Rates Of Extra-pair Paternity Research Articles

Microsatellite analysis detects low rate of extra-pair paternity in Tengmalm's owl,Aegolius funereus

Abstract. Genetic methods enable to reveal cryptic parental contributions in reproduction, especially in socially monogamous species. The rate of extra-pair paternity is generally low in raptors and owls and its presence in some species is tightly associated with sequential polyandry which can rarely occur in years with high food availability. In this study we investigated the mating system of the Tengmalm's owl (Aegolius funereus) in the Ore Mountains (Czech Republic). In this area, the species usually nests in high breeding densities which could increase an opportunity for extra-pair copulations. In total, 297 individuals (54 females, 47 males and 196 juveniles) from 46 nest boxes were genotyped at seven microsatellite loci. We present results of a five-year study and four extra-pair nestlings (2.3 %) were detected which did not result from sequential polyandry.

Affairs happen-to whom? A study on extrapair paternity in common nightingales.

Most birds engage in extrapair copulations despite great differences across and within species. Besides cost and benefit considerations of the two sex environmental factors have been found to alter mating strategies within or between populations and/or over time. For socially monogamous species, the main advantage that females might gain from mating with multiple males is probably increasing their offspring’s genetic fitness. Since male (genetic) quality is mostly not directly measurable for female birds, (extrapair) mate choice is based on male secondary traits. In passerines male song is such a sexual ornament indicating male phenotypic and/or genetic quality and song repertoires seem to affect female mate choice in a number of species. Yet their role in extrapair mating behavior is not well understood. In this study, we investigated the proportion of extrapair paternity (EPP) in a population of common nightingales Luscinia megarhynchos. We found that EPP rate was rather high (21.5% of all offspring tested) for a species without sexual dimorphism and high levels of paternal care. Furthermore, the occurrence of EPP was strongly related to the spatial distribution of male territories with males settling in densely occupied areas having higher proportions of extrapair young within their own brood. Also, song repertoire size affected EPP: here larger repertoires of social mates were negatively related to the probability of being cuckolded. When directly comparing repertoires sizes of social and extrapair mates, extrapair mates tended to have larger repertoires. We finally discuss our results as a hint for a flexible mating strategy in nightingales where several factors—including ecological as well as male song features—need to be considered when studying reproductive behavior in monogamous species with complex song.

Extra-pair paternity in the black-headed gull: is it exceptional among colonial waterbirds?

Although nesting at high densities promotes frequent interactions with individuals other than social mates, the rate of extra-pair paternity (EPP) in colonial waterbirds is generally low. So far, the highest EPP rate within this group has been reported in the black-headed gull Chroicocephalus ridibundus breeding in a colony in Czech Republic (33% broods with extra-pair offspring). In this study, we used a set of microsatellite loci to analyse parentage in 34 gull families (102 nestlings) from northern Poland. We recorded intra-specific brood parasitism in 10.8% of broods, but no evidence for EPP was found. The striking discrepancy between our results and previous estimates of EPP rate in the black-headed gull strongly indicate that promiscuity is a context-dependent strategy in this species and that its prevalence may greatly vary between populations. We recommend that a special care should be taken while using single-population data on EPP in the inter-specific comparative analyses.

The Sexual Proclivities of Northern Bobwhites

Mating systems and mating behavior are historically viewed as static characteristics of populations. ‘Monogamy’, ‘polygamy’, ‘multiple clutch polygamy’, ‘polyandry’, etc. imply most individuals express similar social and genetic mating patterns and characterize the behavior of most or all individuals in a given population. Mating systems of different populations of northern bobwhites (Colinus virginianus) have been described as monogamous, polygamous, multi-clutch polygamous, ambisexually polygamous, and polyandrous in contrast to the expectation that behavior, at the species level, fits defined categories. Prior studies of bobwhite breeding behavior, to arrive at these classifications, were based on observations of social interactions and did not incorporate genetic outcomes. Thus, it is challenging to discern whether social behaviors predict genetic outcomes and whether bobwhite mating behavior varies among populations or if behavior is flexible within populations. We used 3 years of field observations and variation at 14 microsatellite loci of 601 adult and 841 neonatal bobwhites to estimate rates of extra-pair paternity in bobwhite broods, evaluate the utility of social behavior as an indicator of genetic outcomes, and evaluate the fit of bobwhite social and genetic behavior to classic mating system theories. Extra-pair paternity occurred in >50% of bobwhite broods, whereas extra-pair matings resulted in few (x¯= 1.1) extra-pair offspring per nest. Social interactions between female and male bobwhites generally predicted the father of most offspring in a brood, but social interactions did not predict extra-pair matings better than chance. The mating behavior of individual females changed within and between breeding seasons, suggesting individual reproductive decisions of females were flexible. The mating ‘system’ of bobwhites meets neither the predictions nor the assumptions of classic mating theories.

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...

Cuckolded Fathers Rare in Human Populations

Contemporary data of extra-pair paternity (EPP) in human populations may be biased by the use of modern contraceptives. Studies have now estimated historical EPP rates in several human populations. The observed low EPP rates challenge the idea that women routinely 'shop around' for good genes by engaging in extra-pair copulations.

