High levels of extra-pair paternity in an isolated, low-density, island population of tree swallows (Tachycineta bicolor)

Molecular genetic studies have suggested that apparently nonbreeding males ('floaters') may account for a significant proportion of extra-pair paternity (EPP) in avian populations. Attempts to determine the influence of breeding density on EPP are therefore confounded by the presence of a subpopulation of floaters whose numbers are difficult to estimate. To study EPP in a tree swallow (Tachycineta bicolor) population with few floaters, we chose a nestbox grid on an island with an excess of available breeding sites and very few floaters. We obtained DNA samples from 13 complete families and performed DNA profiling on them using four microsatellite loci. For comparison, we also obtained a sample of 58 extra-pair young (EPY) from a mainland population typed at five microsatellite loci. Paternity assignments among resident males in both populations were made using the microsatellite profiles and a likelihood-based statistical method. Of the 67 island nestlings typed, we found 37 (55%) nestlings from 11 (85%) different nests that were EPY. The proportion of nestlings that were EPY and the proportion of broods containing EPY did not differ significantly between island and mainland populations studied previously. There was no significant difference between island and mainland populations in the proportion of extra-pair paternities assigned among neighbouring resident males. Male breeding density does not appear to affect the ability of female tree swallows to obtain extra-pair fertilizations, at least over the range of densities studied so far. The rate of EPP has remained remarkably consistent over many years, studies and populations implying an important role of active female choice in determining EPP.     

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.     

Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment

The blue throat feathers of male bluethroats (Luscinia s. svecica) show a reflectance peak in the ultraviolet (UV) waveband (320 to 400 nm). The throat is actively displayed during courtship, suggesting a role for sexual selection on an ultraviolet signal. Indeed, a recent aviary experiment demonstrated that females discriminated against males with artificially reduced UV reflectance (Andersson and Amundsen 1997). Here, we report the results of a similar experimental manipulation applied on free-ranging males. UV-reduced (UVR) males had a lower success in attracting mates, as judged from a significantly later start of egg laying, compared with control (C) males. UVR males also spent significantly less time advertising for additional mates when their own mate was fertile, and they had a lower success in achieving extra-pair fertilizations. Furthermore, UVR males tended to guard their mates more closely and lose more paternity in their own brood than C males did. We conclude that the treatment affected both social and extra-pair mate choice. This is the first experimental evidence that UV signalling influences male mating success in free-ranging birds.     

Male mate choice, male availability and egg production as limitations on polyandry in the red-necked phalarope

In sequentially polyandrous birds, a female's second mate faces a substantial risk of cuckoldry due to rapid mate switching and stored sperm. Secondary males are potentially available to females because males arrive asynchronously and/or are recycled into the breeding pool following nest predation. In a study of red-necked phalaropes, Phalaropus lobatus, a sex-role reversed shorebird, we tested the hypotheses that the proportion of females that become polyandrous is proximately limited by: (1) the ability of females to produce eggs, (2) the availability of males as mates and (3) male mate choice. In a colour-banded population in which rates of nest loss were manipulated by researchers, females that produced second clutches required similar lengths of time to complete clutches as those contemporaneously producing first clutches, and increased their egg size relative to their first clutch, making egg limitation unlikely. There was no correlation between an annual measure of males' availability as potential mates following nest losses and the proportion of females that were polyandrous. The majority of males that lost clutches (66%) re-paired with their original female significantly more often than expected by random mate choice (P<0.0001). Although 76% of polyandrous nestings involved renesting males, only 6% (N=46) of renesting males changed mates if their original female was still available. Renesting males that changed mates did not select for or against females that had already produced clutches (NS). Our results suggest that the level of polyandry in this species is not constrained by the females' abilities to produce more eggs or by the number of males recycling back into the breeding pool. Instead, the proportion of females that become polyandrous is limited by males choosing to renest with their original females, thereby decreasing their probability of caring for eggs potentially fertilized by a female's previous mate.     

