Social Mates Research Articles

Polygyny in the tree swallow Tachycineta bicolor: a result of the cost of searching for an unmated male

The costs imposed by parental care duties on an individual's future survival and reproduction generate conflicts because parents should attempt to minimize their investment in the present brood, and exploit the parental care of the other parent. This conflict is likely to contribute to cases of both polygamy and desertion. Here, we study the costs of polygyny in the tree swallow Tachycineta bicolor, using observations on 52 nests that were attended by polygynous males over 14 y. Both females mated to polygynous males paid reproductive costs at several stages of the nesting cycle. Clutches laid by social mates of polygynous versus monogamous males did not differ in size. However, initial brood sizes for polygynously mated females were lower because a higher proportion of their eggs failed to hatch. Likewise, fledging success was lower and nest predation rates were higher, perhaps reflecting the direct or indirect effects of reduced male attention. These results demonstrate that females pay a productivity cost when breeding with reduced male parental care. In contrast, polygynous males fledge on average more young than monogamous ones and clearly benefit from the association. We suggest that a mate‐search cost is leading to the few cases of polygamous males: although females are likely evaluating males for their prospective dedication to the breeding attempt, in a short‐lived bird with a short breeding season, the cost to females of searching for a more dedicated male is the risk of not breeding at all.

Effects of extrapair paternity and sex on nestling growth and condition in the collared flycatcher, Ficedula albicollis

Extrapair fertilizations (EPFs) have been found in most socially monogamous passerine species. EPFs are generally beneficial for males because they increase the number of sired offspring. The benefit accrued by females, however, is less obvious. Maternal benefits may involve fertility insurance, increased genetic variability of the offspring, and improved offspring quality via compatible genes or ‘good genes’. In a Hungarian population of the collared flycatcher, we investigated whether the occurrence of extrapair young (EPY) in a brood could be predicted by the traits of the females or their social mates, and whether EPY were superior to their half sibs in terms of growth and fledging condition. We found that 55.7% of the broods contained EPY. The females' participation in extrapair copulations (EPCs) was not related to any of the characteristics of their mates (body size, condition, wing and forehead patch size). The EPY did not differ from their half sibs in any measures of offspring quality. The half sibs had similar embryonic and postembryonic growth and fledged with similar body condition. Female body size was related to extrapair paternity: larger females were less likely to produce mixed-paternity broods. This suggests that the role of female traits in EPCs deserves more attention. We also found that male nestlings grew faster than females, although females could catch up by the time of fledging, so we argue that sex-dependent development should be taken into account in studies using nestling growth as a measure of nestling quality.

Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird

BackgroundEvidence of multiple genetic criteria of mate choice is accumulating in numerous taxa. In many species, females have been shown to pair with genetically dissimilar mates or with extra-pair partners that are more genetically compatible than their social mates, thereby increasing their offsprings' heterozygosity which often correlates with offspring fitness. While most studies have focused on genetically promiscuous species, few studies have addressed genetically monogamous species, in which mate choice tends to be mutual.ResultsHere, we used microsatellite markers to assess individual global heterozygosity and genetic similarity of pairs in a socially and genetically monogamous seabird, the black-legged kittiwake Rissa tridactyla. We found that pairs were more genetically dissimilar than expected by chance. We also identified fitness costs of breeding with genetically similar partners: (i) genetic similarity of pairs was negatively correlated with the number of chicks hatched, and (ii) offspring heterozygosity was positively correlated with growth rate and survival.ConclusionThese findings provide evidence that breeders in a genetically monogamous species may avoid the fitness costs of reproducing with a genetically similar mate. In such species that lack the opportunity to obtain extra-pair fertilizations, mate choice may therefore be under high selective pressure.

Paternity in the classical polyandrous black coucal (Centropus grillii)—a cuckoo accepting cuckoldry?