Subtle benefits of cooperation to breeding males of the Red-backed Fairywren

ABSTRACT Cooperative breeding is a phenomenon whereby breeding and nonbreeding individuals collectively provision young. Nonbreeding group members (“helpers”) may gain indirect and/or direct fitness benefits by breeding in a group, but there has been conflicting evidence regarding the benefits to breeders. In fact, the presence of helpers may sometimes be detrimental to aspects of breeder fitness. For example, in some species of the chiefly Australian genus Malurus, breeding males with helpers have lower within-pair paternity than do males without helpers. Additionally, indirect benefits to breeding males are often limited by low relatedness to their helpers due to high extrapair paternity rates, and helpers often appear to have minimal impact on breeder reproductive success. However, the presence of helpers may allow breeding males to shift their behaviors from guarding and provisioning young to alternative behaviors that affect other components of fitness, such as extraterritory forays (which might incr...

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.

Spatial patterns of extra-pair paternity in a waterbird colony: separating the effects of nesting density and nest site location.

Centres of avian colonies are usually associated with reduced predation risk and, thus, attract individuals of high quality, while poor-quality individuals are relegated to peripheral zones. Assuming that the incidence of extra-pair paternity (EPP) is dependent on individual quality, we could expect lower incidence of extra-pair offspring in the central parts of colonies. On the other hand, central pairs often nest in higher densities, which might increase EPP rate. To test these hypotheses, we sampled 124 great cormorant Phalacarocorax carbo sinensis chicks from 30 broods from different zones of a colony and genotyped them at seven highly polymorphic microsatellite loci. Sibship reconstruction confirmed the presence of at least one extra-pair chick in 30.0 % of broods. We found that EPP varied significantly between the zones of the colony, with higher incidence of extra-pair broods in the peripheral zone (53.3 vs. 6.7 % of broods). Centre-edge difference in EPP was consistent with the expected distribution of pair quality and suggested that poor-quality peripheral females were more likely to solicit extra-pair interactions, possibly to gain ‘good genes’ for their offspring. By contrast, we found no evidence for density dependence in EPP rate, indicating that likelihood of raising extra-pair offspring was not constrained by limited availability of local males. The results indicate that spatial randomization of sampling within avian colonies is critical to obtain robust estimations of EPP for non-solitary species. To our knowledge, this study provides the first evidence for the centre-edge difference in EPP within a breeding colony of birds.

Food Supplementation and Extrapair Paternity in House Sparrows

Abstract We tested whether food availability affects extrapair paternity in House Sparrows (Passer domesticus) by providing supplemental food at their nests during some fertile periods but not others. When comparing broods produced by the same pair, a higher proportion of broods contained at least one extrapair young when food supplements were present, although the difference was not significant, and the proportion of extrapair young per brood was higher when food supplements were present, although again the difference was not significant. There was also little evidence that the presence of food supplements affected the amount of time spent at the nest by males, females, or both sexes at the same time. We also conducted two smaller experiments designed to either increase or decrease the rate at which individuals encountered one another but found no concomitant increase or decrease in the rate of extrapair paternity. Overall, we found little evidence food distribution affects extrapair paternity in House S...

Sperm size evolution in African greenbuls (Passeriformes: Pycnonotidae)

Sperm morphology is highly diversified across the animal kingdom and recent comparative evidence from passerine birds suggests that postcopulatory sexual selection is a significant driver of sperm evolution. In the present study, we describe sperm size variation among 20 species of African greenbuls and one bulbul (Passeriformes: Pycnonotidae) and analyze the evolutionary differentiation of sperm size within a phylogenetic framework. We found significant interspecific variation in sperm size; with some genera exhibiting relatively long sperm (e.g. Eurillas) and others exhibiting short sperm head lengths (e.g. Phyllastrephus). However, our results suggest that contemporary levels of sperm competition are unlikely to explain sperm diversification within this clade: the coefficients of inter-male variation (CVbm) in sperm length were generally high, suggesting relatively low and homogeneous rates of extra-pair paternity. Finally, in a comparison of six evolutionary or tree transformation models, we found support for both the Kappa (evolutionary change primarily at nodes) and Lambda (lineage-specific evolutionary rates along branches) models in the evolutionary trajectories of sperm size among species. We therefore conclude that African greenbuls have more variable rates of sperm size evolution than expected from a neutral model of genetic drift. Understanding the evolutionary dynamics of sperm diversification remains a future challenge.