Explicit experimental evidence for the effectiveness of proximity as mate-guarding behaviour in reducing extra-pair fertilization in the Seychelles warbler

Extra-pair copulations (EPCs; copulations outside the pair bond) are widespread in birds and may result in extra-pair fertilizations (EPFs). To increase reproductive success, males should not only seek to gain EPFs, but also prevent their own females from gaining EPFs. Although males could reduce the number of EPCs by their mates, this does not necessarily mean that they reduce the number of EPFs; indeed several studies have found no association between EPCs and EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when the pair female is most receptive (fertile period). We show that males that guarded their mates more closely were less likely to have extra-pair young in their nest. This study on the Seychelles warbler is the first to provide explicit experimental evidence that mate guarding is effective in reducing EPFs. First, in territories where free-living males were induced to stop mate guarding during the pair female's fertile period, extra-pair parentage was higher than in the control group. Second, in the experimental group, the probability of having an extra-pair nestling in the nest was positively associated with the number of days during the fertile period for which mate guarding was artificially stopped. Thus, male mate guarding was effective in reducing the risk of cuckoldry.     

Sequential mating patterns suggest extra-pair mating is not part of a mixed reproductive strategy by female red-winged blackbirds

Studies aimed at determining why female birds often produce offspring sired by males other than their social mates generally compare traits of social and genetic mates. Here I examine paternity patterns in nests of the same female red-winged blackbirds (Agelaius phoeniceus) in successive breeding seasons. Returning females preferentially selected their former social mates as their new social mates when those males were present. However, paternity patterns were much less consistent. A female''s behaviour (faithful versus unfaithful) in one year did not predict her behaviour the following year. Females unfaithful in successive years did not prefer the same extra-pair males. Females unfaithful in one year that switched social mates the next year did not preferentially choose their former extra-pair mates as their new social mates. By switching genetic mates, females did not generally improve the quality of their mates. These results, together with previous analyses, suggest that female blackbirds in this population have little control over extra-pair mating. Although females may benefit from extra-pair mating because extra-pair males are generally longer lived, paternity patterns in this population are not consistent with extra-pair mating being part of a finely tuned female reproductive strategy.     

Sexual selection in the monogamous barn swallow (Hirundo rustica). II. Mechanisms of sexual selection

Mechanisms of sexual selection in the monogamous, sexually dimorphic barn swallow (Hirundo rustica) were studied during a seven-year period. First, the sex ratio of reproducing adults was male-biased, and mated males had significantly longer tail ornaments than unmated males. Secondly, some of the unmated individuals later committed infanticide and became mated with the mother of the killed brood. Fathers of killed broods had significantly shorter tails than other males, and there was a tendency for infanticidal males to have longer tail ornaments than other unmated males. Thirdly, long-tailed male barn swallows were more successful in acquiring extra-pair copulations than other males, and females involved in extra-pair copulations, as compared to females not involved in such copulations, had mates with shorter tail ornaments. Fourthly, male barn swallows having long tails as compared to short-tailed males acquired mates in better body condition. Females mated to long-tailed males reproduced earlier, laid more eggs and were more likely to have two clutches than were females mated to short-tailed males. Finally, females mated to long-tailed males put more effort into reproduction than did other females, as evidenced by their relatively larger contribution to feeding of offspring. Thus, at least five different components of sexual selection affected male reproductive success. Selection arising from differential success during extra-pair copulations, differential reproductive success and differential male reproductive effort thus accounted for most of the selection on tail ornaments in male barn swallows.     

