Microsatellite identification of extrapair sires in a socially monogamous warbler

Few studies of avian mating systems have identified the siresof extrapair young, and hence it has been difficult to determinethe scale at which reproductive interactions occur. For instance,females may be free to copulate with any male in the population(a "global" scale of interactions), or females may be restrictedto copulating only with males on neighboring territories (a"local" scale). The scale of such interactions has importantconsequences for an understanding of the evolutionary causesand consequences of extrapair fertilizations. We used five hypervariable microsatellite loci and multilocus DNA fingerprintingto examine parentage of more than 400 nestling black-throatedblue warblers (Dendroica caerulescens). Extrapair fertilizationswere common, and the microsatellite markers allowed us to identifythe sires for 89% of the young analyzed. Most identified extrapairsires were males on neighboring or nearby territories, andmost nestlings for whom we could not identify a sire came fromterritories at the edge of the study plot. Thus, reproductive interactions appear to be more local than global in this population.Extrapair fertilizations contributed significantly to totalvariation in male reproductive success. However, the standardizedvariance in male reproductive success (0.68-0.74) was not substantiallygreater than that for females (0.53-0.60), and the contributionof extrapair fertilizations (9-14%) was much lower than thecontribution of within-pair fertilizations (75-77%). This suggeststhat the local scale of reproductive interactions may limitvariation in male reproductive success and hence the opportunityfor selection.     

EFFECTS OF SOCIAL AND EXTRA‐PAIR MATING ON SEXUAL SELECTION IN BLUE TITS (CYANISTES CAERULEUS)

The contribution of extra‐pair paternity (EPP) to sexual selection has received considerable attention, particularly in socially monogamous species. However, the importance of EPP remains difficult to assess quantitatively, especially when many extra‐pair young have unknown sires. Here, we combine measurements of the opportunity for selection (I), the opportunity for sexual selection (I_S), and the strength of selection on mating success (Bateman gradient, β_SS) with a novel simulation of random mating tailored to the specific mating system of the blue tit (Cyanistes caeruleus). In a population where social polygyny and EPP are common, the opportunity for sexual selection was significantly stronger and Bateman gradients significantly steeper for resident males than for females. In general, success with the social mate(s) contributed most to variation in male reproductive success. Effects of EPP were small, but significantly higher than expected under random mating. We used sibship analysis to estimate the number of unknown sires in our population. Under the assumption that the unknown sires are nonbreeding males, EPP reduced the variance in and the strength of selection on mating success, a possibility that hitherto has not been considered.     

Survival of extrapair and within-pair young in tree swallows

In monogamous species, it is generally accepted that males seekextrapair matings to increase their reproductive success withoutadditional parental investment; however, the benefits of extrapairmatings to females are much less clear. One possibility isthat females obtain genes for enhanced offspring viabilityfrom the extrapair sires. If this is the case, then the increasedviability of extrapair young may be evident throughout the periodof embryonic development as well as later in life. Tree swallows(Tachycineta bicolor) have one of the highest known levelsof extrapair mating in birds, and females have substantialcontrol over the paternity of their offspring. We used moleculartechniques to determine the parentage of nestlings and unhatchedembryos to examine the possibility that female tree swallowsgain viability benefits for their extrapair offspring. Althoughboth extrapair paternity and mortality of embryos and nestlingswere high (89% and 54% of broods respectively), we found nodifference in the viability of within-pair and extrapair youngprior to fledging. In addition, extrapair young were not morelikely to be male. There was no bias in the sex of young atfledging, but unhatched embryos were more likely to be male.Our results do not support the idea that female tree swallowsengage in extrapair mating to increase offspring viability,at least early in life.     

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 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.     

Effects of extra-pair and within-pair reproductive success on the opportunity for selection in birds

The number of mates, their fecundity, and the number of extra-pairfertilizations can all affect male reproductive success in biparentalspecies. Extra-pair mating in birds has been of particular interest,because it could generate strong levels of sexual selectioneven when a species is socially monogamous. We examined howextra-pair fertilizations affect the opportunity for selectionin the sexually dimorphic common yellowthroat (Geothlypis trichas)and the sexually monomorphic house wren (Troglodytes aedon).We were able to identify sires for at least 95% of all nestlings,and, thus, we were able to make a nearly complete accountingof male reproductive success. Although extra-pair fertilizationswere common in yellowthroats (26% of young) it contributed little(21%) to the total variance in male reproductive success. Mostof the variance in reproductive success (58%) was attributableto the male's within-pair success, which was influenced primarilyby the number of young produced by each mate and the proportionof within-pair young sired. Despite a moderate level of extra-pairfertilizations (10% of young) in house wrens, almost all ofthe variance in male reproductive success (97%) was attributableto within-pair success, particularly the number of social mates.Although extra-pair fertilizations generally increase the variancein male reproductive success, within-pair reproductive successmay be the major source of variation in male reproductive success.Thus, sexual dimorphism in monogamous birds may be influencedmore by the number of mates and their fecundity than by extra-pairmatings.     

