Extrapair paternity and hybridization in birds

Hybridization in birds is a widely acknowledged phenomenon. It often occurs when one species is absent or rare which leads to mixed pairings between different species (Hubb's principle). However, Hubb's principle cannot explain hybridization in one of the most common Passeriform hybrids, barn swallow Hirundo rustica×house martin Delichon urbica, since these hybrids usually occurred in areas where both species were common. Such hybrids were often found as singletons between true barn swallows siblings suggesting that extrapair copulations, and not mixed breeding pairs, might be the reason for the existence of these hybrids. Extrapair copulations are common in both these species. Here, I tested the idea, that EPP and hybridization may be linked on a macro‐evolutionary scale across species. I used data on EPP from review studies and assigned each species a dichotomous variable whether it has produced hybrids or not. Hybridizing species did not show a higher percentage of extrapair copulations compared to non‐hybridizing species. However, while these data did not show any influence on the macro‐ecological scale, these factors could, nevertheless, facilitate hybridization in some species pairs as in the example of the swallows.     

Extrapair paternity, migration, and breeding synchrony in birds

To understand interspecific patterns in the strength of sexualselection, variation in the costs and benefits of exercisingmate choice needs to be evaluated. One manifestation of sexualselection in birds is the occurrence of greatly variable levelsof extrapair paternity (EPP). A proposed general explanationfor this variation is that the benefits to females in seekingextrapair copulations vary in a predictable manner accordingto the degree of breeding synchrony because females are betterable to assess potential extrapair partners when males are simultaneouslyin breeding condition. This hypothesis predicts a latitudinaltrend in EPP because birds tend to breed more synchronouslyaway from the equator. Expanding on previous geographicallyand taxonomically restricted tropical/temperate comparisons,we used phylogenetically independent standardized linear contraststo show that this positive relationship persists when all birdspecies for which EPP estimates currently exist are considered.However, if a third factor covaries with latitude in the sameway as breeding synchrony and EPP, this relationship need notbe causal. Migration could also account for latitudinal variationin the benefits to females of pursuing EPP, if migration isassociated with (1) hasty or (2) inaccurate mate choice, (3)facilitated assessment of male quality through the condition-dependenceof arrival time, or (4) increased genetic variance in male quality.We show that migration distance is positively related to theproportion of EPP and that migration can statistically explainthe latitudinal trend in EPP, even when confounding factorsare simultaneously controlled. Hence, alternative explanationsfor latitudinal variation in EPP may be feasible, and carefulintraspecific tests are needed to assess their relative importanceand their implications for geographical variation in life-historyevolution.     

Extrapair paternity in hooded warblers

We examined the role of extrapair fertilizations (EPFs) in themating system of the hooded warbler (Wilsonia citrina), a monogamoussongbird. DNA fingerprinting revealed that 8 of 17 (47%) femaleshad extrapair young in their first or second brood, and 23 of78 (29%) nestlings were the result of EPFs. Extrapair youngwere signifkandy more likely to occur in first broods than insecond broods. The proportion of EPFs within a brood was stronglybirnodal among broods: nests had 50% or more extrapair youngor none. In seven of eight broods where EPFs occurred, an adjacentmale neighbor was identified as the actual father. Male-likecoloration in females did not reduce the likelihood of havingextrapair young. Females with extrapair young did not receiveless parental care from their mates. All males who obtainedEPFs were mated to fertile females or were feeding offspringat the time they most likely mated with the extrapair female.Our results are consistent with the female control hypothesis,which predicts that females benefit from extrapair copulations(EPCs) and have some control over which males, if any, obtainEPCs. However, we could not reject the alternative hypothesisthat some male neighbors are particularly dominant and aggressiveduring EPC attempts, so females accept these EPCs to minimizecosts.     

