Extra-pair Fertilizations Research Articles

Do female great reed warblers seek extra–pair fertilizations to avoid inbreeding?

Females of many species mate with several males. According to a recent hypothesis, female promiscuity serves to avoid inbreeding. We tested this hypothesis in a polygynous bird, the great reed warbler (Acrocephalus arundinaceus), in which extra-pair fertilization, inbreeding and inbreeding depression occur. However, the extra-pair males and social males did not differ in relatedness to the promiscuous females, nor did the least related males sire most of the females' chicks. Thus, contrary to recent findings in some insects, birds and reptiles, we found no evidence for inbreeding avoidance among the promiscuous females. Instead, female great reed warblers may seek other potential benefits when cuckolding, such as good gene effects at particular functional genes.

Extrapair paternity and offspring immunocompetence in the reed bunting, Emberiza schoeniclus

Female promiscuity is widespread in birds, as well as in other taxa. It is often assumed that in bird species with a socially monogamous mating system, females engage in extrapair copulations to obtain indirect (genetic) benefits. ‘Good genes’ and ‘compatible genes’ models predict that extrapair young (EPY) should be of higher quality than within-pair young (WPY), but the empirical evidence for this effect is limited. A recent study, however, indicated an enhanced cellular immunity in EPY in a passerine bird, the bluethroat, Luscinia svecica. To assess the generality of that finding, we replicated the study using the reed bunting, a passerine with an extrapair mating system similar to that of the bluethroat. Using the same immune assay protocol, we found no indication of enhanced cellular immunity in EPY compared with WPY. Female reed buntings thus do not seem to engage in extrapair copulations to achieve the same type of genetic benefit as in bluethroats. Furthermore, EPY in mixed-paternity broods did not grow faster and were not in better body condition close to fledging than WPY. We conclude that our results do not support the hypotheses assuming indirect benefits to female extrapair copulations. It appears that the adaptive value for females of pursuing extrapair fertilizations varies, even between species with similar extrapair mating systems.

Extrapair Paternity Increases Variability in Male Reproductive Success in the Chestnut-Sided Warbler (Dendroica Pensylvanica), A Socially Monogamous Songbird

Abstract A monogamous mating system that includes extrapair fertilization can potentially generate higher variability in male reproductive success than monogamy without extrapair fertilization. That increased variability could provide a correspondingly higher opportunity for sexual selection and, thus, for the origin and persistence of sexual dimorphism in monogamous species. To determine whether extrapair fertilization enhanced the opportunity for sexual selection in a sexually dimorphic, monogamous bird species, we used microsatellite DNA typing to assess the prevalence of extrapair fertilization and its effect on variation in male reproductive success in a population of Chestnut-sided Warblers (Dendroica pensylvanica). We found that the level of extrapair fertilization in our study population was at the upper end of the range reported for bird populations (47% of nestlings had extrapair fathers; 61% of broods contained extrapair offspring). We also discovered that almost all extrapair offspring were sired by paired males resident on nearby territories. In addition, we found that variation in male reproductive success was substantially higher than variation in female reproductive success, and that extrapair fertilizations made a significant contribution to variation in male reproductive success. Together, those findings suggest that extrapair fertilization creates an opportunity for sexual selection on male traits in this population.

Males achieve greater reproductive success through multiple broods than through extrapair mating in house wrens

In polygynous species, it is unclear whether extrapair matings provide a better reproductive payoff to males than additional social mates. Male house wrens, Troglodytes aedon, show three types of social mating behaviour: single-brooded monogamy, sequential monogamy (two broods) and polygyny. Thus, male reproductive success can vary depending on the number of mates, the number of broods and the number of extrapair fertilizations. We used microsatellite markers to determine the realized reproductive success (total number of young sired from both within-pair and extrapair fertilizations) of males in these three categories. We found that polygynous males were more likely to be cuckolded than monogamous males; however, half of the polygynous males had a third brood, which resulted in similar reproductive success for sequentially monogamous and polygynous males. Despite the paternity gained from extrapair fertilizations by single-brooded males, males were more successful when they produced multiple broods during a season, either sequentially (monogamy) or simultaneously (polygyny). In our population, multibrooded males were more likely to have prior breeding experience and arrived earlier in the season, which provided a better opportunity to obtain more than one brood and, thus, produce more young.

