High Rates Of Extra-pair Paternity Research Articles

Plural breeding among unrelated females and other insights on complex social structure in the cooperatively breeding Variegated Fairywren

ABSTRACT Cooperatively breeding species vary widely in degree of social complexity, and disentangling relationships among group members can reveal the costs and benefits of cooperation. Here, we describe the social system of the cooperatively breeding Variegated Fairywren (Malurus lamberti) and explore how social complexity and group dynamics may affect cooperation and conflict. We used a combination of field-based population monitoring and detailed social association observations to determine group membership annually across four breeding seasons (2014–2017) and used a ddRAD-seq genotyping method to determine genetic relationships within social groups. Social groups ranged in size from two to eight individuals and nearly half of all social groups had multiple adult individuals of both sexes. Approximately half of all groups exhibited plural breeding, in which multiple females within the same social group nested individually in the same territory. Genetic relationships were diverse among social groups due to high rates of extra-pair paternity and immigration, with most groups containing close relatives and non-relatives of each sex. Notably, although related females were often present within a social group, co-breeding females in the same social group were never closely related to each other. Given the extensive variation in relatedness among group members, cooperation in the Variegated Fairywren is likely maintained by a combination of direct and indirect fitness benefits.

High level of extra-pair paternity in the socially monogamous Marsh Tits (Poecile palustris)

BackgroundExtra-pair copulation behavior has been widely studied among socially monogamous birds. Many species revealed high rates of extra-pair paternity. But few of the studies have been carried out in the Asian population.MethodsFrom 2012 to 2019, we explored the extra-pair paternity of Marsh Tits (Poecile palustris) in Xianrendong National Nature Reserve, Liaoning Province, China. During the study, adult Marsh Tits were captured with mist nets and parental birds, with nest-box traps. Blood samples were taken from the brachial vein. Parentage analyses were carried out using nine highly variable microsatellite loci through Cervus 3.0 software and maximum likelihood approach.ResultsForty-nine offspring (15.08%) from 20 nests (45.45%) were the results of extra-pair fertilization out of a total of 325 offspring in 44 nests. The average extra-pair offspring ratio was 33.54%, with a set varying from 11.11 to 71.43%. Nine extra-pair fathers had been successfully identified, four of whom were the close neighbors of the focus nest while the nests of the remaining five were relatively far. No significant difference was found in the genetic similarity between the social and extra-pair mates of the female, nor in the heterozygosis among the maternal half-siblings.ConclusionsIn general, our study proved that the extra-pair paternity in Marsh Tits and its extra-pair mating is independent of the genetic compatibility hypothesis. This complements the understudied bird’s extra-pair paternity in Asian area and contributes to the comprehensive insight of birds’ extra-pair paternity behaviors.

Large brain size is associated with low extra-pair paternity across bird species.

BackgroundGaining extrapair copulations (EPCs) is a complicated behavior process. The interaction between males and females to procure EPCs may be involved in brain function evolution and lead to a larger brain. Thus, we hypothesized that extrapair paternity (EPP) rate can be predicted by relative brain size in birds. Past work has implied that the EPP rate is associated with brain size, but empirical evidence is rare.MethodsWe collated data from published references on EPP levels and brain size of 215 bird species to examine whether the evolution of EPP rate can be predicted by brain size using phylogenetically generalized least square (PGLS) models and phylogenetic path analyses.ResultsWe found that EPP rates (both the percentage EP offspring and percentage of broods with EP offspring) are negatively associated with relative brain size. We applied phylogenetic path analysis to test the causal relationship between relative brain size and EPP rate. Best‐supported models (ΔCICc < 2) suggested that large brain lead to reduced EPP rate, which failed to support the hypothesis that high rates of EPP cause the evolution of larger brains.ConclusionThis study indicates that pursuing EPCs may be a natural instinct in birds and the interaction between males and females for EPCs may lead to large brains, which in turn may restrict their EPC level for both sexes across bird species.

Do the ages of parents or helpers affect offspring fitness in a cooperatively breeding bird?