Extrapair paternity and the evolution of bird song

Bird song is usually considered to have evolved in the contextof sexual selection. Because extrapair paternity is a majorcomponent of sexual selection, mating advantages at the sociallevel for males that produce songs of high quality may be transformedinto higher success in extrapair paternity. Therefore, maleswith longer and more complex songs should suffer less from extrapairpaternity intraspecifically, whereas species with high ratesof extrapair paternity, reflecting intense sperm competition,should produce more elaborate songs. Although some intraspecificstudies demonstrated a negative link between features of songsand extrapair paternity in own nest, others failed to detectsuch a relationship. Contrary to expectation, a meta-analysisof all studies revealed no significant intraspecific evidencefor songs being associated with extrapair paternity. In addition,in comparative analyses based on generalized least squares (GLS)models, we found that no measures of song complexity and temporaloutput were significantly related to extrapair paternity interspecifically,even when potentially confounding factors such as social matingsystem, life history, migration, habitat, or sexual dichromatismwere held constant. Only plumage dichromatism was significantlyrelated to extrapair paternity. The absence of both intra- andinterspecific relationships between measures of song variabilityand extrapair paternity suggests that factors other than postmatingsexual selection have been the important evolutionary forcesshaping differences in song.     

Extrapair paternity and mate choice in a chickadee hybrid zone

The dynamics of hybrid zones are likely to be influenced greatlyby patterns of mate choice, including cryptic choice mediatedthrough extrapair copulations. To understand changes in hybridzones over time and space, a detailed examination of matingpatterns and correlates is needed. We studied the role of extrapairfertilizations (EPFs) in the breeding biology of hybridizingblack-capped and Carolina chickadees in southeastern Pennsylvaniaover 4 years, using microsatellite DNA markers. We detectedextrapair offspring (EPO) in 56% of 90 broods examined; theseaccounted for at least 26% of 477 offspring. Chickadees do notappear to use EPFs to reduce costs of heterospecific pairing:EPFs were no more likely to occur in genetically dissimilar(heterospecific) social pairs than in pairs where social mateswere genetically similar. However, females paired with black-capped–likemales were more likely to have EPO. Females that acquired EPFsdid not obtain these from males genetically similar to themselves;instead, all females, regardless of their genotype or that oftheir social mate, tended to prefer Carolina-like males as extrapairpartners. There was no relationship between the presence ofEPO and hatching or fledging success. High rates of extrapairpaternity and apparent female preference for Carolina-like malessuggest that mate choice is an important influence in ongoingnorthward movement of this hybrid zone.     

Extrapair paternity and the opportunity for sexual selection in long-distant migratory passerines

Extrapair fertilizations (EPFs) are frequently documented insongbirds; however, the extent to which this reproductive tacticcontributes to variance in male reproductive success and hencethe strength of sexual selection on males remains little studied.Using 2 approaches, intraspecific and comparative, we test thehypothesis that the contribution of EPFs to variance in malefitness increases with migration distance in north temperatesongbirds. Using data on the genetic mating system of the scarletrosefinch Carpodacus erythrinus, a long-distance migrant, weshow that the number of extrapair mates and within-pair paternityare the most important components of variance in male reproductivesuccess. There was no evidence of a trade-off between extrapairand within-pair success of individual males as males successfulin procuring EPFs were less likely to be cuckolded. Comparativedata reveal that the opportunity for sexual selection due toEPFs is positively associated with both migration distance andbreeding synchrony in north temperate passerines, and we discussseveral mechanisms that could extend these relationships. Ingeneral, these data suggest that EPFs have a potential to playan important role in the evolution of sexually selected traitsin long-distance migratory songbirds such as rosefinches.     