Speckled warblers break cooperative rules: absence of helping in a group-living member of the Pardalotidae

In the majority of cooperatively breeding bird species, subordinates help the dominant pair to provision the young, regardless of the origin of groups and relatedness between members. Within the family that includes speckled warblers, Chthonicola sagittata, there is considerable variation in social organization and parental behaviour, but the societies of other group-living species in this family are of kin, and subordinates provision the young of breeders. Speckled warblers differ in that offspring are never philopatric, and breeding groups comprise unrelated individuals. We used behavioural observations and DNA fingerprinting to examine genetic parentage and the mating system of the group-living speckled warbler in Canberra, Australia. Speckled warblers breed as pairs or in trios consisting of a female with two males. Alpha males are socially dominant to beta males and maintain dominance through aggression. Beta males never helped to feed nestlings or fledglings, even though they competed for copulations and in one case gained paternity of two of three young in a brood. The social system is therefore polyandrous but not cooperative. As well as competing for copulations with females on their own territories, beta males and single males (those that had lost their breeding partner) regularly undertook extraterritorial forays, most often when the neighbouring female was fertile. Failure by beta males to help even with broods containing their own offspring may be adaptive in this species and may result from increased opportunity for extrapair fertilizations or enhancement of prospects for future reproduction through the formation of alliances with females.

EXTRAPAIR PATERNITY INCREASES VARIABILITY IN MALE REPRODUCTIVE SUCCESS IN THE CHESTNUT-SIDED WARBLER (DENDROICA PENSYLVANICA), A SOCIALLY MONOGAMOUS SONGBIRD

Abstract A monogamous mating system that includes extrapair fertilization can potentially generate higher variability in male reproductive success than monogamy without extrapair fertilization. That increased variability could provide a correspondingly higher opportunity for sexual selection and, thus, for the origin and persistence of sexual dimorphism in monogamous species. To determine whether extrapair fertilization enhanced the opportunity for sexual selection in a sexually dimorphic, monogamous bird species, we used microsatellite DNA typing to assess the prevalence of extrapair fertilization and its effect on variation in male reproductive success in a population of Chestnut-sided Warblers (Dendroica pensylvanica). We found that the level of extrapair fertilization in our study population was at the upper end of the range reported for bird populations (47% of nestlings had extrapair fathers; 61% of broods contained extrapair offspring). We also discovered that almost all extrapair offspring were si...

Breeding synchrony does not affect extra-pair paternity in great reed warblers

AbstractBreeding synchrony is hypothesised to influence the occurrence and frequency of extra-pair fertilisations (EPFs) in birds irrespective of the social mating system. The two proposed hypotheses make opposite predictions. (1) Synchronous breeding leads to a lower frequency of EPFs because males face a trade-off between mate guarding and obtaining additional matings via extra-pair copulations (EPCs) ('guarding constraint' hypothesis). (2) Synchronous breeding promotes EPFs because females are able to compare displaying males simultaneously, which provides them with more reliable cues for extra-pair mate choice ('mate assessment' hypothesis). In a study of great reed warblers (Acrocephalus arundinaceus) from 1987-1998, annual breeding was asynchronous and the frequency of EPFs was rather low (extra-pair young occurring in 6.4% of the broods). Within this population, however, there was no relationship between the frequency of EPFs and breeding synchrony, thus not favouring any of the two hypotheses. Contrary to assumptions of the hypotheses, mate guarding did not seem to constrain males from engaging in EPCs (disfavouring the 'guarding constraint' hypothesis), and females seem to have repeated opportunities to compare males irrespective of breeding synchrony (disfavouring the 'mate assessment' hypothesis). Our results suggest that breeding synchrony is not an important factor influencing patterns of EPFs in great reed warblers. The low frequency of EPFs may instead be explained by the socially polygynous mating system, where females are less constrained in their choice of a social male.