Spatiotemporal and genetic contingency of extrapair behaviour in a songbird

Multiple mating to obtain genetic benefits has been championed as the most likely cause of the evolution of polygamy. However, this assumption has been put into question by an increasing number of recent studies, most of which highlight the importance of considering ecological constraints to comprehend variation in extrapair (EP) behaviour. Here, we studied patterns of extrapair paternity (EPP) in the great tit, Parus major, using data from 11 nestbox plots that differed in population size and breeding conditions. Specifically, we analysed EPP rates in relation to socioecological variables that could influence the way individuals encountered one another in space and time, we tested whether adults engaged in EPP with more heterozygous, more compatible or phenotypically superior individuals than their social mates and we analysed whether extrapair offspring (EPO) were phenotypically or genetically superior to within-pair offspring. Our results do not provide support for the genetic benefit hypothesis from either the male or the female perspective. EPO were heavier than their within-pair paternal half-siblings, but there was no significant difference between EPO and their within-pair maternal half-siblings in terms of phenotypic quality. Regarding socioecological factors, we found a negative relationship between breeding synchrony and EPP rates both within and among plots, which suggests that males face a trade-off between mate guarding and obtaining EPP elsewhere. Our results show that most males engaged in EPP after the fertile period of their social female despite having to travel long distances: about half of the detected cases of EPP involved individuals from different woodlands. This study indicates that when and where to engage in EPP seem to be more relevant factors than with whom to do it and highlights the importance of considering spatiotemporal constraints at a landscape scale to achieve a better understanding of variation in EP mating behaviour.

Genetic diversity does not explain variation in extra-pair paternity in multiple populations of a songbird.

Many songbirds are socially monogamous but genetically polyandrous, mating with individuals outside their pair bonds. Extra-pair paternity (EPP) varies within and across species, but reasons for this variation remain unclear. One possible source of variation is population genetic diversity, which has been shown in interspecific meta-analyses to correlate with EPP but which has limited support from intraspecific tests. Using eight populations of the genetically polyandrous red-winged blackbird (Agelaius phoeniceus), including an island population, we investigated whether population-level differences in genetic diversity led to differences in EPP. We first measured genetic diversity over 10 microsatellite loci and found, as predicted, low genetic diversity in the island population. Additional structure analyses with multilocus genotypes and mtDNA showed the island population to be distinct from the continental populations. However, the island population's EPP rate fell in the middle of the continental populations' distribution, whereas the continental populations themselves showed significant variation in EPP. This result suggests that genetic diversity by itself is not a predictor of EPP rate. We discuss reasons for the departure from previous results, including hypotheses for EPP that do not solely implicate female-driven behaviour.

Increased hatching success as a direct benefit of polyandry in birds.

Multiple mating by females is difficult to explain in primarily socially monogamous taxa such as birds because mating outside the pair bond often provides no obvious benefit to females. Although indirect selection is often invoked to explain the evolution of polyandry, current evidence suggests that selection on indirect benefits of mating is weak. Here, I consider a direct benefit of remating in birds: increased fertilization success. I test whether increased hatching success of a female's eggs is related to rates of extra-pair paternity (EPP), a proxy of polyandry, across 113 bird species. I use two statistical approaches, control for phylogenetic uncertainty, and assess the fit of competing evolutionary models. Results show there is indeed a positive relationship between rates of EPP and hatching success in birds. I propose that by mating with many males, females may increase their fertility. I end by discussing the biological rationale for this explanation, alternative interpretations of the results, and how this study furthers our understanding of polyandry and mating system evolution.

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.

Extra-Pair Paternity in Varied TitsPoecile varius

Extra-pair paternity is of particular interest in socially monogamous species, in which there is a substantial discrepancy between social and genetic mating systems. Varied Tits Poecile varius are socially monogamous passerine birds with a distribution in Japan, Korea, and northeast China. We established paternity in all individuals of 40 broods by microsatellite genotyping. Extra-pair paternity occurred in 16 of the 40 broods (40%) and accounted for about 14.7% (37/251) of offspring, higher than the average value (11%) among socially monogamous birds. The relatedness between social partners did not correlate with the percentage of extra-pair offspring in the brood and there was no difference in heterozygosity between maternal half-siblings. As the first such investigation in this species, this study adds to our understanding of their mating system and will be useful for comparative studies of variations in extra-pair paternity rate.

Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys

Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara's owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.

High Urban Breeding Densities Do Not Disrupt Genetic Monogamy in a Bird Species

Urbanization causes widespread endangerment of biodiversity worldwide. However, some species successfully colonize cities reaching higher densities than in their rural habitats. In these cases, although urban city dwellers may apparently be taking advantage of these new environments, they also face new ecological conditions that may induce behavioural changes. For example, the frequency of alternative reproductive behaviours such as extra-pair paternity and intraspecific brood parasitism might increase with breeding densities. Here, using a panel of 17 microsatellites, we tested whether increments in breeding densities such as those associated with urban invasion processes alter genetic monogamy in the burrowing owl Athene cunicularia. Our results show low rates of extra-pair paternity (1.47%), but relatively high levels of intraspecific brood parasitism (8.82%). However, we were not able to detect differences in the frequency at which either alternative reproductive behaviour occurs along a strong breeding density gradient. Further research is needed to properly ascertain the role of other social and ecological factors in the frequency at which this species presents alternative reproductive strategies. Meanwhile, our results suggest that genetic monogamy is maintained despite the increment in conspecific density associated with a recent urban invasion process.