Extra-pair Chicks Research Articles

Extra-pair paternity in a species with frequent extra-pair courtship feedings, few extra-pair copulations, and male-biased parental care

Patterns of extra pair paternity (EPP) and intraspecific brood parasitism (IBP) were studied in a Whiskered Tern Chlidonias hybrida population characterized by female brood desertion, a high level of extra pair courtship feedings (10%) and a low level of extra pair copulation (EPC; 0.6%). In this study, we used a set of microsatellite loci to analyse parentage in 56 Whiskered Tern families from southern Poland. Depending on the method, we detected that 1.4%–3.6% of chicks were sired by an extra-pair male, and extra-pair chicks were present in 3.6%–8.9% of broods. IBP was observed in 8.9%–14.3% of broods, corresponding to 3.6%–6.4% of the chicks. The low rate of EPP is in agreement with the hypothesis that in species with high male parental investment, females should avoid EPC. The low level of IBP indicates that intraspecific egg dumping is not a common female strategy in Whiskered Tern, similar to many other colonial waterbird species.

Genetic mating system, population genetics and effective size of Saffron Finches breeding in southern South America.

Thraupidae (Tanagers and allies) show a remarkable array of behaviors, ecologies, morphologies and plumage colors, offering a great opportunity to investigate the evolution of avian mating strategies. We characterize the population genetics and mating system of Sicalis flaveola pelzelni, a socially monogamous Neotropical songbird with biparental care. We found moderate to high levels of neutral genetic variation, similar across three breeding seasons, consistent with large and stable populations, and no temporal genetic structure. Parentage analyses of 114 adults and 198 nestlings (54 nests) revealed 31.8% of extra-pair offspring (EPO) and 51.8% of broods with at least one extra-pair chick. Extra-pair paternity (EPP) rates varied across seasons and were significantly higher in 2014/2015. Neither breeding synchrony nor pair genetic relatedness was significantly associated to EPP rates. Males paired with females in nests with and without EPO were equally heterozygous, and EPO were significantly less heterozygous than within-pair offspring, not supporting the 'indirect genetic benefits' hypotheses. Females were more related to their extra-pair mates than to their social mates, not supporting the 'inbreeding avoidance' hypothesis. The non-monogamous genetic mating system uncovered here seems not to lower the effective size of the population, which was higher than the sample size of adult breeders. We report and discuss possible cases of quasi-parasitism, as indicated by maternity exclusion patterns. We contribute novel information to expand the knowledge about the largely unexplored genetic mating systems of Thraupidae. Our findings also set the stage for further studies examining if plumage coloration or song traits predict paternity gain or loss in Saffron Finches.

Growth benefit to house wren nestlings of having an asynchronously late-hatching nestmate is greater for extra-pair offspring

Because nestling growth influences survival and future reproductive success, early-life conditions that impact growth have potentially large effects. One notable source of variation in early-life conditions for birds is the relative timing of egg hatching: hatching asynchrony leads to size hierarchies among nestlings and may affect competition for, or parental allocation of, resources. Paternity is another potentially important factor, as extra-pair offspring have been shown in some systems to be of higher quality and therefore might be better competitors. We tested whether the presence of an asynchronously late-hatched nestmate affected nestling growth in a population of house wrens (Troglodytes aedon) and whether paternity status (within-pair vs. extra-pair) affected growth either individually or in interaction with hatching synchrony. We measured mass and wing chord of nestlings repeatedly between the ages of 0 and 10 days and determined the paternity status of each nestling. Both mass and wing chord were significantly greater in nestlings who shared the nest with at least one late-hatched nestling. This effect was significantly greater for extra-pair chicks for wing chord, but not mass. We found no effect on nestling mass or wing chord of paternity status alone, hatch timing (early or late), hatch date, brood size, sex, or social father mass. Considered together, these results suggest that hatching synchrony affects nestling growth and that extra-pair nestlings may be more responsive to early-life conditions in some aspects of growth. We discuss possible mechanisms for these effects. Bird eggs can hatch synchronously or asynchronously. In nests with asynchronous hatching, nestlings are different sizes, which may affect competition among them and therefore their growth rates. If hatching asynchrony does influence nestling growth, it may have far-reaching impacts on the fitness of the nestlings. We measured mass and wing length in house wren nestlings. Nestlings with an asynchronously late-hatching nestmate were larger in both measures, demonstrating an advantage to having a younger nestmate. This advantage was greater for extra-pair nestlings for wing length. This suggests a difference between extra-pair and within-pair nestlings in their responsiveness to early-life conditions, which might be due to the genetics of the extra-pair chicks or to differences in parental investment. This study documents a previously unknown potential benefit of hatching asynchrony, as well as a context-dependent difference between extra-pair and within-pair nestlings.