LOW FREQUENCY OF EXTRA-PAIR PATERNITY AND HIGH FREQUENCY OF ADOPTION IN BLACK-LEGGED KITTIWAKES

Abstract We studied the timing and frequency of extra-pair copulations and extra-pair fertilizations in the Black-legged Kittiwake (Rissa tridactyla), a socially monogamous seabird that breeds in dense colonies. We recorded 313 copulations by 82 marked pairs in 25 000 nest-hr over three years. We recorded only two extra-pair copulations, both of which were obtained by opportunistic males that disrupted pair copulations in progress. Pairs performed a mean of 14 copulations per clutch suggesting that males may copulate relatively frequently for paternity assurance. Our parentage analysis based on eight microsatellite markers did not detect any extra-pair paternity in 119 offspring from 86 broods; however we did detect three cases of adoption caused by chicks moving to adjacent nests. The between-nest movement of a minimum of 8% of chicks suggests that escaping siblicide may be an adaptive strategy for some nestlings, despite the risk of falling into the sea and drowning (observed in 11 of 21 chicks). Baja F...

PARENTAGE IN AN OKLAHOMA POPULATION OF LOGGERHEAD SHRIKES ASSESSED USING NUCLEAR MICROSATELLITES

Abstract I used six nuclear microsatellites to assess rates of intraspecific brood parasitism and extra- pair paternity in relationship to conspecific density in 218 offspring from 44 broods of Loggerhead Shrikes (Lanius ludovicianus). I also estimated statistical power associated with these markers for each parentage test and suggest a method for adjusting power estimates when individuals are incompletely genotyped. No offspring were the result of intraspecific brood parasitism. Eight offspring from five families (4% of all offspring; 14% of families) were sired by extra-pair fertilization. Average exclusionary power was 0.94 when adjusted to account for incomplete genotyping. Assuming a 1% genotyping error rate, this power drops to 0.91. This is the first genetic assessment of parentage in a wild population of Loggerhead Shrikes. Parentesco en una Poblacion de Oklahoma de Lanius ludovicianus Evaluado Usando Microsatelites Nucleares Resumen. Utilice seis microsatelites nucleares para evaluar las tasas de...

Mate Attentiveness, Seasonal Timing of Breeding and Long-term Pair Bonding in the House Finch (Carpodacus mexicanus)

AbstractIn seasonally breeding birds, natural selection favors individuals that begin breeding earlier in a year because they produce more or higher quality offspring than those that begin breeding later. Among the factors that influence the timing of breeding, which include the age, health, competitive ability, or mate quality of individuals, is the longevity of the pair bond, with birds that remain mated across years initiating breeding earlier in the season than newly formed pairs. The behavioural interactions between pair members that may facilitate long-term pair bonding and early breeding onset have infrequently been studied, however. Here we report the relationship between male-female affiliative behaviour, pair-bond duration, and breeding date in house finches (Carpodacus mexicanus), a short-lived, socially monogamous passerine species in which the duration of pair bonds is highly variable within and among seasons. Finches that initiated breeding earliest in the season were those that had bred with one another in previous years. Early breeding males from returning pairs maintained significantly closer contact with their mate during the first egg-laying period of the year than did males from late-breeding, newly formed pairs. Similarly, early-breeding females from returning pairs followed their mate more closely in nest-vicinity flights during the fertile period than females from late-breeding, newly formed pairs. These results suggest that attributes of and interactions between both pair members may help to maintain stable breeding pairs and influence the timing of breeding in seasonally nesting, short-lived songbirds. Rather than advertising for or seeking extra-pair fertilization opportunities, high-quality pairs of finches may invest heavily in their mate to secure the pair bond and ensure high intrapair reproductive success.

The reproductive choices of eavesdropping female black-capped chickadees, Poecile atricapillus.

In animals where males engage in signalling interactions, females might evaluate male-male contests to inform their reproductive choices. We used interactive playback to engage territorial male black-capped chickadees (Poecile atricapillus) of known dominance status in countersinging contests with an aggressive or submissive opponent. Previous analysis of these data showed that high-ranking males who received aggressive playback were more likely to be cuckolded. Here we describe the particular reproductive decisions of females whose partners received aggressive versus submissive playback. The proportion of extra-pair young per brood was higher for females paired to high-ranking males that received aggressive playback compared to submissive playback, and similar to levels in broods of females paired to low-ranking males. We found no strong predictors of whether high-ranking subjects lost paternity following aggressive playback. Females usually preferred extra-pair sires with high dominance status. When females had extra-pair fertilizations with low-ranking males, females chose males who had received submissive playback. We conclude that females mated to aggressive-playback, high-ranking males pursued mixed mating strategies similar to those of females mated to low-ranking males. Our results support the idea that male performance in song contests may influence multiple aspects of female reproductive choices.

