How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).     

Timing of copulations and the pattern of paternity in relation to laying order in tree swallows Tachycineta bicolor

It is well established that extra-pair young are present to varying degrees in nests of most avian species. However, the timing of extra-pair copulations during a female's fertile cycle is not well known, nor is how these copulations translate into the distribution of extra-pair young within the laying sequence. We determined the rates of successful within-pair copulations where at least one cloacal contact was achieved, and the number of extra-pair copulations/attempts in 17 pairs of tree swallows Tachycineta bicolor during the mornings encompassing the female's fertile period. We also examined nestling paternity with respect to laying order in eighteen mixed-paternity tree swallow broods. The rate of successful within-pair copulations peaked three days prior to a female laying her first egg, and decreased steadily throughout the laying period. We therefore predicted that extra-pair young would be more likely to hatch out of later-laid than earlier-laid eggs within a female's brood. We found no evidence of an increased frequency of extra-pair young with laying order. Instead, extra-pair young appear to be randomly distributed within the laying sequence of tree swallows.     

Do extra‐pair paternities provide genetic benefits for female blue tits Parus caeruleus?

A large body of theories on extra-pair paternity (EPP) in birds has proposed four main "genetic" hypotheses to explain this behaviour: the "good genes" hypothesis, the genetic diversity hypothesis, the genetic compatibility hypothesis and the fertility insurance hypothesis. Empirical tests have been scarce, mainly because high sample sizes are difficult to collect. We have tested these hypotheses in three Mediterranean populations of blue tits Parus caeruleus in which 50–68% of the broods contained extra-pair young. Results showed that the distribution of extra-pair young among broods was not random, and that survival to fledging of extra-pair young was higher than that of their within-pair sibs. These results support the idea of genetic effects benefiting extra-pair young. However, comparison of cuckolded and cuckolding males showed no significant difference in their body size, age, survival or relatedness with their paired females, and offspring morphometrics did not differ between extra-pair and within-pair young. We conclude that none of the genetic hypotheses can explain fully the high level of extra-pair paternity, at least in our populations of Mediterranean blue tits. We suggest that direct ecological benefits of EPP for females should be tested more often in correlative as well as experimental approaches.     

Genetic evaluation of the mating system in the blue-and-yellow macaw (Ara ararauna, Aves, Psittacidae) by DNA fingerprinting

More than 90% of birds are socially monogamous, although genetic studies indicate that many are often not sexually monogamous. In the present study, DNA fingerprinting was used to estimate the genetic relationships between nestlings belonging to the same broods to evaluate the mating system in the socially monogamous macaw, Ara ararauna. We found that in 10 of 11 broods investigated, the nestlings showed genetic similarity levels congruent with values expected among full-sibs, suggesting that they shared the same parents. However, in one brood, the low genetic similarity observed between nestlings could be a result of intraspecific brood parasitism, intraspecific nest competition or extra-pair paternity. These results, along with available behavioral and life-history data, imply that the blue-and-yellow macaw is not only socially, but also genetically monogamous. However, the occurrence of eventual cases of extra-pair paternity cannot be excluded.     

Cuckoldry as a cost of polyandry in the sex-role-reversed wattled jacana,Jacana jacana

In this paper we provide the first molecular genetic data on extra-pair paternity in a simultaneously polyandrous, sex-role-reversed avian species, the wattled jacana (Jacana jacana). Female jacanas often copulated with multiple mates, provided that the mates were not actively incubating eggs or tending young chicks. Both the presence of multiple ''available'' mates, and the copulation behaviour of the female near the time of nest initiation, significantly predicted the probability of extra-pair fertilizations. A male''s risk of being cuckolded was 0% in monandrous pairings, rose to 41% of broods (17% of chicks) in polyandrous associations where an additional mate was ''available'', and increased to 74% of broods (29% of chicks) where the female was observed to copulate with multiple mates. Unlike findings from several sequentially polyandrous bird species, few if any fertilizations resulted from sperm stored from a previous nesting. We conclude that lost paternity can constitute a very real cost of polyandry for male wattled jacanas. The source of this cost is sexually active males simultaneously paired to the same female.     

Do Female Red-winged Blackbirds Engage in a Mixed Mating Strategy?