No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows

Sex allocation theory predicts that parents should adjust investment in sons and daughters according to relative fitness of differently sexed offspring. In species with female preference for highly ornamented males, one advantage potentially accruing to parents from investing more in sons of the most ornamented males is that male offspring will inherit characters ensuring sexual attractiveness or high-quality genes, if ornaments honestly reveal male genetic quality. Furthermore, in species where extra-pair fertilizations occur, offspring sired by an extra-pair male are expected to more frequently be male than those of the legitimate male if the latter is of lower quality than the extra-pair male. We investigated adjustment of sex ratio of offspring in relation to ornamentation of the extra-pair and the social mate of females by direct manipulation of tails of male barn swallows Hirundo rustica . Molecular sexing of the offspring was performed using the W chromosome-linked avian chromo-helicase-DNA-binding protein (CHD) gene while paternity assessment was conducted by typing of hypervariable microsatellite loci. Extra-pair offspring sex ratio was not affected by ornamentation of their biological fathers relative to the experimental ornamentation of the parental male. Experimental ornamentation of the parental males did not affect the sex ratio of nestlings in their broods. Female barn swallows might be unable to bias offspring sex ratio at hatching according to the quality of the biological father. Alternatively, fitness benefits in terms of sexual attractiveness of sons might be balanced by the cost of compensating for little parental care provided by highly ornamented parental males, if sons are more costly to rear than daughters, or the advantage of producing more daughters, if males with large ornaments contribute differentially more to the viability of daughters than sons.     

Fitness consequences of divorce in the azure-winged magpie depends on the breeding experience of a new mate

Sexual conflict in producing and raising offspring is a critical issue in evolutionary ecology research.Individual experience affects their breeding performance,as measured by such traits of provisioning of offspring and engagement in extra-pair copulations,and may cause an imbalance in sexual conflict.Thus,divorce is hypothesized to occur within aged social pairs,irrespective of current reproductive success.This concept was explored in the azure-winged magpie Cyanopica cyanus by investigating the divorce of a social pair and its relationship to their changes in breeding performance with prior experience.Females engaging in extra-pair copulation may intensify sexual conflicts and may be the main reason for divorce.Once divorced,females repairing with an inexperienced male realized higher reproductive success than that repairing with an experienced male;males repairing with an experienced female realized higher reproductive success than that repairing with an inexperienced female.This finding indicates that the fitness consequence of divorce depends on the breeding experience of new mates.Divorced females can obtain more extra-pair copulations,whereas divorced males cannot,when they repair with inexperienced breeders.Divorced females provisioned a brood at lower rates than inexperienced females whereas divorced males had no such difference.It appears that divorced females can obtain an advantage in sexual conflicts with inexperienced mates in future reproduction.Consequently,females are probably more active than males in divorcing their aged mates so as to select an inexperienced male as a new mate.Azure-winged magpies thus provide novel insights into the implicaticns of sexual conflict in birds.     

Singing strategies among male Black-browed Reed Warblers Acrocephalus bistrigiceps during the post-fertile period of their mates

Bird song is critical to mate attraction. Because singing involves fitness costs, males that sing vigorous and complex songs are thought to be of high quality. Males of the Black-browed Reed Warbler Acrocephalus bistrigiceps sang actively when they were solitary, but stopped singing as soon as they had attracted a female. Males exhibited two distinct patterns of singing behaviour after the fertile period of their mates: some resumed singing, whereas others did not. Males that resumed singing acquired secondary females more frequently than those that did not sing, suggesting that resuming males seek polygynous mating. The occurrence of extra-pair fertilization was rare (6.4%) in the study population, and extra-pair young were sired by both resuming and non-resuming males. There is no strong evidence that non-resuming males compensate for their disadvantage in social mate acquisition by extra-pair paternity. Resuming males arrived at the breeding ground earlier, suggesting that they were high-quality males.     

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.     

Repeatability of extra-pair mating in tree swallows

Models of sexual selection assume that female mating preferences are heritable and, thus, repeatable for individual females across multiple mating episodes. Previous studies of the repeatability of female preference have examined individuals in captivity and focused presumably on social mate choice. However, extra-pair mating is widespread and can also influence sexual selection. We examined the repeatability of extra-pair mating in a wild population of tree swallows (Tachycineta bicolor) by experimentally inducing females to lay two clutches in rapid succession within the same season. We found that the proportion of extra-pair young and the number of extra-pair sires were highly repeatable for individual females. However, the repeatability of specific extra-pair sires was low. We suggest that this unusual pattern of mating may be due to females maximizing the heterozygosity of their offspring.     