Indiscriminate polyandry and male parental effort

Extrapair paternity involves cooperation between mated females and extrapair males. On the other hand, mated males exhibit a spectrum of anti-cuckolding strategies. Hence, extrapair attributes of diverse species and populations reported in the literature are particular solutions of evolutionary games involving gender-specific cuckolding/anti-cuckolding strategies. Here we use game theoretical methods to study the effect of male paternal effort conserving strategies in situations where females seek extrapair fertilizations (EPF) for reasons of genetic compatibility and/or in pursuit of genetic diversity for their offspring. In such cases, females cannot make a pre-copulatory selection of the optimal genetic partners, and therefore combine promiscuous copulation with the use of in copula and/or post-copulatory selection mechanisms to optimize the genetic endowment of their offspring— indiscriminate polyandry. Our results indicate that, when indiscriminate polygamy is constrained by the availability of extrapair male partners, there are three possible (parameter regime wise) evolutionary stable strategy solutions. (1) All females seek EPF, while all males restrict parental care. (2) All females seek EPF, while all males are unconditionally parental. (3) Females use a combination strategy where pursuit of EPF is mixed—on either a population, or an individual level—with genetic monogamy, while all males use a conditional paternal care strategy, which involves adjusting their parental efforts according to their certainty of paternity.

Extrapair Paternity and Breeding Synchrony in Gadwalls (Anas Strepera) in North Dakota

AbstractExtrapair paternity and its correlates with breeding synchrony were examined in Gadwall (Anas strepera) using microsatellite DNA fingerprinting. Eleven of 261 ducklings (4.2%) within 8 of 29 broods (27.6%) had genotypes consistent with extrapair fertilizations, a comparable frequency to other species of waterfowl for which extrapair paternity has been documented. We found no evidence of intraspecific brood parasitism. The frequency of extrapair paternity was not significantly correlated with breeding synchrony. We suggest that female absences during egg-laying may have provided males with opportunities to pursue extrapair copulation when breeding was synchronous.

Male share of provisioning is not influenced by actual or apparent loss of paternity in western bluebirds

Approximately 45% of western bluebird (Sialia mexicana) females have some chicks in the nest that are not sired by their social mates. Extrapair fertilizations account for 42% of offspring in these nests and 19% of nestlings overall. I tested the hypothesis that males reduce nestling provisioning when their certainty of paternity or share of paternity is reduced. Capture and detention of socially monogamous males for 1 h or 24 h during the laying period reduced males' copulatory access and their ability to mate guard, increasing the frequency with which extrapair males intruded and attempted to copulate with resident females. Males detained during laying did not reduce their share of feeding trips compared to control males detained during incubation, compared to unmanipulated males, or compared to males that were captured but not detained. Males detained on territory for 1 h during the laying period did not reduce their share of feeding trips when they observed male intrusion, nor when they observed their mates accepting extrapair copulations. Males that witnessed their mates accepting extrapair copulations did not reduce their share of risk in provisioning. Genetic fingerprinting at nonexperimental nests indicated that males also failed to reduce their feeding contributions when their estimated share of paternity was reduced, even when a helper male was present to reduce the impact on nestlings. These results suggest that male western bluebirds do not make significant adjustments in their share of provisioning when they have evidence of partial paternity loss. Together with prior results, this study suggests that western bluebird males use an all-or-none rule, contributing approximately half of the parental provisioning at nests, as long they have some copulatory access to the female during egg laying.

Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence

Organisms exhibiting genetic polymorphism often also exhibit true alternative life-history strategies in which behavioral tactics are genetically fixed. Such systems are ideal for the study of the evolution of life histories because the consequences of selective episodes can be more easily identified. Here I report an interesting and classic example of a species exhibiting true alternative strategies. Due to a chromosomal inversion, male and female white-throated sparrows (Zonotrichia albicollis) occur as two distinct morphs, tan or white. Tan and white morphs mate disassortatively, and this mating pattern maintains the polymorphism in relatively equal proportions within the population. In comparison with tan males, white males are more aggressive, frequently intrude into neighboring territories, spend less time guarding their mates, occasionally attempt polygyny, and provide less parental care. White females are also more aggressive and solicit copulation from their mates twice as often as tan females. Multilocus DNA fingerprinting revealed that 31.8% of nestlings and 56.3% of broods from white male--tan female pairs were the result of extrapair fertilizations, whereas only 4.4% of nestlings and 6.3% of broods from tan male--white female pairs contained extrapair offspring. However, 4.4% of the nestlings (12.5% of broods) from tan male--white female pairs were attributable to conspecific brood parasitism, and brood parasitism was not a factor for white male--tan female pairs. For three excluded extrapair offspring, actual paternity was assigned to territorial white males, suggesting that, although white males are not preferred by females in previous mate choice studies, they do attempt to increase their reproductive success by securing additional matings via extrapair copulations. However, by doing so, white males also lose paternity at home. Behavioral and genetic evidence suggest that the two morphs use alternative strategies and that reproductive trade-offs may serve to maintain a competitive equilibrium between the morphs. Copyright 2003.

Determinants of Between-Season Site, Territory, and Mate Fidelity in Hooded Warblers (Wilsonia Citrina)

Abstract We examined nestling paternity, fate of nests, and prior experimental manipulations in Hooded Warblers (Wilsonia citrina) to test the hypothesis that those factors influenced the warblers' fidelity to their previous breeding site (general breeding area), territory (specific nesting and feeding area within general breeding area), and mate the following year. Field re-search was conducted at Hemlock Hill Biological Research Area in northwestern Pennsylvania from 1991 to 1998. Hooded Warblers returned to Hemlock Hill at an average annual rate of 47% over seven years. Significantly more males than females returned in 1992 and 1995, but overall difference between male and female return rates was not significant. Frequency of males returning to their former territory (58%) was greater than frequency of females returning to their former territory (29%). When mates from the previous year returned, remated pairs (n = 13) occupied their former territory more often than they occupied a new territory. Average number of young fledged per nest tended (P = 0.06) to be greater for females that returned to Hemlock Hill than for females that did not return. There was also a tendency (P = 0.09) for females that returned to the breeding site to have more nests with extrapair young than those that did not return. Territory fidelity and mate fidelity for both males and females were not related to prior nest fate or paternity of young. During those years, we conducted two relatively long-lasting experimental manipulations: vegetation removal from nest sites and radiotagging. Those experimental manipulations did not significantly affect future selection of breeding site, territory, or mate. Thus, whereas male Hooded Warblers demonstrated greater territory fidelity than females, only females were possibly affected by factors that we examined from the previous year, specifically extrapair fertilization and prior reproductive success or failure.

Extra-pair paternity in the facultatively polygynous spotless starling, Sturnus unicolor

A potential cost of polygyny that may have restrained its evolution in some avian species is the presence of extra-pair offspring in the nests of males mated with several females. However, this relationship is not frequently found and an experimental approach investigating the association between extra-pair offspring and polygyny, while controlling for male traits related to polygyny, has not been undertaken. In this study, we manipulated the testosterone levels of facultatively polygynous spotless starlings, Sturnus unicolor, to establish experimentally different groups of polygyny and analyse its influence on levels of extra-pair offspring in males for which other traits were randomised. During two consecutive breeding seasons, we examined the effects of harem size on the ability of males to assure genetic paternity, assessed by DNA fingerprinting, and on reproductive success in their own nests. The frequency of extra-pair fertilisations varied between 10% (14/140) in 1996 and 20% (39/194) in 1997. Year-to-year analyses of extra-pair paternity variables with treatment as factor and harem size (number of simultaneous mated females) as covariate, were significant only in relation to harem size. Males with few simultaneously mated females were less cuckolded than more polygynous males in 1997 but not in 1996, indicating that mating costs of polygyny occurred, at least in the year with the higher rate of extra-pair paternity. Because polygynous males have more social mates, they may accrue higher reproductive success irrespective of their risk of being cuckolded. However, our results suggest that to be polygynous is costly in terms of paternity loss when we experimentally induce mating status controlling for individual male traits. However, the low values of our power tests for the statistically non-significant results of hormone on cuckoldry do not allow us to discard this hormone effect altogether.