Parentage analyses of broods of nestling red-winged blackbirds (Agelaius phoeniceus) revealed that extra-pair fertilizations (EPFs) accounted for 24% of the offspring. 8% of attempted copulations and 13% of male courtship displays during observations of focal females were by extra-pair males. In addition, mates and non-mates often chased and occasionally made physical contact with females; 34% of those chases in which contact was made were extra-pair chases. Females behaved variably during both within-pair and extra-pair events; females crouched less and resisted more frequently during extra-pair courtship than during within-pair courtship. All extra-pair events, whether natural or induced by male removal, were either resisted or accepted by the female. In 318 focal female-hours of observation during the fertilizable period, no female was ever seen in another male's territory soliciting a copulation. In addition, removal of females' mates resulted in frequent extra-pair courtship and copulation; all of these occurred on the removed male's territory. Some females left their mates' territories on occasion — these forays were nearly always off the study area, no female was ever seen copulating with an extra-pair male while on these forays, and neither the frequency nor the duration of female forays correlated with the frequency of extra-pair fertilizations within broods. There were no associations between extra-pair fertilizations and female age, settlement order, nest order, or clutch size. The number of fledglings produced from a nest was significantly positively associated with the number of sires of the brood. Fewer offspring apparently starved in broods that were multiply sired, yet males did not provide courtship feedings during either within-pair or extra-pair copulations, nor was any paternal care provided to young sired through extra-pair matings. The frequency of infertile eggs was low (< 1%); in those instances of infertile eggs the territory owner sired some young in the same nest or another nest on his territory. Fewer broods were a mixture of within-pair and extra-pair paternity than expected by chance. Clear evidence implicating a mixed strategy on the part of females could not be gathered. Because females behaved variably and because not all costs and benefits to females of extra-pair copulations could be measured, it remains possible that female behavior patterns are either (1) part of a mixed strategy, or (2) part of a strategy minimizing the costs of copulation.     

Genetic evidence for extra-pair fertilizations in a monogamous passerine, the Great Tit Parus major

The incidence of extra-pair paternity in a Great Tit Parus major population at Wytham Wood, Oxford, in 1985–1987 was determined using two polymorphic allozymes. In 831 nestlings from 94 broods, 27 genetic exclusions were detected in 25 (3%) nestlings from 16 broods. Seven (44%) of these broods contained offspring that excluded the putative male parent from being the genetic parent. The distribution of exclusion types indicated that excluded offspring were the result of fertilizations by extra-pair males and not of egg-dumping. The true frequency of extra-pair paternity was estimated as 14% of offspring. These results suggest a mixed reproductive strategy for males in which they breed mo-nogamously whilst simultaneously seeking extra-pair matings with females of other pairs.     

No evidence of genetic benefits from extra-pair fertilisations in female sand martins (Riparia riparia)

Genetic parentage studies of socially monogamous birds reveal a widespread prevalence of extra-pair paternity. Variation in extra-pair paternity among individuals may depend on how different individuals benefit from extra-pair fertilisations and on the opportunity to pursue extra-pair copulations. A long-term study of sand martins (Riparia riparia) in Hungary allowed us to examine patterns of extra-pair fertilisations in a large colony of over 3,000 breeding pairs with many known age individuals. We used multi-locus DNA fingerprinting to determine whether extra-pair fertilisations occur when females are paired to (1) presumably low quality mates, or (2) genetically similar or dissimilar mates, and whether extra-pair fertilisations result in offspring of higher quality. Extra-paternal young were found in 38% of 47 broods and comprised 19% of 190 offspring. Males that lost paternity did not differ significantly from others in age or body condition. Social mates of broods containing extra-pair offspring did not differ in genetic similarity from pairs without extra-pair offspring. Furthermore, there was no significant difference in body condition between extra-pair young and their maternal half-siblings. We were unable to assign paternity and therefore cannot exclude the possibility that extra-pair males differed from the within-pair males they cuckolded, in age, body condition or genetic similarity with the female. We found a positive relationship between paternity losses and breeding density, suggesting that low breeding density may constrain opportunities for seeking extra-pair copulations.     

Extra-pair paternity in birds: explaining variation between species and populations

Molecular techniques used to assign paternity have revealed previously unknown incidences of extra-pair paternity in socially monogamous bird species. DNA fingerprinting has now been used sufficiently often for mating-system biologists to appreciate the natural variation in the frequency of broods showing extra-pair young. The variation between species and between populations of the same species is surprisingly marked. Explaining this variation may help us to understand the factors promoting sexual selection. Recent comparative studies and detailed behavioural studies suggest that factors such as breeding density, genetic variation in the population and the intensity of sexual conflicts determine the costs and benefits to males and females of engaging in extra-pair copulations, and therefore contribute to the variation among populations.     