Sperm Competition and Copulation Intervals of the White Spoonbill (Platalea leucorodia,Aves, Threskiornithidae)

Some aspects of sperm competition were studied in the white spoonbill (Platalea leucorodia) breeding in Doñana National Park (SW Spain). Shorter pair copulation intervals occurred during the prelaying period, when females were subjected to a relatively high frequency of extra-pair copulations. Pair copulation intervals with an intermediate extra-pair copulation by the male mate were longer than those without extra-pair copulation. This result indicates that males need a time of recovery between copulations before they can perform another. Extra-pair copulations by the females did not affect the length of intervals between pair copulations. There were no differences between the lengths of the intervals between an extra-pair copulation by the female and the following pair copulation for cases in which the male mate detected an intruder male attempting copulation with his mate and those in which the intruder remained undetected. However, the correlations obtained between copulatory intervals for detected and undetected cases suggest a copulatory response by their mates, although affected by the required recovery time between copulations by the males. Finally, since extra-pair copulations mainly occurred while male mates were collecting nest material, they engaged in this activity shortly after pair copulations, probably to avoid a last-male advantage under the sperm competition pressure.     

Female ground tits prefer relatives as extra‐pair partners: driven by kin‐selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female's engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female's nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative nongenetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.     

The ‘Widow Effect’ and its Consequences for Reproduction in Burying Beetles,Nicrophorus vespilloides (Coleoptera: Silphidae)

Burying beetles tend their young on small vertebrate carcasses, which serve as the sole source of food for the developing larvae. Single females are as proficient at rearing offspring as male-female pairs, yet males opt to remain with their broods throughout most of the larval development. One potential benefit of a male's extended residency is that it affords him the opportunity of additional copulations with the female, which could ensure his paternity in a replacement brood should the female's first egg clutch fail to hatch. We tested this hypothesis by manipulating males' access to their mates during the production of replacement clutches, using genetic colour markers to determine the paternity of offspring. Females were induced to produce a replacement brood by removing their first clutch of eggs. In one experimental treatment, we removed the female's mate upon the removal of her first egg clutch (‘widowed’ females); in a second treatment, the female was permitted to retain her mate up until she produced a replacement clutch. There was no significant difference in paternity between males removed from females before the initiation of replacement clutches and those permitted to remain with their mates. However, widowed females produced fewer offspring in replacement broods than did females permitted to retain their mates. This difference occurred primarily because a significantly greater proportion of widowed females opted not to produce a replacement clutch, a result we refer to as the ‘widow effect’. This widow effect was further shown in those replicates in which females of both treatments produced replacement clutches: widowed females took significantly longer to produce a replacement clutch than did females permitted to retain their mates. The loss of her mate could be a signal to a female that a take-over of the carcass is imminent. Her reluctance to produce a replacement clutch under these circumstances might constitute a strategy by which she conserves carrion for a subsequent reproductive attempt with an intruding male successful at ousting her previous mate. Regardless of its functional significance, the widow effect favours the extended residency of males and therefore contributes to the selective maintenance of male parental care.     

Fitness benefits of polyandry for experienced females

Females often mate with several different males, which may promote sperm competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in birds where recent reviews have suggested that females gain few genetic benefits from extra‐pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of sexual conflict.     

Extra-pair paternity in relation to male age in Bullock's orioles

Single-locus minisatellite DNA profiling was used to assign paternity in a population of Bullock's orioles, Icterus galbula bullockii, and to determine the contribution of age to a male's success in obtaining extra-pair paternity. There was a very low rate of intraspecific brood parasitism (2/202 = 1.0% of chicks). Older adult males lost less within-pair paternity and gained more extra-pair fertilizations than did yearling subadult males. This resulted in adult males benefiting from an annual reproductive success more than double that of subadult males. Behavioural observations, used to determine the role of female choice in extra-pair copulations (EPCs), indicated that females actively participate in EPCs and that they prefer to obtain them from older males. While it was possible that females obtained EPCs as an insurance against the possible infertility of their social mate, the results of this study fit best with the hypothesis that females were attempting to obtain better-quality genes for their offspring by obtaining EPCs with older, better-quality males.     