No evidence that genetic compatibility drives extra‐pair behavior in female blue‐footed boobies

The function of female birds' extra‐pair (EP) behavior has remained an unresolved question in ornithology and behavioral ecology for > 30 yr. The genetic compatibility hypothesis (GCH) proposes that females benefit by acquiring biological sires that yield more heterozygous, and therefore fitter, offspring than their social mates. We used ten polymorphic microsatellite loci to test GCH predictions and its assumption that fitness increases with heterozygosity in blue‐footed boobies Sula nebouxii, a long‐lived tropical seabird. Our predictions were not supported. Heterozygosity was uncorrelated with quality indicators (fledging probability, fledgling or adult body size or mass, adult ornamentation, mean breeding success). Females were no more likely to have EP behavior or chicks when their social mates were less heterozygous or compatible, nor were EP males more heterozygous or compatible than the males they cuckolded. Finally, EP chicks were no more heterozygous than within‐pair chicks overall or in half‐sib comparisons, nor were within‐pair chicks from all‐within‐pair nests more heterozygous that those with EP nest‐mates. There are both methodological and biological explanations for these consistently negative results. Inadequate sample size is possible but unlikely, since our samples were comparable or larger than those of similar studies with significant findings. Lack of identity disequilibrium (within‐individual heterozygosity correlation) among our marker loci could be responsible, and suggests either insufficient marker coverage or lack of inbreeding, bottleneck, and/or admixture. An independent social pedigree revealed infrequent inbreeding, suggesting that pressure on females to select sires that maximize offspring heterozygosity may be genuinely lax. Alternatively, it is possible that the GCH is only upheld when selection on young is strongest; this would not be detected in our sample, which was taken during an extremely productive year. Whatever their cause, our results expand the taxonomic breadth of avian EP behavior analyses and should be considered in future evaluations of the GCH.

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

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

Interactive effects of male and female age on extra-pair paternity in a socially monogamous seabird

Females sometimes obtain older sires for their offspring through extra-pair interactions, but how female age influences paternity is largely unexplored and interactive effects across the age span of both sexes have not been analyzed. To test whether female choice of sire age varies with female age in the blue-footed booby (Sula nebouxii), we examined associations between ages of both partners and the probability of extra-pair paternity (EPP) in 350 broods of parents up to 22 years old in a single breeding season. Extra-pair paternity enables a female to select an alternative sire for her offspring and could function to avoid or achieve particular combinations of parental ages. A male age × female age interaction revealed that in young females (≤4 years), EPP decreased with increasing age of the social partner, whereas in old females (≥8 years), it increased. Moreover, sires of extra-pair (EP) chicks of young females paired to young males were on average 6.33 years older than the females’ social partners. Since female boobies control copulatory access, this pattern could imply that young females choose old sires for their proven genetic quality and that old females avoid very old males because matings with them may risk infertility or genetic defects in offspring. Taking female age into account and observing across the whole age span may be necessary for understanding female age-based mate choice.

Experimentally Simulating Paternity Uncertainty: Immediate and Long-Term Responses of Male and Female Reed Warblers Acrocephalus scirpaceus

In many socially monogamous species, both sexes seek copulation outside the pair bond in order to increase their reproductive success. In response, males adopt counter-strategies to combat the risk of losing paternity. However, no study so far has tried to experimentally prove the function of behaviour for paternity assurance. Introducing a potential extra-pair partner during the female fertile period provides a standardised method to examine how pair members respond immediately (e.g. increase mate guarding or copulation frequency) or long term (e.g. later parental investment and paternity uncertainty). In this study on a socially monogamous passerine species, we experimentally confronted pairs of reed warblers with a conspecific male (caged male simulating an intruder) during egg-laying. Our results revealed that occurrence of an intruder during that period triggered aggression against the intruder, depending on the presence of the female. The male territory owner also attacked the female partner to drive her away from the intruder. Thus territory defence in reed warblers also serves to protect paternity. The increase in paternity uncertainty did not affect later paternal investment. Paternal investment was also independent of the actual paternity losses. In females, the experiment elicited both, immediate and long-term responses. E.g. female copulation solicitations during the intruder experiment were only observed for females which later turned out to have extra-pair chicks in their nest. In relation to long term response females faced with an intruder invested later less in offspring feeding, and had less extra-pair chicks in their nests. Extra-pair paternity also seems to be affected by female quality (body size). In conclusion female reed warblers seem to seek extra-pair fertilizations but we could demonstrate that males adopt paternity assurance tactics which seems to efficiently help them to reduce paternity uncertainty.

