasting cuckoo vocalizations and presenting taxidermic models of cuckoos did not affect levels of extrapair paternity in redstarts. Our results, therefore, suggest that the risk of brood parasitism does not affect host extrapair paternity.

Mutual mate guarding with limited sexual conflict in a sex-role-reversed shorebird.

Mate guarding is typically considered a male strategy to protect paternity. However, under some circumstances, females might also benefit from guarding their mate. Female mate guarding might be particularly important in socially polyandrous species in which females compete for access to care-giving males. Because males also benefit from being near their partner to avoid paternity loss, pair members may have a mutual interest in mate guarding in polyandrous species. We studied the time spent together and movements that lead to separation, as behavioral measures of mate guarding, in the classically polyandrous red phalarope (Phalaropus fulicarius). We equipped 64 breeding pairs with miniaturized telemetry loggers with GPS to assess variation in mate-guarding intensity in relation to breeding phenology and season, nest attendance, and the occurrence of extrapair paternity. We show that red phalarope pairs were almost continuously together in the days before clutch initiation with no sex bias in separation movements, indicating mutual contribution to mate guarding. Our results suggest that in red phalaropes, both pair members guard their mate, with limited sexual conflict arising through biases in the operational sex ratio and a trade-off with male nest attendance. We found no clear relationship between mate-guarding intensity and the occurrence of extrapair paternity. In this non-territorial socially polyandrous species, mutual mate guarding might be the process underlying the evolution of a brief but strong social pair bond, with no other purpose than producing a clutch for a care-giving male.