Extrapair paternity in chestnut-sided warblers is correlated with consistent vocal performance

The elaborateness of many bird songs is commonly presumed tohave evolved under the influence of sexual selection by femalemate choice. Thus, aspects of acoustic diversity, such as songrepertoire size, are seen as likely targets of female choice.In many songbird species with song repertoires, however, therepertoires are small. In such species, female choice mightbe based on song features other than, or in addition to, songdiversity. To investigate this conjecture, I assessed singingand paternity in a population of chestnut-sided warblers (Dendroicapensylvanica), a species in which song repertoires are of modestsize. Twenty-two song traits were evaluated to determine whichones best predicted male extrapair reproductive success. Thecandidate traits encompassed measures of song diversity (e.g.,song repertoire size), gross-scale song performance (e.g., singingrate), and fine-scale song performance (e.g., variability amongsongs in a bout). Regression analysis revealed that the bestpredictor of extrapair success was singing with little variability.In particular, the most successful males sang with consistentpitch and timing, as well as high pitch. The greater extrapairsuccess of males with more consistent vocal performance maybe due to female preference for such performance, which couldbe an indicator of male quality.     

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 is influenced by breeding synchrony and density in the common yellowthroat

The effects of breeding synchrony and density on levels of extrapair paternity in birds are controversial. We used multilocus DNAfingerprinting and microsatellite analysis to examine the effectsof breeding synchrony and density on levels of extrapair paternityin the common yellowthroat (Geothlypis trichas). As in manyNeotropical migrants, breeding synchrony was greatest at thebeginning of the breeding season. Levels of extrapair paternitywere higher after the peak in synchrony, leading to an overallnegative relationship between extrapair paternity and breeding synchrony. However, there was a significant interaction betweenbreeding synchrony and density, as levels of extrapair paternitywere higher only for males breeding when both synchrony anddensity were low. We discuss several possible explanationsfor this interaction, including lower quality males or territoriesin low density areas and greater demands on mate guarding among males with larger territories. Most studies have not consideredsimultaneously the effects of breeding synchrony and densityon extrapair paternity. Our results suggest that ecologicalcorrelates of paternity may be revealed only after testingfor interactions in multivariate analyses.     

Extrapair paternity and the opportunity for sexual selection in a socially monogamous passerine

Effects of alternate mating strategies on the opportunity forsexual selection are widely debated, and recent studies haveconcluded that the effects of extrapair (EP) paternity on theopportunity for sexual selection may have been overstated dueto 1) methodological limitations of empirical studies and 2)the potential for males to gain from additional within-pair(WP) reproductive opportunities. We therefore examined the impactof EP paternity on the opportunity for sexual selection in thesocially monogamous and single-brooded eastern kingbird (Tyrannustyrannus). EP paternity was common in all 3 years of our study(61% of 89 broods, 47% of nestlings) and realized reproductivesuccess (EP + WP young) ranged from 0 to 9 young/male/year.A total of 31% of males lost all WP paternity (24% sired neitherWP nor EP young, whereas 7% sired EP but not WP young), andvariance in male realized reproductive success was more than9 times greater than that of apparent reproductive success.Nearly half of EP mates were not nearest neighbors, and manywere separated by 3 or more territories (>1000 m). EP successwas independent of nest defense behavior, but early singingmales and males with high song rates were most successful atboth a population level and when cuckolders and cuckoldees werecompared. EP paternity contributed significantly to the opportunityfor sexual selection in kingbirds, and we suggest that thisis probably due to the low potential for WP variation in reproductivesuccess, apparent long-distance movements of one or both sexes,and consequent absence of reciprocal cuckoldry.     

Extrapair paternity in a flock-living passerine, the vinous-throated parrotbill Paradoxornis webbianus

Understanding the factors that affect the occurrence of extrapair paternity (EPP) is one of the central issues in sexual selection. We investigated genetic parentage and the ecological factors affecting patterns of EPP in the vinous-throated parrotbill, Paradoxornis webbianus , a flock-living species with double broods. Using microsatellite DNA fingerprinting, we determined parentage of 246 offspring in 50 broods over two years (2005 and 2006). Nineteen offspring (8%) from 13 broods (26%) were sired by extrapair males and one offspring (0.4%) was probably the result of intraspecific brood parasitism. The prevalence of EPP varied significantly through the breeding season: 95% of broods with EPP (12/13) occurred in the first of two laying peaks. Parentage assignment revealed that half of extrapair males (6/12) were adjacent neighbours. The distribution of EPP was not significantly related to the ecological factors including breeding density and breeding synchrony. Instead, we suggest that social characteristics such as flocking and weak territoriality may determine the observed pattern of EPP in this study.     