Age-related changes in parental phenotypes or genotypes can impact offspring fitness, but separating germline from nongermline transgenerational effects of ageing is difficult for wild populations. Further, in cooperatively breeding species, in addition to parental ages, the age of 'helpers' attending offspring may also affect juvenile performance. Using a 30-year study of a cooperative breeder with very high rates of extra-pair paternity, the superb fairy-wren (Malurus cyaneus), we investigated the effects of maternal, paternal and helper ages on three measures of offspring performance: nestling weight, juvenile survival to independence and recruitment to the breeding population. Mothers with a longer lifespan had offspring with higher juvenile survival, indicating selective disappearance, but the effect of maternal age on juvenile survival was of similar magnitude but negative. For extra-pair offspring, there was no evidence of any effect of the ages of either the genetic sire or the cuckolded 'social' father. However, for within-pair offspring, there was a positive effect of paternal age on juvenile survival, which we suggest may be driven by sexual selection. There were positive associations between the average age of helpers attending a nest and two of the three aspects of offspring performance; these effects were stronger than any of the effects of parental age. In general, the multiple associations between offspring fitness and the ages of adults around them appeared to be driven more by age-related changes in environmental effects than by age-related changes in the germline.

High rate of extrapair paternity in a human population demonstrates diversity in human reproductive strategies.

Among nonhuman species, social monogamy is rarely accompanied by complete fidelity. Evolutionary theory predicts that the rate of extrapair paternity (EPP) should vary according to socioecological conditions. In humans, however, geneticists contend that EPP is negligible and relatively invariable. This conclusion is based on a limited set of studies, almost all of which describe European-descent groups. Using a novel, double-blind method designed in collaboration with a community of Himba pastoralists, we find that the rate of EPP in this population is 48%, with 70% of couples having at least one EPP child. Both men and women were very accurate at detecting cases of EPP. These data suggest that the range of variation in EPP across human populations is substantially greater than previously thought. We further show that a high rate of EPP can be accompanied by high paternity confidence, which highlights the importance of disaggregating EPP from the notion of "cuckoldry."

Molecular evidence of extra-pair paternity and intraspecific brood parasitism by the Magellanic Penguin (Spheniscus magellanicus)

Molecular studies have shown that, although most avian species are socially monogamous, they can exhibit different reproductive strategies, such as extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). We investigated the genetic mating system of the Magellanic Penguin, Spheniscus magellanicus, a species that is reported to be monogamous, with little or no evidence of extra-pair paternity, high partner faithfulness over the years and intense biparental care. Thus, we proposed that if EPP does occur, the rate will be low and could be related to increased genetic diversity among offspring or the body condition of parents. As a consequence, we hypothesize that offspring from EPP will exhibit faster growth than non-EPP offspring, thus increasing their survival probability. In contrast to expectations, EPP was detected in 31% of the offspring and 48% of the nests had at least one extra-pair young. In addition, 6% of chicks were not the offspring of the putative mother or either member of the social pair, indicating evidence of IBP. However, we did not find a difference in genetic diversity between nests with or without EPP, nor did we find differences in parent body condition. Offspring from EPP showed slightly faster growth than non-EPP offspring, although this difference was not statistically significant. These results reveal a high rate of EPP and a low rate of IBP, both of which were previously unknown for this species. Our findings demonstrate that the Magellanic penguin has a more complex social mating system than previously thought.

Polygyny is linked to accelerated birdsong evolution but not to larger song repertoires

Non-monogamous mating behaviors including polygyny or extra-pair paternity are theorized to amplify sexual selection, since some males attract multiple mates or copulate with paired females. In several well-studied songbird species, females prefer more complex songs and larger repertoires; thus, non-monogamous mating behaviors are predicted to accelerate song evolution, particularly toward increased complexity. However, studies within songbird clades have yielded mixed results, and the effect of non-monogamy on song evolution remains unclear. Here, we construct a large-scale database synthesizing mating system, extra-pair paternity, and song information and perform comparative analyses alongside songbird genetic phylogenies. Our results suggest that polygyny drives faster evolution of syllable repertoire size (measured as average number of unique syllables), but this rapid evolution does not produce larger repertoires in polygynous species. Instead, both large and small syllable repertoires quickly evolve toward moderate sizes in polygynous lineages. Contrary to expectation, high rates of extra-pair paternity coincide with smaller repertoires.