Amplified fragment length polymorphism (AFLP) markers reveal extra-pair parentage in a bird species: the bluethroat (Luscinia svecica)

We tested the use of amplified fragment length polymorphism (AFLP) to assess the frequency of extra-pair parentage in a bluethroat (Luscinia svecica namnetum) population. Thirty-six families totalling 162 nestlings were analysed. Using a combination of three primer pairs, we reached an exclusion probability of 93% for the population. This probability can reach 99% considering families independently. We revealed that extra-pair fertilizations are very common: 63.8% of all broods contain at least one extra-pair young, totalling 41.9% of all young analysed. However, with the technique and the three primer pairs used it was not possible to attribute the parentage exclusions to extra-pair paternity, maternity or both. As brood parasitism has never been reported in this species, it seems likely that the exclusions are due to extra-pair males. This study shows that dominant AFLP markers can be useful for studying the mating system of taxa for which no microsatellite primers are available. This technique allows the approximate estimation of parentage exclusions despite the fact that it is not possible to know which parent has to be excluded.     

Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens

Despite great interest in the use of extra-pair mating as a tool for examining female choice and intersexual selection, the underlying assumption of female control has proved difficult to verify empirically. We combined microsatellite genotyping and radiotelemetry of fertile females in order to investigate mate choice in superb fairy-wrens Malurus cyaneus, the bird with the highest known rate of extra-pair fertilization. All five females radio tracked during the peak of fertility, two to four days before the first egg is laid, undertook pre-dawn forays. All extra-pair young produced by the female were sired by a male visited during their forays, indicating that females control extra-pair fertilizations. In a larger sample of paternity data, some broods were sired by two extra-group males. In virtually all the cases the territory of the two sires were on an identical linear trajectory from the female's territory. This again suggests that extra-group paternity in superb fairy-wrens is directly linked to female extra-territorial forays. In other species mixed paternity has been taken to indicate that females attempt to insure against infertile pairings or try to maximize the genetic diversity of their brood. However, in fairy-wrens the likelihood of multiple extra-group paternity increased greatly as females traversed more territories in order to mate, perhaps suggesting that females which foray further are more likely to have difficulties locating the preferred male.     

Experimental manipulation of timing of breeding suggests laying order instead of breeding synchrony affects extra-pair paternity in house sparrows

The timing of breeding may not only affect breeding patterns such as the overlap of chick rearing period with the peak in food availability but also the opportunity for extra-pair mating. A negative relationship has been predicted between extra-pair paternity and breeding synchrony, assuming that male extra-pair activity is traded against mate guarding and parenting duties. In contrast, if female ability to assess male quality is temporally constrained, sperm competition might be a positive function of breeding synchrony. Here we manipulated the progress of nesting by nest material exchange within nesting aggregations to see whether the timing of breeding affects extra-pair paternity in house sparrows. We found that late broods within nesting clusters contained extra-pair young more often than early broods, but breeding synchrony did not turn out to be a significant predictor of extra-pair paternity. Our study indicates that temporal constraints of male extra-pair activity may account for extra-pair paternity levels, but it is also possible that late-breeding females may accept extra-pair copulations to ensure egg fertilization.     

Extra-pair paternity in monogamous and polygynous Savannah sparrows,Passerculus sandwichensis

Extra-pair paternity can influence mating systems by affecting the fitness costs associated with polygyny. Polygyny is disadvantageous to males when the time and energetic demands of multiple pairings decrease either a male's success at gaining extra-pair fertilizations or his ability to ensure paternity among harem members. In Savannah sparrows,Passerculus sandwichensison Kent Island, New Brunswick, Canada, multilocus DNA fingerprinting of 136 adults and young revealed substantial female infidelity: overall, 31 of 92 young (33.7%) in 15 of 24 nests (62.5%) were the product of extra-pair fertilizations. Male mating status was a strong predictor of paternity. Each of seven monogamous females produced at least one extra-pair offspring, but only six of 11 primary females (54.5%) and two of six secondary females (33.3%) were unfaithful. As a result, nearly 80% of the young in nests of polygynous males resulted from within-pair fertilizations, compared with only 40% of the young in nests of monogamous males. Kent Island Savannah sparrows are simultaneously polygynous, and the absence of paternity costs associated with polygyny is surprising. The observed pattern of paternity suggests the operation of female choice, although male control of parentage cannot be excluded.     