Extrapair paternity, inclusive fitness, and within-group benefits of helping in western bluebirds

In central coastal California, USA, 3–16% of western bluebird ( Sialia mexicana ) pairs have adult male helpers at the nest. Demographic data on a colour-ringed population over a 13-year period indicate that helpers gain a small indirect fitness benefit through increases in the number of young fledged from nests of close kin. A small proportion of adult helpers (16%) that were able to breed and help simultaneously had higher annual inclusive fitness than males that only bred. These males comprised such a minor proportion of helpers that the mean fitness of helpers was still lower than the mean fitness of independent breeders. We used DNA fingerprinting to determine whether extrapair fertilizations alter within-group benefits enough to tip the balance in favour of helping behaviour. Overall, 19% of 207 offspring were sired by males other than their social father and extrapair fertilizations occurred in 45% of 51 nests. Intraspecific brood parasitism was rare so that mean mother-nestling relatedness approximated the expected value of 0.5. Extrapair paternity reduced putative father-offspring relatedness to 0.38. Mean helper-nestling relatedness was 0.41 for helpers assisting one or both parents and 0.28 for helpers aiding their brothers. Helpers rarely sired offspring in the nests at which they helped. Helping was not conditional on paternity and helpers were not significantly more closely related to offspring in their parents' nests than to offspring in their own nests. Although helpers may derive extracurricular benefits if helping increases their own or their father's opportunities for extrapair fertilizations, within-nest inclusive fitness benefits of helping do not compensate males for failing to breed. Breeding failure and constraints on breeding are the most likely explanations for why most helpers help.     

Extrapair paternity and genetic diversity: the white‐throated dipper Cinclus cinclus

Passerine bird species vary considerably in the frequency of extrapair paternity, but the factors causing this variation are not well understood. There is some comparative evidence that extrapair paternity is associated with the population level of genetic diversity, but there is no consensus of how genetic diversity should be measured and compared across species or populations. Here we report a low frequency of extrapair paternity (2% extrapair offspring) in a Norwegian population of the white‐throated dipper Cinclus cinclus, which shows strong signs of reduced genetic diversity. We encountered difficulties in constructing a robust parentage analysis system for the species, largely due to consistently low polymorphism levels in 100 heterologous microsatellite markers. Furthermore, single‐nucleotide polymorphisms (SNPs) were almost absent in intron sequences in 10 nuclear genes (>5 kb) that are much more polymorphic in other species. Hence, our results seem consistent with the genetic diversity hypothesis that predicts a low frequency of extrapair paternity in species with low genetic diversity. Heterologous microsatellite markers are generally unsuitable for interspecific comparisons of genetic diversity as they show strong phylogenetic dependency in polymorphism levels. We suggest that SNP rates at homologous nuclear introns, like those presented here, can provide a useful method for obtaining unbiased estimates of genome‐wide genetic diversity across populations and species.     

Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird

We tested the novel hypothesis that arrival date in migratorybirds represents a reliable indicator of male quality that canbe used by females as a cue in extrapair mating decisions. Secondarysexual characters are often condition-dependent, and competitionfor early arrival leads to condition-dependent migration. Hence,both secondary sexual characters and arrival date are predictedto be condition-dependent indicators of male phenotypic quality.We studied the relationship between expression of a secondarysexual character, arrival date, and condition, respectively,and extrapair paternity in a Spanish population of barn swallows,Hirundo rustica. By using microsatellite markers to determinepaternity, we showed that 17.8% of all offspring (N = 674) and32.4% of all broods (N = 170) were due to extrapair paternity.Quasi-parasitism (in which the male nest owner fathered theoffspring, but the eggs were laid by another female) occurredin 2.6% of all nestlings and 2.9% of all broods. Individualswere consistent in the frequency of extrapair paternity amongfirst, second, and third broods. Males with long outermost tailfeathers, arriving early and in prime body condition, had littleextrapair paternity in their nests. This was also the case whencontrolling for the confounding effects of male age. Partialcorrelation analysis was used to investigate the direct andindirect effects of tail length, arrival date, and body conditionon extrapair paternity. Body condition accounted for most ofthe variance in extrapair paternity, whereas tail length andarrival date accounted for a smaller proportion of the variance.Body condition was strongly correlated with tail length andarrival date. However, because females cannot directly assesscondition or arrival date (males arrive before females), femalesmay obtain an indirect measure of condition and migration abilityfrom tail length and other phenotypic traits of males. Thissuggests that extrapair paternity depends on the effects ofcondition, through its indirect effects on arrival date, taillength, and other variables.     

Extrapair paternity in the common sandpiper, Actitis hypoleucos, revealed by DNA fingerprinting

The prevalence of extrapair paternity in many socially monogamous passerines has not been mirrored in most monogamous nonpasserines studied to date. Here, we investigated the reproductive behaviour of a socially monogamous shorebird, the common sandpiper, using multilocus DNA fingerprinting. Given the high level of paternal care in the species, and the likely high costs in allocating care between kin and nonkin in species with precocial young, we predicted low levels of extrapair paternity similar to other monogamous shorebirds. We found the social mating system to be predominantly monogamous although one polyandrous pairing was identified. Of 83 offspring from 27 broods, 13 (15.7%) young from five (18.5%) broods were identified as being extrapair. There was no evidence of intraspecific nest parasitism or quasiparasitism. In this population, territorial intrusions were carried out largely by males but did not appear to be related to seeking extrapair copulations (EPCs). Seventy copulation attempts were observed and most were within-pair (84%). Six of eight EPC attempts occurred outside the territory of the female's social mate. Copulation rates were significantly higher just before and during egg laying than at other times during the study. At least two females that reared extrapair young had associated with males other than their eventual mates on arrival, suggesting that some females use rapid mate switching as a mating tactic, facilitated perhaps by the asynchronous arrival among both sexes in this population. Why some female sandpipers mate promiscuously remains unresolved.     

Immune defence,extra-pair paternity,and sexual selection in birds

Secondary sexual characters have been suggested to reliably reflect the ability of individuals to resist debilitating parasites, and females may gain direct or indirect fitness benefits from preferring the most extravagantly ornamented males. Extra-pair paternity provides an estimate of an important component of sexual selection in birds. Species with a high frequency of extra-pair paternity have a variance in realized reproductive success that is greater than the variance in apparent reproductive success, and extra-pair copulations and hence extra-pair paternity by females are often directly associated with the expression of male secondary sexual characters. If sexually dichromatic species have experienced a long period of antagonistic coevolution with their parasites, such species should have evolved larger immune defence organs than sexually monochromatic species. Bird species with sexual dichromatism had larger spleens for their body size than monochromatic species in a comparative analysis. Furthermore, species with a high frequency of extra-pair paternity were sexually dichromatic and had large spleens for their body size. These results are consistent with the hypothesis that females of dichromatic bird species seek extra-pair copulations to obtain indirect fitness benefits in terms of superior resistance of their offspring to virulent parasites.     