Fertility Assurance through Extrapair Fertilizations and Male Paternity Defense

Extrapair paternity has been observed in many formally monogamous species. Male pursuit of extrapair fertilizations is explained by the advantages of having offspring that receive essential paternal care from other males. Since females are capable of exercising a degree of control over the post-copulatory sperm competition, extrapair paternity cannot persist unless it confers fitness benefits on cuckolding females. Thus, extrapair paternity involves cooperation between mated females and extrapair males. On the other hand, paired males frequently exhibit strategies that minimize their loss of paternity and/or conserve paternal investment if paternity is lost. Hence, extrapair attributes of diverse species and populations reported in the literature are particular solutions of evolutionary games involving gender-specific cuckolding/anti-cuckolding strategies. Here we use methods of evolutionary game theory to study the role of male paternity guarding strategies in situations where females seek extrapair fertilizations for reasons of genetic compatibility and/or in pursuit of genetic diversity for their offspring. Our results indicate that in these circumstances pursuit of extrapair fertilizations is the only evolutionary stable female strategy. Males, on the other hand, have two, mutually exclusive, evolutionary stable strategies: full time pursuit of extrapair fertilizations and a compromise strategy wherein they protect in-pair paternity during their mate's fertile periods and pursue extrapair paternity the rest of the time. The relative merits of these two strategies are determined by the efficiency of male in-pair paternity defense, breeding synchrony, fitness advantages of extrapair over in-pair offspring, and the intensity of competition for extrapair fertilizations from floater males.

EXTRAPAIR PATERNITY AND BREEDING SYNCHRONY IN GADWALLS (ANAS STREPERA) IN NORTH DAKOTA

Abstract Extrapair paternity and its correlates with breeding synchrony were examined in Gadwall (Anas strepera) using microsatellite DNA fingerprinting. Eleven of 261 ducklings (4.2%) within 8 of 29 broods (27.6%) had genotypes consistent with extrapair fertilizations, a comparable frequency to other species of waterfowl for which extrapair paternity has been documented. We found no evidence of intraspecific brood parasitism. The frequency of extrapair paternity was not significantly correlated with breeding synchrony. We suggest that female absences during egg-laying may have provided males with opportunities to pursue extrapair copulation when breeding was synchronous.

Sexual selection, germline mutation rate and sperm competition

BackgroundAn important component of sexual selection arises because females obtain viability benefits for their offspring from their mate choice. Females choosing extra-pair fertilization generally favor males with exaggerated secondary sexual characters, and extra-pair paternity increases the variance in male reproductive success. Furthermore, females are assumed to benefit from 'good genes' from extra-pair sires. How additive genetic variance in such viability genes is maintained despite strong directional selection remains an evolutionary enigma. We propose that sexual selection is associated with elevated mutation rates, changing the balance between mutation and selection, thereby increasing variance in fitness and hence the benefits to be obtained from good genes sexual selection. Two hypotheses may account for such elevated mutation: (1) Increased sperm production associated with sperm competition may increase mutation rate. (2) Mutator alleles increase mutation rates that are revealed by the expression of condition-dependent secondary sexual characters used by choosy females during their mate choice. M Petrie has independently developed the idea that mutator alleles may account for the maintenance of genetic variation in viability despite strong directional selection.ResultsA comparative study of birds revealed a positive correlation between mutation rate at minisatellite loci and extra-pair paternity, but not between mutation rate and relative testes mass which is a measure of relative sperm production. Minisatellite mutation rates were not related to longevity, suggesting a meiotic rather than a mitotic origin of mutations.ConclusionWe found evidence of increased mutation rate in species with more intense sexual selection. Increased mutation was not associated with increased sperm production, and we suggest that species with intense sexual selection may maintain elevated mutation rates because sexual selection continuously benefits viability alleles expressed in condition-dependent characters. Sexual selection may increase mutational input, which in turn feeds back on sexual selection because of increased variance in viability traits.