Male extraterritorial forays, age and paternity in the socially monogamous reed bunting (Emberiza schoeniclus)

Genetic studies have shown that extra-pair paternity is widespread among socially monogamous bird species. Yet, the role of males and females and their behavior leading to this mixed reproductive strategy is poorly understood. Here, we analyze paternity in relation to male age and mating behavior in the socially monogamous reed bunting (Emberiza schoeniclus). We report a positive relation between male extraterritorial forays and success in obtaining extra-pair fertilizations. Extraterritorial forays tended to increase in frequency with male age and older males sired a larger number of extra-pair offspring than young males. Identified extra-pair sires were old in nine out of ten cases. The likelihood of being cuckolded was not affected by male age. Although based on correlative data, our results highlight age-dependent explorative male behavior as a key determinant for the understanding of extra-pair mating in the reed bunting. We do, however, emphasize the need for further studies to reveal the role of females in extra-pair copulations and fertilizations.     

Allocation of Male Parental Care in Relation to Paternity Within and Among Broods of the Common Yellowthroat (Geothlypis trichas)

The relationship between male parental care and paternity has been investigated in a number of avian species, but in many cases the influences of confounding factors, such as variation in male and territory quality, were not addressed. These sources of variation can be controlled for by making within-male comparisons between successive broods or within-brood comparisons between groups of fledglings in a divided brood. We studied the relationship between male parental care and paternity in the common yellowthroat ( Geothlypis trichas ) at three levels: between groups of fledglings in divided broods, between first and second broods of the same pair, and among all broods in the population. In this study we proposed three hypotheses: first, males in double-brooded pairs should provide relatively more parental care to broods in which they have higher paternity; secondly, after fledging and brood division, males should provide more care to related offspring; and finally, among all broods in the population, paternity should be related positively to male parental care. Brood division occurred in many of the broods studied; however, broods were not divided according to fledgling size or paternity. Furthermore, within divided broods, males fed within-pair and extra-pair fledglings at similar rates. For sequential broods of the same pair, male feeding rates were not associated with differences in paternity between broods. Among all broods in the population, males did not provide relatively less care to broods containing unrelated young. The lack of a relationship between male parental care and paternity suggests that either males cannot assess their paternity or the costs of reducing male parental care outweigh the benefits.     

大山雀的婚外父权调查

婚配制度作为一种进化稳定对策是动物对某一环境包括种群内部环境适应的结果,在动物生殖过程中具有重要意义.大山雀(Parus major)是一种广域分布物种,研究显示广域分布物种的形态、生理、行为、生态特征及婚配制度在不同地区或种群间存在显著差异,因此,该文选择了分布于中国辽宁仙人洞国家级自然保护区的大山雀(P.m.minor)种群开展其婚配制度研究.野外共采集了22巢大山雀亲代和子代血液样本.结果如下:(1)从11个微卫星位点中筛选出了8个多态性较好的微卫星位点用于大山雀父权鉴定,在母本已知的情况下确定父权的准确率可达99.98％;(2)巢内父权鉴定结果显示,31.8％ (7/22)的巢包含婚外父权,8.12％ (16/197)的子代为婚外子代.与其他森林雀形目鸟类相比,大山雀婚外子代的比例明显偏低(＜10％),每个存在婚外父权巢的婚外子代比例各异(55.6％～9.1％),且无明显规律.     