In birds, a high degree of paternal care is expected to correlate with a relatively low frequency of extrapair paternity. If females seek extrapair copulations, they may lose fitness because their partners may reduce paternal care. Conversely, a high degree of paternal care might give females extra opportunities to pursue extrapair copulations, whereas their mates are occupied with offspring care. The aim of this study was to investigate paternity in the classically polyandrous African black coucal. In this sex-role reversed species, males intensively invest in offspring care of altricial young. However, the likelihood of extrapair fertilizations through stored sperm or extrapair copulations seems very high because females lay up to 3 clutches for up to 3 males each. Using 9 novel, highly polymorphic microsatellite loci developed for black coucals, we determined paternity of 127 chicks from 35 nests. Of these, 18 chicks (14.2%) from 13 broods (37.1%) were not fathered by the social male. Black coucals thus have the highest average rate of extrapair paternity reported for any classically polyandrous species. Extrapair young were the result from both extrapair copulations with males outside the female’s group of social mates and stored sperm from previous mates. We suggest that males were unable to effectively guard their females to prevent extrapair paternity due to 1) the dense habitat they live in and 2) the onset of incubation before clutch completion. Key words: African black coucal, home range, paternal care, paternity, polyandry, sex-role reversal. [Behav Ecol]

Do male plumage and song characteristics influence female off-territory forays and paternity in the hooded warbler?

Extra-pair fertilizations are common in many socially monogamous species, and paternity studies have indicated that females may use male vocal performance and plumage ornaments as cues to assess male quality. Female off-territory forays may represent a key component of female choice and male extra-pair mating success, and female foray behaviour is expected to be strongly influ- enced by indictors of male quality. In this study, we examined how male song and ornamentation affect how often females left their territories, which males they visited and extra-pair paternity in a socially monogamous passer- ine, the hooded warbler (Wilsonia citrina). We radiotracked 17 females during the fertile period and quantified male vocal performance (song output and rate) and plumage characteristics (size of the black melanin hood and colour of the black hood, yellow cheeks and breast areas). We obtained blood samples and determined paternity at 35 nests including those of 14 females that we radiotracked. Eleven (65%) of the 17 females forayed off-territory, whilst fertile and female foray rate was positively correlated with the number of extra-pair young in the nest. Females that left their territories more frequently were paired with males that sang at a low rate. In addition, extra-pair mates had higher song rates than the social mates they cuckolded (5.3 songs/ min vs. 4.4 songs/min). Female off-territory forays or extra- pair paternity were not significantly related to male plumage characteristics. Our results indicate that a high song rate influences both the foray behaviour of a male's social mate and the likelihood that he will sire extra-pair offspring with neighbouring females.

GENETIC PARENTAGE AND VARIABLE SOCIAL STRUCTURE IN BREEDING SOUTHERN LAPWINGS

Abstract We examined the genetic mating system and social breeding structure of the Southern Lapwing (Vanellus chilensis), a shorebird that breeds in Brazil in secluded pairs or groups (3–4 adults). We never observed copulation between males or females of primary pairs with additional adults in groups; all recorded copulations were between primary pair members. Where DNA from primary males was available, we found mixed paternity in 18.8% of the broods (3 of 16), comprising 9.8% of the chicks (4 of 41). All broods containing young sired by different males occurred in groups. One chick had a DNA fingerprint with four novel bands but shared a high proportion of bands with both primary pair members of its group. One explanation is that the chick's mother copulated with a relative of her social mate. However, quasi parasitism (i.e., nest-sharing by two females) cannot be excluded. Our study demonstrates a flexible social and genetic mating system in Southern Lapwings.

Male-Biased Sex of Extra Pair Young in the Socially Monogamous Red-Backed ShrikeLanius collurio

Females of many socially monogamous bird species engage in — or even actively seek — copulations outside their social pair bond. However, in socially monogamous birds with low breeding abundance, such as the Red-backed Shrike, extra-pair paternity (EPP) was thought to be an exceptional and random incident. Drawing on samples collect- ed in an unusually dense Red-backed Shrike population in the Czech Republic, we show through DNA microsatellite typing that among 65 chicks from 15 nests, 10 individuals (26.5%) had been sired by males other than the nest-attend- ing social mate. All 10 extra pair young were of male sex. In all cases, genetic fathers of extra pair young stemmed from neighbouring territories. Extra pair fathers had significantly longer tarsi than social mates, indicating that female choice was a function of age-class dependent male body size. Our findings support sex allocation theory, which suggests that promiscuous females mating with higher quality males should produce mostly sons.