Reproductive promiscuity in the variegated fairy-wren: an alternative reproductive strategy in the absence of helpers?

Cooperative breeding, in which auxiliary group members help rear related, but nondescendent young, is often explained by kin selection. Reproductive monogamy is predicted in cooperatively breeding systems, as monogamy increases intragroup relatedness and maximizes auxiliary inclusive fitness. While monogamy is observed across many systems, including eusocial insects and cooperatively breeding mammals, some cooperatively breeding birds exhibit high rates of extrapair paternity. Here we quantify paternity and examine the role of auxiliaries on extrapair paternity in the highly cooperative variegated fairy-wren, Malurus lamberti, a species with both male and female auxiliaries. Extrapair paternity occurred in 55.4% of nests, and 39.8% of offspring were the result of extrapair matings. The presence of both male and female auxiliaries had a positive relationship with the percentage of within-pair young sired by dominant males, however, the presence of male auxiliaries had a stronger impact than the presence of females. The number of extrapair young sired by dominant males decreased as the number of male auxiliaries increased. The total number of young sired by dominant males, however, was not predicted by group size or relatedness to their social partner, nor did group composition or relatedness to the breeding pair predict the reproductive success of subordinate males. We hypothesize that breeders use alternative reproductive strategies in the presence or absence of auxiliaries. Males and females may seek extrapair reproductive opportunities when no help is available in their group and nest survival is expected to be low. When help is available, breeders may reduce extrapair paternity, either to increase intragroup relatedness or because confidence in nest survival is high. Our data suggest that group composition is important in understanding extrapair paternity rates in cooperatively breeding birds and that variation in extrapair paternity rates may be the result of flexible breeding strategies when auxiliary presence and identity varies.

Is telomere length associated with mate choice in a songbird with a high rate of extra-pair paternity?

Telomere length is related to aging in many eukaryotes and the rate of telomere attrition has been suggested to reflect individual genetic quality. Telomere length could thus have implications for mate choice. We investigated telomere length variation in bluethroat Luscinia svecica families with mixed paternity, including social parents, extra-pair fathers and nestlings, testing whether telomere length is associated with social and/or extra-pair mate choice through assortative mating or selection of mates with relatively long telomeres. In adults, relative telomere length (rTL) did not differ between the sexes, nor between two age categories. In chicks, however, rTL decreased with body mass at sampling (an index of nestling age). We found a positive correlation between the rTL of social mates, suggesting assortative mating with respect to telomere length or a correlative thereof. However, extra-pair males did not differ from social mates in rTL, and accordingly there was also no difference between within- and extra-pair young (i.e. half-siblings) when controlling for the effect of mass. We found no relationships between telomere length, age and fitness-related traits in adults, but an intriguing year-difference in telomere length in both sexes. In conclusion, we found no support for the idea that females choose extra-pair males based on their telomere length, but social mate choice seems to be influenced by rTL, possibly through its co-variation with aspects reflecting individual quality, like early arrival at the breeding grounds.

Breeding synchrony and extrapair paternity in a species with alternative reproductive strategies