Causes of extra-pair paternity and its inter-specific variation in socially monogamous birds

Based on molecular technology, researchers find that extra-pair paternity (EPP) prevails among socially monogamous bird species. This phenomenon challenges traditional views of sexual selection and mating system, and has become one of the hot-spots in the avian behavior ecology. This review focuses on the evolutionary causes leading to EPP and the potential factors affecting it. Early studies of EPP in birds used a wide variety of tools, including plumage color polymorphism, polymorphic enzymes, and sex-differences in estimation of the heritability of morphological traits. Although each of these methods can be used to estimate the likelihood that EPP are present or absent in a population, none of them provide enough accurate estimation to allow meaningful cross-species comparison. Currently, studies of EPP mainly use “DNA-methods”, namely multi-locus mini-satellite fingerprints, single-locus mini-satellite fingerprints, and micro-satellite genotyping, because they can provide accurate outcome of paternity identification and their results are reproducible. From the point of the female, the driving forces for EPP are that females may gain direct benefits or indirect genetic benefits from EPP. Hypotheses explaining the benefits include fertility assurance, good genes, genetic compatibility, and genetic diversity. Despite large numbers of theoretically plausible explanations for EPP, there have been few direct empirical tests that can provide unambiguous support for only one type of explanation. The most straightforward test of the genetic benefit hypothesis of extra-pair copulation is a comparison of the performance of maternal half-siblings from multiply sired broods. Some highly-cited landmark studies spectacularly support the genetic benefit hypothesis, while other studies failed to reveal any systematic differences in maternal half-sibling performance, even in the same species or in taxonomically closely-related species. Briefly, the point that purpose of extra-pair copulation is to gain genetic benefits is still facing great challenges. Therefore, some researchers suggest that more attention should be focused on the interactions between parties involved in the extra-pair paternity phenomenon. Others, however, believe that such interactions can also be of a cooperative nature, and involve exchange of direct benefits. In brief, an approach focusing on interactions (involving either conflict or cooperation) seems to be the most promising direction to improve our understanding of the phenomenon of extra-pair paternity. As for the factors leading to intra- and inter-specific variation in the level of EPP, current researches mainly focus on the breeding density, breeding synchrony, the complexity of the habitat, paternal care, adult mortality, food availability, and genetic diversity. Explaining intra- and inter-specific variation in the extent of EPP has been difficult, but an appreciation of the problems of small sample sizes, and an ever-increasing comparative database have led to several recent advances. It now seems probable that differences between species in the rate of EPP are due to a combination of differences in life history, pattern of parental care, and local opportunities for promiscuity. In a word, although there have been a lot of theoretical and empirical researches about EPP of birds, no consensus on the basic questions has been received in this area. Thus, more scientific statistical analysis method and more empirical experiments are still badly needed to improve the theoretical system.     

Extrapair paternity in the blue tit (Parus caeruleus) : female choice, male charateristics, and offspring quality

Extrapair paternity is common in many birds, and it is now generallyaccepted that female choice plays an important role. However,die benefits that females obtain from extrapair paternity aremuch less dear. To test the hypothesis that females obtain indirectfitness benefits, we studied paternity in a blue tit populationover 4 years. Extrapair paternity occurred in 31-47% of allnests and accounted for 11-14% of all offspring. Most malesthat fathered extrapair young did not lose paternity themselves,males never "exchanged" paternity, and within nests the extrapairoffspring were usually fathered by a single male. Comparisonsbetween males that did and did not lose paternity and pairwisecomparisons between the extrapair male(s) and the within-pairmale showed that successful males had longer tarsi and sangon average longer strophes during the dawn chorus. Successfulmales weighed less (relative to their size) during the nettlingstage, but nevertheless they survived better. Male age did notinfluence their likelihood of losing paternity, but extrapairmales were usually older than the within-pair male they cuckolded.Within nests with mixed paternity, extrapair young were morelikely to survive than within-pair young in cases of partialbrood mortality. Our data also suggest that extrapair offspringwere more likely to be males. Because extrapair males were usuallyclose neighbors, male quality should be considered relativeto the quality of the neighbors. Despite this, we found consistencyin female choice over years. Our observations provide supportfor the hypothesis that female blue tits engage in extrapaircopulations to obtain good genes for their offspring.