The role of genetic relatedness among social mates in a cooperative breeder

Breeding with relatives can have severe fitness consequences, so avoiding these costs is often evolutionarily favored. There are a number of mechanisms that reduce the likelihood of mating with relatives, including avoiding relatives as mates (through sexbiased dispersal and mate choice) and delayed sexual maturity in the presence of relatives. Here, we examine these mechanisms in Neolamprologus pulcher, a group-living cichlid fish that exhibits male-biased dispersal. Despite sex-biased dispersal in this species, mean relatedness between social mates was not different from that expected if pairs had formed randomly, suggesting individuals neither actively avoid nor prefer pairing with relatives. Furthermore, gonadal investment of subordinates living in social groups was not correlated with their relatedness to the opposite-sex dominant breeder in the group, suggesting that sexual maturation does not depend on the presence or absence of a relative. Highly related social pairs showed higher rates of within-pair aggression and lower rates of nonaggressive social affiliation than less-related social pairs. Breeder investment and indicators of female breeder and group quality were not correlated with relatedness values between social mates. However, scraping rates (a potential quality indicator) were lower in males paired with more closely related females. We consider whether the apparent lack of inbreeding avoidance reflects an evolutionary history of limited breeding opportunities in N. pulcher or a facultative strategy of more-fit individuals and discuss the behavioral results in light of the suggested nonassortative mating with regard to relatedness.

Agricultural management affects evolutionary processes in a migratory songbird

Hay harvests have detrimental ecological effects on breeding songbirds, as harvesting results in nest failure. Importantly, whether harvesting also affects evolutionary processes is not known. We explored how hay harvest affected social and genetic mating patterns, and thus, the overall opportunity for sexual selection and evolutionary processes for a ground-nesting songbird, the Savannah sparrow (Passerculus sandwichensis). On an unharvested field, 55% of females were in polygynous associations, and social polygyny was associated with greater rates of extra-pair paternity (EPP). In this treatment, synchrony explained variation in EPP rates, as broods by more synchronous females had more EPP than broods by asynchronous females. In contrast, on a harvested field, simultaneous nest failure caused by haying dramatically decreased the overall incidence of EPP by increasing the occurrence of social monogamy and, apparently, the ability of polygynous males to maintain paternity in their own nests. Despite increased social and genetic monogamy, these haying-mediated changes in mating systems resulted in greater than twofold increase in the opportunity for sexual selection. This effect arose, in part, from a 30% increase in the variance associated with within-pair fertilization success, relative to the unharvested field. This effect was caused by a notable increase (+110%) in variance associated with the quality of social mates following simultaneous nest failure. Because up to 40% of regional habitat is harvested by early June, these data may demonstrate a strong population-level effect on mating systems, sexual selection, and consequently, evolutionary processes.

The mask of seniority? A neglected age indicator in house sparrows Passer domesticus

S. Nakagawa, (correspondence) and T. Burke, Department of Animal and Plant Sciences, University of Sheffield, S10 2TN, UK. Email:itchyshin@yahoo.co.nzIn many species, females prefer older males as social and genetic mates, and male secondary sexual traits often act as ageindictor mechanisms. It has been reported that almost all the extra-pair paternity in one population and recently inanother population of house sparrows Passer domesticus, was achieved by males more than one year old. We aimed todetermine whether there is a morphological trait that distinguishes yearlings from older males in house sparrows. Here,we report that such a trait the extent of black around a male’s eye, which we term the ‘mask’ or ‘mask of seniority’, is areasonable indicator of male age, being adequate to assign yearlings and older males correctly 81% of the time. It is wellknown that a male’s black throat patch, often called the ‘badge’ or ‘badge of status’, signals fighting ability. We speculatethat badge size signals dominance, and is therefore often used in male male competition, whereas mask size may play akey role as an age indicator mechanism, potentially used in female choice. It is surprising that this important trait evadedresearchers’ attention during 20 years of house sparrows being a model organism for sexual selection.

Within-pair young are more immunocompetent than extrapair young in mixed-paternity broods of the red bishop