Breeding synchrony may affect the tradeoff between pursuing multiple mates and avoiding paternity loss, translating into differences in the rate of extrapair paternity (EPP). However, diverse empirical relationships between breeding synchrony and EPP remain challenging to explain. We examined whether the relationship between breeding synchrony and EPP varied with male morph, age, body size, or breeding density in the white-throated sparrow (Zonotrichia albicollis). In this species, males of two genetically determined morphs pursue alternative mating strategies. Breeding synchrony positively correlated with EPP within polygamous white morph males, which have high rates of EPP and cuckoldry, but was unrelated to EPP within tan morph males, which prioritize mate guarding and paternal care. As previously reported, males that gained EPP were primarily white males. Males gained EPP more often than expected by chance during their mate's fertile period and on neighboring territories. Since extrapair copulation appears primarily male-driven in this species, these results indicate that white males focus extra-pair mating effort during periods of high synchrony and during their mates’ fertile periods, even at the expense of paternity loss within their own nests. Breeding density, male age, and male size did not modify the relationship between breeding synchrony and EPP. However, older white males had higher cuckoldry rates, perhaps reflecting declines in performance associated with senescence. Results suggest that, even within species, mating strategy may modify how breeding synchrony affects rates of EPP, with positive relationships manifest only within subsets of individuals that pursue a strategy of polygyny at the expense of paternity loss. This article is protected by copyright. All rights reserved.

An assessment of the reliability of quantitative genetics estimates in study systems with high rate of extra-pair reproduction and low recruitment

Quantitative genetics approaches, and particularly animal models, are widely used to assess the genetic (co)variance of key fitness related traits and infer adaptive potential of wild populations. Despite the importance of precision and accuracy of genetic variance estimates and their potential sensitivity to various ecological and population specific factors, their reliability is rarely tested explicitly. Here, we used simulations and empirical data collected from an 11-year study on tree swallow (Tachycineta bicolor), a species showing a high rate of extra-pair paternity and a low recruitment rate, to assess the importance of identity errors, structure and size of the pedigree on quantitative genetic estimates in our dataset. Our simulations revealed an important lack of precision in heritability and genetic-correlation estimates for most traits, a low power to detect significant effects and important identifiability problems. We also observed a large bias in heritability estimates when using the social pedigree instead of the genetic one (deflated heritabilities) or when not accounting for an important cause of resemblance among individuals (for example, permanent environment or brood effect) in model parameterizations for some traits (inflated heritabilities). We discuss the causes underlying the low reliability observed here and why they are also likely to occur in other study systems. Altogether, our results re-emphasize the difficulties of generalizing quantitative genetic estimates reliably from one study system to another and the importance of reporting simulation analyses to evaluate these important issues.

Frequency of extra-pair paternity in Scissor-tailed Flycatchers (Tyrannus forficatus) and other suboscines: are oscines and suboscines different?

ABSTRACT Extra-pair paternity (EPP) appears to be widespread in passerine birds, but few studies have focused on suboscine species, and therefore it is unclear if this generalization can be extended to this group. In this study, we document high rates of EPP in a socially monogamous, suboscine passerine, the Scissor-tailed Flycatcher (Tyrannus forficatus) in southwest Oklahoma in the summers of 2009–2011. Averaged across years, EPP occurred in 66% of nests in our study population and accounted for 49% of all nestlings. EPP rates were variable (50–88%), but did not differ significantly among years or between two study sites. Our review of the literature yielded EPP data for only 11 other species of suboscines (0.7% of total), which we compared to EPP rates for the 83 oscine species (1.9% of total) reported in Spottiswoode and Moller (2004). EPP was as common and variable in suboscines (21.7% of young) as oscines (17.5% of young). Our study adds to our knowledge of mating systems in the understudied subosci...

The couple that sings together stays together: duetting, aggression and extra-pair paternity in a promiscuous bird species.

When individuals mate outside the pair bond, males should employ behaviours such as aggression or vocal displays (e.g. duetting) that help assure paternity of the offspring they care for. We tested whether male paternity was associated with aggression or duetting in the red-backed fairy-wren, a species exhibiting high rates of extra-pair paternity. During simulated territorial intrusions, aggression and duetting were variable among and repeatable within males, suggesting behavioural consistency of individuals. Males with quicker and stronger duet responses were cuckolded less often than males with slower and weaker responses. In contrast, physical aggression was not correlated with male paternity. These results suggest that either acoustic mate guarding or male-female vocal negotiations via duetting lead to increased paternity assurance, whereas physical aggression does not.