Hatching order explains an extrapair chick advantage in western bluebirds

Within-family comparisons of offspring growth rates have provided important tests of genetic benefits of extrapair mating for females. Here, we demonstrate that hatching order explains the growth advantage for extrapair young in western bluebirds (Sialia mexicana); extrapair nestlings are larger than within-pair nestlings in the same nest, but they also hatch earlier in the clutch, thus benefiting from hatching asynchrony. By controlling for hatch order and other nongenetic factors and comparing mixed-paternity broods with genetically monogamous broods, we show that the extrapair nestling growth advantage is not genetically based. We cannot rule out the possibility that females benefit from extrapair mating because genetic quality indicators may appear later in life and may be independent of hatch order, however, based on our results, we do not see evidence of genetic superiority of extrapair nestlings. Although findings similar to ours have been attributed to maternal effects, it is currently unclear whether overrepresentation of extrapair nestlings early in the laying and hatching sequence results from investment patterns of females, their social mates, or extrapair males. This study highlights the need to investigate the potentially complex interactions among all players, and how these may lead to higher performance of extrapair offspring compared with within-pair offspring within the same family.

Condition‐dependent genetic benefits of extrapair fertilization in female blue tits Cyanistes caeruleus

In many socially monogamous birds, both partners perform extrapair copulations (EPC). As this behaviour potentially inflicts direct costs on females, they are currently hypothesized to search for genetic benefits for descendants, either as 'good' or 'complementary' genes. Although these hypotheses have found some support, several studies failed to find any beneficial consequence of EPC, and whether this behaviour is adaptive to females is subject to discussion. Here, we test these two hypotheses in a natural population of blue tits by accounting for the effect of most parameters known to potentially affect extrapair fertilization. Results suggest that female body mass affected the type of extrapair genetic benefits obtained. Heavy females obtained extrapair fertilizations when their social male was of low quality (as reflected by sexual display) and produced larger extrapair than within-pair chicks. Lean females obtained extrapair fertilizations when their social mate was genetically similar, thereby producing more heterozygous extrapair chicks. Our results suggest that mating patterns may be condition-dependent.

Extra-Pair Fertilizations in Sandhill Cranes Revealed Using Microsatellite DNA Markers

AbstractAbstractThe presence of extra-pair fertilizations (EPF) in a dense breeding population of Sandhill Cranes (Grus canadensis) was examined using six microsatellite DNA markers. In this long-lived species that maintains long-term pair bonds, 4.4%–11% of 45 chicks were not genetically related to one social parent, and extra-pair chicks were present in 5.6%–22% of 18 family groups. Two confirmed extra-pair chicks were from different broods of the same pair that was socially bonded for a minimum of 12 years. The social male was rejected as the genetic father of both of these chicks. Three other potential cases of EPF (two cases in which the social male was rejected as the genetic parent, one in which the social female was rejected) could also have resulted from mate replacement prior to sampling. The range of EPF in this population of Sandhill Cranes is similar to that of other species with similar mating systems. In the confirmed cases of EPF, the female was able to increase her individual reproductive success without losing her territory.

EXTRA-PAIR FERTILIZATIONS IN SANDHILL CRANES REVEALED USING MICROSATELLITE DNA MARKERS

Abstract ABSTRACT The presence of extra-pair fertilizations (EPF) in a dense breeding population of Sandhill Cranes (Grus canadensis) was examined using six microsatellite DNA markers. In this long-lived species that maintains long-term pair bonds, 4.4%–11% of 45 chicks were not genetically related to one social parent, and extra-pair chicks were present in 5.6%–22% of 18 family groups. Two confirmed extra-pair chicks were from different broods of the same pair that was socially bonded for a minimum of 12 years. The social male was rejected as the genetic father of both of these chicks. Three other potential cases of EPF (two cases in which the social male was rejected as the genetic parent, one in which the social female was rejected) could also have resulted from mate replacement prior to sampling. The range of EPF in this population of Sandhill Cranes is similar to that of other species with similar mating systems. In the confirmed cases of EPF, the female was able to increase her individual reproducti...