Male-male competition and parental care in collared flycatchers (Ficedula albicollis): an experiment controlling for differences in territory quality

Females are known to benefit from mate choice in several different ways but the relationship between these benefits has received little attention. The quality of resources provided by males, such as nest sites, and paternal care are often assumed to covary positively However, because the location of the nest affects the cost of parental care, these two benefits from mate choice can easily be confounded. To investigate the provisioning ability of successful competitors while controlling for differences in territory quality we removed early-settled pairs of collared flycatchers (Ficedula albicollis) and allowed replacement by later-arriving males or floaters (i.e.'poor competitors'). A control group of early-settled males (i.e. 'good competitors') had their females removed. Females paired to good competitors enjoyed a significantly higher reproductive success and tended to receive more parental assistance from their mates compared with females mated to poor competitors. Thus, some males seem able not only to compete successfully over resources but also to feed their offspring at a relatively higher rate. An alternative explanation, that poor competitors invested less in offspring quality in response to a lower share of paternity, could be rejected. The rate of extra-pair paternity did not differ between the two treatment groups. Our results suggest that male- male competition can sometimes facilitate female choice of superior care-givers. Thus, a female's benefit from choosing a competitive male may not be restricted to the quality of the resource he defends but can also include superior paternal care.     

Extra-pair young in house wren broods are more likely to be male than female

Sex-allocation theory predicts that females should preferentially produce offspring of the sex with greater fitness potential. In socially monogamous animal species, extra-pair mating often increases the variance in fitness of sons relative to daughters. Thus, in situations where offspring sired by a female''s extra-pair mate(s) will typically have greater fitness potential than offspring sired by the within-pair mate, sex-allocation theory predicts that females will bias the sex of offspring sired by extra-pair mates towards male. We examined the relationship between offspring sex and paternity over six breeding seasons in an Illinois population of the house wren (Troglodytes aedon), a cavity-nesting songbird. Out of the 2345 nestlings that had both sex and paternity assigned, 350 (15%) were sired by extra-pair males. The sex ratio of extra-pair offspring, 0.534, was significantly greater than the sex ratio of within-pair offspring, 0.492, representing an increase of 8.5 per cent in the proportion of sons produced. To our knowledge, this is the first confirmed report of female birds increasing their production of sons in association with extra-pair fertilization. Our results are consistent with the oft-mentioned hypothesis that females engage in extra-pair mating to increase offspring quality.     

Effects of site fidelity and breeding performance on mate retention in a short‐lived passerine,the tree swallow Thachycineta bicolor

We studied the relationship among re‐mating, site fidelity and breeding performance in the tree swallow Tachycineta bicolor using 16 y of data on reproductive biology in a population breeding in nest boxes near Ithaca, New York. Of 217 pairs for which both members survived the non‐breeding season, 76% mated with a new partner and 24% reunited with their previous mate. Pairs did not increase their breeding success by breeding together for more than one breeding season. Males produced fewer fledglings after breeding with a new partner, but females neither increased nor decreased their success when breeding with a new mate. Females who bred with a new partner were younger than females that reunited with their previous mates, and they were more likely to move to a different nest box. Males that bred with a new mate were of similar age to males that reunited, and they did not move more often. The probability of breeding with a new partner was better predicted by female age than by previous breeding success, suggesting that re‐mating was not strongly affected by past breeding performance. Because younger females change breeding sites more frequently than do older females and females that mated with a new partner were younger than females that reunited with their previous mates, we suggest that the tendency of tree swallows to change partners between years is a by‐product of lower site fidelity of younger females rather than a strategy for increasing breeding success.