Testosterone secretion in a socially monogamous but sexually promiscuous migratory passerine

The steroid hormone testosterone (T) influences a multitude of traits critical to reproduction in vertebrates. In birds, high male T supports territory establishment and mate attraction, but is thought to interfere with parental care. Interspecific comparisons indicate that migratory species with short, synchronous breeding seasons have the highest peak T, and that the seasonal profile of T exhibits a rapid decline with the onset of incubation by females. We describe the T profile of the migratory, socially monogamous, and biparental Eastern Kingbird (Tyrannus tyrannus) from the high desert of eastern Oregon, USA, where breeding occurs within a short 2–3month period. Eastern Kingbirds are socially monogamous but exhibit high rates of extra-pair paternity as ∼60% of broods contain extra-pair young. We therefore evaluate whether Eastern Kingbirds exhibit the “typical” T profile expected for a synchronously breeding migratory species, or whether T is maintained at a more constant level as would be predicted for a species with opportunities for mating that extend over a majority of the breeding season. Our samples were divided into six periods of the reproductive cycle from territory establishment to the feeding of fledglings. T did not change across stages of the nest cycle. Instead, T declined with sampling date and nest density, and increased with the number of fertile females in the population. Male kingbirds advertise their presence through song for most of the breeding season, and we suggest that T is maintained throughout most of the breeding season because male fitness is equally dependent on within- and extra-pair reproductive success.

Male size predicts extrapair paternity in a socially monogamous bird with extreme sexual size dimorphism

Lay Summary The New Zealand tui is an iconic bird exhibiting extreme sexual size dimorphism. This is an unusual trait for a monogamous species and so we tested whether a male’s body size was related to his paternity success. First, we found that tūī had very high rates of extrapair paternity compared to other monogamous species. Second, larger males had higher paternity success. Thus, in contrast with previous studies, our results show that extrapair paternity can lead to the evolution of sexual size dimorphism.

Individual and environmental determinants of reproductive success in male tree swallow (Tachycineta bicolor)

Evaluating the contribution of individual and environmental determinants of reproductive success is essential to improve our understanding of sexual selection. In socially monogamous bird species with high rates of extrapair paternity, traits or environmental contexts affecting the number of within-pair young (WPY) produced by males can differ from those affecting the number of extrapair young fathered (EPY). Here, we use a 4-year dataset collected in contrasted environments to assess the factors affecting male reproductive success in tree swallows (Tachycineta bicolor), a species showing high levels of extrapair paternity. Our analyses revealed that the number of WPY was higher under better environmental conditions, while the number of EPY was mainly related to male characteristics. Males nesting in more intensive agricultural areas had fewer WPY produced and a lower reproductive success. Also, males breeding earlier in the season had more WPY. The presence of parasites reduced males’ reproductive success, mainly by reducing the number of EPY. The influence of male phenotype varied according to population density: Tarsus length variation had a greater effect on reproductive success at low population density than at high density, while wing length was also positively related to the number of EPY, more so at high than at low density. Altogether, our results suggest a complex interplay between individual and environmental determinants of reproductive success and imply that sexual selection dynamics varies depending on environmental contexts.

Parent-environmental interactions shape acoustic signatures in tree swallows: a cross-fostering experiment

Acoustic signatures are common components of avian vocalizations and are important for the recognition of individuals and groups. The proximate mechanisms by which these signatures develop are poorly understood, however. The development of acoustic signatures in nestling birds is of particular interest, because high rates of extra-pair paternity or egg dumping can cause nestlings to be unrelated to at least one of the adults that are caring for them. In such cases, nestlings might conceal their genetic origins, by developing acoustic signatures through environmental rather than genetic mechanisms. In a cross-fostering experiment with tree swallows Tachycineta bicolor, we investigated whether brood signatures of nestlings that were about to fledge were attributable to their genetic/maternal origins or to their rearing environment. We found that the calls of cross-fostered nestlings did not vary based on their genetic/maternal origin, but did show some variation based on their rearing environment. Control nestlings that were not swapped, however, showed stronger brood signatures than either experimental group, suggesting that acoustic signatures develop through an interaction between rearing environment and genetic/maternal effects.