Extrapair Fertilization in the Black-Browed Reed Warbler (Acrocephalus Bistrigiceps): Effects on Mating Status and Nesting Cycle of Cuckolded and Cuckolder Males

Abstract We studied the relationship between the occurrence of extrapair fertilizations (EPFs) and mating status and nesting cycle of mates, respectively, in a population of Black-browed Reed Warblers (Acrocephalus bistrigiceps). Overall, 6.4% (9 of 140) of the chicks were sired by extrapair males, and 13.5% (5 of 37) of the broods contained at least one extrapair chick. Socially polygynous males were cuckolded more frequently than socially monogamous males (40.0% and 3.7%, respectively). In three of four cases where cuckolded males were polygynous, the fertile periods of their mates overlapped. Except for two floating males that obtained EPFs, five out of seven cuckolder males were paired. Males succeeded in EPFs when the fertile period of the extrapair females largely overlapped the incubation period of their own mates. These findings are consistent with the hypothesis that there are trade-offs between extrapair copulation activity and both mate guarding and rearing of nestlings. Fertilisation Extraconjugale chez Acrocephalus bistrigiceps: Effets des Mâles Infidèles et Cocus sur le Statut de Couple et le Cycle de Nidification

EXTRAPAIR FERTILIZATION IN THE BLACK-BROWED REED WARBLER (ACROCEPHALUS BISTRIGICEPS): EFFECTS ON MATING STATUS AND NESTING CYCLE OF CUCKOLDED AND CUCKOLDER MALES

Abstract We studied the relationship between the occurrence of extrapair fertilizations (EPFs) and mating status and nesting cycle of mates, respectively, in a population of Black-browed Reed Warblers (Acrocephalus bistrigiceps). Overall, 6.4% (9 of 140) of the chicks were sired by extrapair males, and 13.5% (5 of 37) of the broods contained at least one extrapair chick. Socially polygynous males were cuckolded more frequently than socially monogamous males (40.0% and 3.7%, respectively). In three of four cases where cuckolded males were polygynous, the fertile periods of their mates overlapped. Except for two floating males that obtained EPFs, five out of seven cuckolder males were paired. Males succeeded in EPFs when the fertile period of the extrapair females largely overlapped the incubation period of their own mates. These findings are consistent with the hypothesis that there are trade-offs between extrapair copulation activity and both mate guarding and rearing of nestlings. Fertilisation Extraconj...

Effect of Extra-Pair Paternity on Effective Population Size in a Reintroduced Population of the Endangered Hihi, and Potential for Behavioural Management

We collected genetic and behavioural data on hihi (Notiomysts cincta, an endangered New Zealand bird) after reintroduction to Mokoia Island to assess the effect of extrapair copulation on effective population size (N e), and investigate the potential for increasing N e through behavioural management. DNA fingerprinting revealed that 46% of chicks (n = 188) resulted from extra-pair paternity, and 82% of broods (n = 56) had at least one extra-pair chick. Of the extra-pair young, 34%(n = 89) were from unpaired males, and the remainder were from paired males. Variance in reproductive success (VRS) among individuals changed between years, and the relative variance among males and females depended on the sex ratio. VRS increased when measured over longer time scales, the variance in recruits being three times higher than the variance in the number of hatchlings. Extra-pair copulation increased VRS by 150% in 1 year and decreased it by 30% in another year, but this only caused a 4% decrease and 8% increase, respectively, to N e/N. Although there is potential to manage VRS in this species through behavioural management, a more important factor is adult lifespan, which is the main correlate of lifetime reproductive success as well as the determinant of generation time. The high annual mortality rate in Mokoia hihi (females = 64%, males = 52%) has prevented the population from growing, so the key factors limiting N and N e/N are the same.

Social mating systems and extrapair fertilizations in passerine birds

Two alternative hypotheses have been proposed to explain how social and genetic mating systems are interrelated in birds. According to the first (male trade-off) hypothesis, social polygyny should increase extrapair fertilizations because when males concentrate on attracting additional social mates, they cannot effectively protect females with whom the); have already paired from being sexually assaulted. According to the second (female choice) hypothesis, social polygyny should decrease extrapair fertilizations because a substantial proportion of females can pair with the male of their choice, and males can effectively) guard each mate during her fertile period. To discriminate these alternatives, we comprehensively reviewed information on social mating systems and extrapair fertilizations in temperate zone passerine birds. We found significant inverse relationships between proportions of socially polygynous males and frequencies of extrapair young, whether each species was considered as an independent data point (using parametric statistics) or phylogenetically related species were treated as nonindependent (using contrasts analyses). When social mating systems were dichotomized, extrapair chicks were twice as frequent in monogamous as in polygynous species (0.23 vs. 0.11). We hypothesize that in socially polygynous species, (1) there is less incentive for females and males to pursue extrapair matings and (2) females incur higher costs for sexual infidelity (e.g., due to physical retaliation or reduction of paternal efforts) than in socially monogamous species. (Less)

Frequency and timing of extrapair fertilisation in the polyandrous red phalarope ( Phalaropus fulicarius )