MEASURING THE EFFECTS OF PAIRING SUCCESS,EXTRA-PAIR COPULATIONS AND MATE QUALITY ON THE OPPORTUNITY FOR SEXUAL SELECTION

Sexual selection can act through variation in the number of social mates obtained, variation in mate quality, or variation in success at obtaining extra-pair fertilizations. Because within-pair fertilizations (WPF) and extra-pair fertilizations (EPF) are alternate routes of reproduction, they are additive, rather than multiplicative, components of fitness. We present a method for partitioning total variance in reproductive success (a measure of the opportunity for selection) when fitness components are both additive and multiplicative and use it to partition the variance into components that correspond to each mechanism of sexual selection. Computer simulations show that extra-pair fertilizations can either increase or decrease total variance, depending on the covariance between within-pair and extra-pair success. Simulations also suggest that for socially monogamous species, extra-pair fertilizations have a greater effect than variation in mate quality or pairing status on the opportunity for selection. Application of our model to data gathered for a population of red-winged blackbirds (Agelaius phoeniceus) indicates that most of the variance in male reproductive success was attributable to within-pair sources of variance. Nevertheless, extra-pair copulations increased the opportunity for selection because males varied both in the proportion of their social young that they sired and in the number of extra-pair mates that they obtained. Furthermore, large and positive covariances existed between the number of extra-pair mates a male obtained and both social pairing success and within-pair paternity, indicating that, in this population, males preferred as social mates also were preferred as extra-pair mates.     

Extra-pair paternity in the Skylark Alauda arvensis

We present the first quantitative data on the genetic breeding system of a lark (Alaudidae), the Skylark Alauda arvensis . Using a set of eight microsatellite loci isolated in a variety of passerine species, we genotyped 171 offspring from 52 broods of Skylark and detected 35 extra-pair offspring (20%), in 14 different broods (27%). All offspring matched their putative mother, so there was no evidence of intraspecific brood parasitism. Previous non-genetic studies had suggested that the species was predominantly socially monogamous, with only rare occurrences of social polygyny and polyandry, although some behaviours, such as mate guarding, did suggest the possibility of extra-pair copulations. The relatively high level of extra-pair paternity in this species is likely to affect the variation in male reproductive success because extra-pair paternity was non-randomly distributed amongst males, with those with shorter wings more likely to be cuckolded.     

Low incidence of extra-pair paternity in the colonially nesting common swift Apus apus

The frequency of extra-pair paternity in a wild colony of swifts Apus apus was determined by multilocus DNA fingerprinting in two successive breeding seasons. The data were used to examine the expectation that extra-pair paternity is frequent in colonial-nesting species, either for proximal reasons such as the increased opportunity for extra-pair matings, or because extra-pair matings are important in the evolution and maintenance of coloniality. Forty-two broods containing 88 chicks were analysed. The genetic analysis revealed four cases of extra-pair paternity (4.5% of chicks) from four (9.5%) nests. Rapid mate-switching was considered unlikely to be the cause of extra-pair paternity since three of the cases were in the nests of previously established breeding pairs. Extra-pair copulations were not observed, but were assumed to be the cause of extra-pair paternity. The data show that high levels of extra-pair paternity are not an inevitable feature of high-density nesting.     

社会性单配制鸟类婚外父权的发生和影响因素

一雌一雄单配制鸟类中,雌性个体与配偶外雄性发生交配的行为称为婚外交配,继而导致了婚外受精产生婚外子代的现象称为产生了婚外父权。婚外父权广泛存在于鸟类中,针对其发生和影响因素已经成为了鸟类行为生态学研究的热点。本文收集了近十年社会性单配制鸟类婚外父权方面的研究文献,从婚外父权的发生及其影响因素两个方面综述了单配制鸟类婚外父权的研究进展。婚外父权发生原因的探讨主要包括：1、从两性的角度探讨雌雄两性在婚外行为中不同的进化繁殖策略。雄性策略旨在增加自身的繁殖输出;有关雌性策略则提出了确保受精假说、食物供给假说、遗传利益假说等,但目前尚存争议;2、在遗传利益假说中较常见的又分为3个假说：“优秀基因”假说、“遗传相容性”假说和“遗传多样性”假说,该三种假说是针对雌性从遗传方面获得的利益而提出的,不断有报道指出雌性配偶选择会被潜在的雄性遗传特性所影响;3、非遗传利益——母系效应影响婚外父权的进化。一些研究指出遗传质量参数,如体重、身体大小、存活率和免疫应答等方面可能会存在母系效应。婚外父权发生的影响因素这里主要指环境因素,包括繁殖同步性、繁殖密度、栖息地环境、产卵及孵化时机等。由于物种不同,受到环境压力不同,导致婚外父权发生率千差万别。最后本文针对未来的研究方向做出了展望。尽管近十年的研究进一步解释了鸟类婚外父权现象,但是该领域仍然存在并且产生了许多新的未解决的问题,而相关实验操作和理论的完善是深入探讨这些问题的关键。