Social and Genetic Mating System of the American Golden-Plover

Shorebirds are exceptionally diverse in their social mating systems, and genetic analyses of a few species have revealed further variation in genetic mating systems. The ecological and evolutionary causes of this variation are largely unknown. We studied the mating system of American Golden-Plovers (Pluvialis dominica) at Barrow, Alaska, between 2004 and 2009. In this arctic population, birds bred in socially monogamous pairs, as has been seen in other populations, yet rates of philopatry and mate fidelity were low. We used microsatellite DNA markers to analyze parentage and found that most offspring originated from monogamous matings, but 8% of 131 offspring and 16% of 37 nests were the result of nonmonogamous matings. One nest was ambiguous; it was either a full clutch sired through extra-pair copulation or represented an instance of social polygyny. Despite wide variation in synchrony of breeding and density of nesting both within and among breeding seasons, these ecological variables were unrelated to mating patterns. We speculate that the low rate of pair fidelity and the high rate of extrapair paternity are linked, because the lack of familiarity between partners reduces benefits of monogamy. Further study of breeding behavior and rates of philopatry are needed to understand why, among socially monogamous shorebirds, the American Golden-Plover has high rates of extra-pair paternity.

The form and function of duets and choruses in Red-backed Fairy-wrens

In many avian species, both members of a pair or all members of a breeding group sing, often in duets or choruses. Previous studies indicate that duets often function in territorial defence. However, other potential functions, such as acoustic mate-guarding, need further study, because most species that have been studied have low or unknown rates of extra-pair paternity (EPP) and theoretical models predict species with moderate rates of EPP will guard more than those with very low or high rates. We conducted behavioural observations to describe the form of duets and test hypotheses for the function of duets in breeding groups of Red-backed Fairy-wrens (Malurus melanocephalus), a species with moderately high rates of EPP. Within duets, notes overlapped in frequency and time, rather than being antiphonally coordinated. Duets and choruses occurred more in pre-breeding than other stages of breeding, and more in inter-group than intra-group contexts, supporting a territorial defence function. Contrary to predictions of an acoustic mate-guarding function, males did not duet with mates more when they were fertile. Likewise, functions of breeding coordination and group establishment were not supported. Thus, Red-backed Fairy-wrens may use duets for territorial defence rather thanmate-guarding, despite their moderately high rates of EPP. Investigating how vocal behaviour varies across different mating systems allows us to test theoretical predictions and determine how mating system affects the evolution of signalling strategies in birds and other taxa.

Dalliances and doubtful dads: what determines extra-pair paternity in socially monogamous wandering albatrosses?

Genetic techniques have revealed surprisingly high rates of extra-pair paternity (EPP) in socially monogamous albatrosses. We sought to establish social and genetic influences on EPP in wandering albatrosses (Diomedea exulans) at Marion Island, where EPP rates were 14–24 % in three successive seasons. EPP probably resulted from both female solicited extra-pair behaviours and male forced copulations. EPP was not linked to breeding experience nor with poor reproductive performance, despite a tendency for pairs to consistently produce either EPP or within-pair paternity (WPP) chicks. Mate guarding may inhibit extra-pair behaviour; however, parental arrival date and presence in the colony prior to laying did not correlate with EPP. There was little support for genetic advantages to producing EPP chicks, but the population is characterised by low genetic variability, which may result in mate incompatibility. Mates of pairs that failed and pairs producing EPP young tended to be more similar genetically to their partners than mates producing WPP young, suggesting that EPP may counter mate incompatibility. EPP and WPP chicks grow equally well, so cuckolded males did not reduce investment in EPP chicks. The lack of discriminatory behaviour by cuckolded males together with low genetic diversity in the population may allow continued high levels of EPP. In albatrosses, pair bonds are typically long lasting and the costs of forming new pairings may discourage mate swapping. Females may undertake extra-pair copulations as an adaptive alternative to mate swapping because the costs of extra-pair behaviour are small.