In sequentially polyandrous bird species, where females mate with different males in succession during a single breeding season, sperm stored by females can occasionally lead to extrapair fertilisations (EPFs) in clutches cared for by the second and subsequent males. Thus, we predicted that in red phalaropes (Phalaropus fulicarius) – a sex-role-reversed, sequentially polyandrous, arctic breeding shorebird – EPFs would occur more frequently in clutches laid later in the breeding season. We used multilocus DNA profiling to examine the frequency and timing of EPFs in a population of red phalaropes breeding in the Canadian high arctic. Using a technique to determine parentage without maternal DNA, we inferred that 6 of 70 chicks in 18 broods resulted from EPFs – one extrapair chick in each of 6 broods. These results were supported by a further analysis using microsatellite DNA. As predicted, broods containing EPFs hatched from clutches laid significantly later in the season than did broods containing no EPFs. The difference in median hatch dates between broods with and without EPFs was 9.0 days, or 38% of the entire egg-laying period in that season. For the whole breeding season, we estimated that 6.5% of chicks were sired by extrapair males, which is similar to extrapair paternity estimates for other sex-role-reversed birds, but relatively low compared to the majority of socially monogamous species studied so far.

An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilizations

We combine behavioral studies with DNA-fingerprinting of a population of bearded tits Panurus biarmicus and test the idea that the pursuit of extra-pair copulations by females acts as selective pressure that may contribute to the formation of colonies in this socially monogamous species. We show that the rate of extra-pair paternity in colonial breeding pairs is very high, whereas no extra-pair chicks were detected in solitary nests. We found no cases of extra-pair maternity and intraspecific brood parasitism in solitary nests, whereas it did occur in dense breeding situations. We further found no difference in die quality of males between colonial and solitary individuals. However, colonial females were of significantly higher quality in terms of body size and condition. We propose that high-quality females settle in colonies to increase their opportunities to adjust the choice of their social partner by obtaining extra-pair copulations. We suggest that colony formation enables high-quality females to incite male-male competition for extra-pair copulations and consequently secure extra-pair fertilizations by high-quality males and that high-density nesting is controlled by female bearded tits. Kty words: Aves, coloniality, extra-pair fertilization, F. Paradoxornithidae, female quality, nest site choice. [Behav Ecol 8:113-119 (1997)]

Extra-pair paternity in willow ptarmigan broods: measuring costs of polygyny to males

Willow ptarmigan are one of only three monogamous grouse species in North America. However, in some populations between 5 and 20% of individuals pair polygynously. It has been suggested that monogamy may be maintained by the high cost of polygyny to males. We have used DNA fingerprinting to assess the actual reproductive success of both monogamous and polygynous adults. We determined whether or not the putative parents were the biological parents of the chicks from 38 broods. Of these clutches 30 were from monogamous matings, and 8 were from bigamous matings. Of the 207 chicks from monogamous matings 96% were within-pair offspring, compared to 67% of the 49 chicks from bigamous matings. All extra-pair offspring chicks resulted from extra-pair fertilizations (EPFs), and there were no instances of intraspecific nest parasitism. Mate guarding by monogamous males seems to be a highly effective method for maintaining genetic monogamy, as the only cases in which EPFs occurred were when the resident female left the territory for a few days or when a second female visited the territory. Our results support the notion that certainty of parentage may be one factor constraining willow ptarmigan males to be monogamous.

Extra-pair fertilizations and paternity defence in house martins,Delichon urbica

DNA fingerprinting showed that 15% of 62 house martin nestlings at study colonies in central Scotland were not related to their putative fathers, and 32% of 19 broods contained at least one extra-pair chick. There was no evidence of intraspecific brood parasitism. Birds were never seen to mate outside nests in the vicinity of nesting colonies, and the single copulation that was observed during this study was a pair mating that took place inside a nestbox. Extra-pair birds were often seen to enter nests, with seven of eight identified intruders being males from other nests where laying had already taken place. Pair males mate guarded by ensuring that females spent very little time alone at the nest from about 7 days before the first egg of the clutch was laid, and by accompanying females on up to 70% of flights away from the nest during the 4-5 days before laying commenced. Mate guarding seemed to slacken after egg laying began, with a gradual transition to incubation behaviour taking place. Associated with this was a higher likelihood that the youngest nestling would be fathered by an extra-pair male. Male removal experiments indicated that extra-pair birds were more likely to enter the nest of a fertile female when the pair male was absent, but in three cases where DNA fingerprints were obtained male removal during the fertile period of the pair female had no apparent influence on paternity.