Two competing hypotheses are commonly used to explain matings with multiple males in female birds. The genetic benefit model sees extrapair copulations as a means to enhance offspring viability, while the fertility-insurance hypothesis states that females copulate with multiple males to guarantee fertilization of eggs. According to the genetic benefit hypothesis, extrapair young are expected to have a genetic advantage over their maternal half-sibs raised in the same brood. A quantifiable measure for offspring quality is the immunocompetence, the ability of an individual to cope with infections. In this study, we used the phytohaemagglutinin induced skin-swelling response technique to test whether the cell-mediated immune reaction differs between extrapair and within-pair nestlings from mixed-paternity broods in the polygynous red bishop, Euplectes orix. The strength of the nestlings' immune response was positively linked to general health status and immunological condition of their genetic fathers, indicating a heritable component of nestling immunocompetence. We found that extrapair young were actually significantly less immunocompetent than within-pair young from the same nest, a result that does not lend support to the genetic benefit hypothesis. We suggest that female red bishops mated to successful high-quality males engage in extrapair copulations to insure against temporary infertility in their social mates caused by sperm depletion because of frequent copulations with their multiple female partners. This result, however, was significant only in the hotter of 2 years, indicating that environmental factors can obscure variation in nestling fitness arising from female extrapair mating behaviour.

Mating Behavior of Reed Buntings (Emberiza schoeniclus) in Captivity

We studied sexual pair behavior and cuckoldry of nine female and five male Reed Buntings (Emberiza schoeniclus) in a large outdoor aviary. Three males established small territories and paired with females. We observed 23 copulation attempts with identified partners during a period of approximately 6 weeks, 10 between social mates, 12 between unpaired females and paired males (extrapair for males), and one between a paired female and a paired male which was not the social mate (extrapair for both). Both males and females initiated copulation attempts which, in most cases, were preceded by precopulatory displays. No forced copulations were observed and females appeared to have an active role in mating behavior.

Paternity and performance of golden-winged warblers (Vermivora chrysoptera) and golden-winged X blue-winged warbler (V. pinus) hybrids at the leading edge of a hybrid zone

We examined two components of reproduction in a population of golden-winged warblers in the initial stages of hybridization with blue-winged warblers. First, we used genetic analyses of mate choice to determine whether copulations outside the social pairbond (extra-pair copula- tions; EPCs) occur in these species and their hybrids. Second, we compared several aspects of reproduction (pairing success, clutch size, hatching success, fledging success, and loss of paternity) in nests raised by phenotypic golden-winged warblers to those raised by hybrid individ- uals. Together, these data provide us with the first quantitative analysis of reproduction within this hybrid system. Our data suggest several reasons why the level of hybridization between these species is likely being under- estimated. First, many birds in our population showed only subtle phenotypic signs of introgression indicating that hybrid status can only be determined by close examination. Second, high rates of extra-pair paternity indicate that we cannot base our estimates of hybridization on pairbond data alone. More than 30% of nestlings were the result of EPCs, occurring in 55% of all nests. Third, there was no difference in the number of hybrid or "pure" golden-winged warbler males chosen as social mates, relative to their abundance. Indeed, based on several components of nesting success, it appears as though hybrids are having as great realized reproductive success as are phenotypic golden-winged warblers in our population. Accordingly, we argue that hybrid reproductive success and extra-pair fertilizations are likely playing a major role in the ongoing hybridization between blue-winged and golden-winged warblers. Studies such as this one are important to our understanding of the process and implications of hybridization, and findings may be applicable to other hybrid zones.

Song and female choice for extrapair copulations in the sedge warbler, Acrocephalus schoenobaenus

Although 90% of passerine birds live in socially monogamous pair bonds, molecular studies have revealed that genetic polygamy occurs in 86% of surveyed passerines, because individuals engage in copulations outside the pair bond (extrapair copulations; EPCs). Most explanations for the occurrence of EPCs involve female gaining indirect benefits from the extrapair male. The sedge warbler is a socially monogamous species in which some offspring result from EPCs (8% in this study). Complex song is a sexually selected male trait used by females which select mates based on a variety of male qualities. We used microsatellite DNA profiling to detect extrapair young and assign paternity. ‘Good genes’ theory predicts that females should engage in EPCs with males of higher quality than their social mate, with resulting fitness benefits. Extrapair males had smaller song repertoires and smaller territories than the social mate. This apparent preference for small-repertoire males as extrapair mates conflicts with the predictions from previous studies of this species. Sudden cessation of song after pairing may mean that song cues are unavailable for later extrapair matings and females may switch to other cues. Such behaviour may lead to different patterns of female choice during social and extrapair mating in the sedge warbler. We conclude that multiple reasons underlie patterns of female choice in this species.

Social common mole-rats enhance outbreeding via extra-pair mating

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.

Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows

High genetic similarity or dissimilarity between parents may result in viability consequences for offspring. However, because female choice of a social mate often reflects access to resources or male parental care, optimal genetic complementarity may be unattainable for social pairs. Thus, extrapair copulations may serve to increase offspring viability by allowing females to obtain sperm from males with more compatible genomes than those of social mates. We investigated whether parental genetic similarity influences offspring viability, including immunocompetence, in house sparrows, Passer domesticus. We also explored whether genetic similarity of social mates predicts the prevalence of young sired through extrapair fertilizations, and whether females enhance offspring viability by engaging in extrapair matings. We used DNA fingerprinting to estimate genetic similarity between social mates, and we assessed offspring viability using two measures of nestling immune response, the phytohaemagglutinin skin test and heterophil:lymphocyte ratios, plus nestling body mass and hatching success. We found no associations between the genetic similarity of parents and offspring immunocompetence, mass or hatching success; however, parental genetic similarity was positively correlated with clutch size. Genetic similarity of social mates also did not predict the frequency of extrapair young. Furthermore, maternal half-siblings within broods of mixed paternity did not differ in immunocompetence. Thus, our results provide no evidence for enhancement of offspring viability as an incentive for female engagement in extrapair copulations.

Dawn song of eastern kingbirds: intrapopulation variability and sociobiological correlates

AbstractWe quantify the singing behaviour of eastern kingbirds (Tyrannus tyrannus) in the 'dawn song' period to describe variation in performance, identify sources of variation, and identify the main recipient(s) of the information conveyed in the display. All males (N = 87) participated in dawn song, but the probability that a male did not sing increased if he was relatively isolated, and it was late in the season. The earliest and longest song bouts were made by males with many neighbours and when population level female fertility was high. High song rates were typical of males in dense nesting assemblages, early in the season and nest cycle, and when social mates were infertile. However, among males with active nests, song rates varied only with neighbour density and either date or population level female fertility. Given the strong inverse correlation between population fertility and date, we suspect that population fertility drove the relationships. The association of start time and song rate with population fertility, continuation of dawn song after territory establishment, and depressed song rate when mates were fertile, are all consistent with the hypothesis that the availability of extra-pair females is the primary factor selecting for male participation in dawn song.

Evaluating molecular and behavioural sexing methods for the Australasian gannet (Morus serrator)

The availability of molecular methods for avian sex identification has revolutionised the study of sexual differences in behaviour, morphology, life-history traits and conservation management. We implemented the recommendations of a recent review of DNA-based sex-identification by (1) verifying the sex-specificity and (2) estimating the accuracy of different sex-assignment methods in an apparently monomorphic seabird, the Australasian gannet (Morus serrator). The polymerase chain reaction (PCR) method based on the amplification of the sex-linked chromodomain-helicase-DNA binding gene (CHD) repeatedly assigned the same sex in 96% (n = 27 replicates) and correctly sexed all individuals with known gonadal anatomy (n = 6). PCR and sex-specific restriction fragment length polymorphism (RFLPs) showed agreement for 99.5% of individuals (n = 201). DNA-sexed pairs known to be social mates consisted of a male and a female in 96% of pairs sexed by PCR (n = 77) and 98% of pairs sexed by RFLP (n = 65). DNA-sexed females were in the bottom and males in the top copulatory position in 86% of observed copulations (n = 43 individuals). These results validate assumptions that both membership in social pairs and different copulatory positions can serve as reliable behavioural proxies for field-based sex identification in this colonial and obligately biparental seabird.

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.

Ecological correlates of extra-group paternity in mammals

Extra-group paternity (EGP) can form an important part of the mating system in birds and mammals. However, our present understanding of its extent and ecology comes primarily from birds. Here, we use data from 26 species and phylogenetic comparative methods to explore interspecific variation in EGP in mammals and test prominent ecological hypotheses for this variation. We found extensive EGP (46% of species showed more than 20% EGP), indicating that EGP is likely to play an important role in the mating system and the dynamics of sexual selection in mammals. Variation in EGP was most closely correlated with the length of the mating season. As the length of the mating season increased, EGP declined, suggesting that it is increasingly difficult for males to monopolize their social mates when mating seasons are short and overlap among females in oestrus is likely to be high. EGP was secondarily correlated with the number of females in a breeding group, consistent with the idea that as female clustering increases, males are less able to monopolize individual females. Finally, EGP was not related to social mating system, suggesting that the opportunities for the extra-group fertilizations and the payoffs involved do not consistently vary with social mating system.