Promiscuity drives sexual selection in a socially monogamous bird

Many socially monogamous species paradoxically show signs of strong sexual selection, suggesting cryptic sources of sexual competition among males. Darwin argued that sexual selection could operate in monogamous systems if breeding sex ratios are biased or if some males attract highly fecund females. Alternatively, sexual selection might result from promiscuous copulations outside the pair bond, although several recent studies have cast doubt on this possibility, in particular by showing that variance in apparent male reproductive success (number of social young) differs little from variance in actual male reproductive success (number of young sired). Our results from a long-term study of the socially monogamous splendid fairy-wren (Malurus splendens) demonstrate that such comparisons are misleading and do not adequately assess the effects of extra-pair paternity (EPP). By partitioning the opportunity for selection and calculating Bateman gradients, we show that EPP has a strong effect on male annual and lifetime fitness, whereas other proposed mechanisms of sexual selection do not. Thus, EPP drives sexual selection in this, and possibly other, socially monogamous species.     

Extra-pair mating,male plumage coloration and sexual selection in yellow warblers (Dendroica petechia)

Extra-pair mating has been proposed as a source of sexual selection responsible for secondary sexual traits that are common among socially monogamous birds, although supporting evidence is scant. In the socially monogamous yellow warbler, males are larger than females, and unlike females, have extensive reddish streaking on their breasts. Using DNA fingerprinting we show that within-pair parentage was positively related to male size, and that extra-pair mating success was positively related to the amount of streaking on the breast. To our knowledge, this is the first intraspecific evidence of an association between a male plumage ornament and gains of extra-pair paternity that is apparently independent of age. This study confirms that extra-pair mating can be an important mechanism of sexual selection even when the most successful sires are commonly cuckolded, and refutes a previous hypothesis that the variation in plumage and behaviour among male yellow warblers is an example of alternative, equally successful, evolutionarily stable strategies (ESS). More generally, the demonstrated independence of within-pair and extra-pair success and their associated traits indicates that where animals have multiple secondary sexual traits, different traits may be selected by different mechanisms that contribute to total reproductive success.     

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.     

Experimental food supplementation reveals habitat-dependent male reproductive investment in a migratory bird

Environmental factors can shape reproductive investment strategies and influence the variance in male mating success. Environmental effects on extrapair paternity have traditionally been ascribed to aspects of the social environment, such as breeding density and synchrony. However, social factors are often confounded with habitat quality and are challenging to disentangle. We used both natural variation in habitat quality and a food supplementation experiment to separate the effects of food availability—one key aspect of habitat quality—on extrapair paternity (EPP) and reproductive success in the black-throated blue warbler, Setophaga caerulescens. High natural food availability was associated with higher within-pair paternity (WPP) and fledging two broods late in the breeding season, but lower EPP. Food-supplemented males had higher WPP leading to higher reproductive success relative to controls, and when in low-quality habitat, food-supplemented males were more likely to fledge two broods but less likely to gain EPP. Our results demonstrate that food availability affects trade-offs in reproductive activities. When food constraints are reduced, males invest in WPP at the expense of EPP. These findings imply that environmental change could alter how individuals allocate their resources and affect the selective environment that drives variation in male mating success.     

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.     

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.     

Genetic evidence for the mating system and reproductive success of black sea bream (Acanthopagrus schlegelii)

Understanding the mating system and reproductive success of a species provides evidence for sexual selection. We examined the mating system and the reproductive success of captive adult black sea bream (Acanthopagrus schlegelii), using parentage assignment based on two microsatellites multiplex PCR systems, with 91.5% accuracy in a mixed family (29 sires, 25 dams, and 200 offspring). Based on the parentage result, we found that 93.1% of males and 100% of females participated in reproduction. A total of 79% of males and 92% of females mated with multiple partners (only 1 sire and 1 dam were monogamous), indicating that polygynandry best described the genetic mating system of black sea bream. For males, maximizing the reproductive success by multiple mating was accorded with the sexual selection theory while the material benefits hypothesis may contribute to explain the multiple mating for females. For both sexes, there was a significant correlation between mating success and reproductive success and the variance in reproductive success of males was higher than females. Variation in mating success is the greatest determinant to variation in reproductive success when the relationship is strongly positive. The opportunity for sexual selection of males was twice that of females, as well as the higher slope of the Bateman curve in males suggested that the intensity of intrasexual selection of males was higher than females. Thus, male–male competition would lead to the greater variation of mating success for males, which caused greater variation in reproductive success in males. The effective population number of breeders (N_b) was 33, and the N_b/N ratio was 0.61, slightly higher than the general ratio in polygynandrous fish populations which possibly because most individuals mated and had offspring with a low variance. The relatively high N_b contributes to the maintenance of genetic diversity in farmed black sea bream populations.     

Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection

Sexual selection theory posits that ornamental traits can evolve if they provide individuals with an advantage in securing multiple mates. That male ornamentation occurs in many bird species in which males pair with a single female is therefore puzzling. It has been proposed that extra-pair mating can substantially increase the variance in reproductive success among males in monogamous species, thus increasing the potential for sexual selection. We documented the frequency of extra-pair paternity and examined its effect on variation in male reproductive success in the mountain bluebird Sialia currucoides , a socially monogamous songbird in which males possess brilliant plumage ornamentation. Extra-pair paternity was common in our Wyoming study population, with 72% of broods containing at least one extra-pair offspring. The standardized variance in actual male reproductive success (i.e., the total number of within-pair and extra-pair offspring sired) was more than seven times higher than the variation in apparent success (i.e., success assuming that no extra-pair mating occurred). Success at siring within-pair and extra-pair offspring both contributed to the variation in overall male reproductive success. Within-pair success, however, did not predict a male's level of extra-pair success, suggesting that males do not sacrifice within-pair paternity to gain extra-pair paternity. Calculation of the sexual selection (Bateman) gradient showed that males sire approximately two additional offspring for each extra-pair mate that we identified. Thus, in this sexually dichromatic species, extra-pair mating increases the variance in male reproductive success and provides the potential for sexual selection to act.     

No evidence of current sexual selection on sexually dimorphic traits in a bird with high variance in mating success

Sexual dimorphism, particularly in ornamental traits, is likely to have arisen by sexual selection. Most empirical and theoretical studies of sexual dimorphism assume that ongoing sexual selection also maintains the dimorphism. Over four seasons, I measured the sexual selection acting on three sexually dimorphic attributes (epaulet size, body size, and the blackness of the body plumage) of male red-winged blackbirds and found no consistent directional or stabilizing selection on any of them. Correlational selection was also negligible. I used path analysis to explore potential relationships in more detail but found no direct or indirect effects of male traits on either within- or extrapair success. Males who were resident on the marsh for more years had higher within-pair success, primarily because they spent more of the season on their territory. Experimental manipulations of epaulet size and color and the extent of nonblack feathers in the black body plumage had no detectable effect on the number of within-pair mates, paternity, or the number of extrapair offspring sired in nearby territories. These results combine with data from other studies of red-winged blackbirds to suggest that, despite high variation in male mating success and hence a strong opportunity for sexual selection, several morphological attributes that differ between the sexes and vary among males are not under current sexual selection. The possible explanations for why add complexity to our understanding of how sexual selection operates.     

Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus)

In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.     

Pronounced reproductive skew in a natural population of green swordtails, Xiphophorus helleri

For many species in nature, a sire's progeny may be distributed among a few or many dams. This poses logistical challenges--typically much greater across males than across females--for assessing means and variances in mating success (number of mates) and reproductive success (number of progeny). Here we overcome these difficulties by exhaustively analyzing a population of green swordtail fish (Xiphophorus helleri) for genetic paternity (and maternity) using a suite of highly polymorphic microsatellite loci. Genetic analyses of 1476 progeny from 69 pregnant females and 158 candidate sires revealed pronounced skews in male reproductive success both within and among broods. These skews were statistically significant, greater than in females, and correlated in males but not in females with mating success. We also compare the standardized variances in swordtail reproductive success to the few such available estimates for other taxa, notably several mammal species with varied mating systems and degrees of sexual dimorphism. The comparison showed that the opportunity for selection on male X. helleri is among the highest yet reported in fishes, and it is intermediate compared to estimates available for mammals. This study is one of a few exhaustive genetic assessments of joint-sex parentage in a natural fish population, and results are relevant to the operation of sexual selection in this sexually dimorphic, high-fecundity species.     

Extra-pair paternity and sexual dimorphism in birds

Differences in the strength of sexual selection between males and females can lead to sexual dimorphism. Extra-pair paternity (EPP) can increase the variance in male reproductive success and hence the opportunity for sexual selection. Previous research on birds suggests that EPP drives the evolution of dimorphism in plumage colour and in body size. Because EPP increases the intensity of sexual selection in males, it should lead to increased dimorphism in species with larger or more colourful males, but decreased dimorphism in species with larger or more colourful females. We explored the covariation between EPP and sexual dimorphism in wing length and plumage colouration in 401 bird species, while controlling for other, potentially confounding variables. Wing length dimorphism was associated positively with the frequency of EPP, but also with social polygamy, sex bias in parental behaviour and body size and negatively with migration distance. The frequency of EPP was the only predictor of plumage colour dimorphism. In support of our prediction, high EPP levels were associated with sexual dichromatism, positively in species in which males are more colourful and negatively in those in which females are more colourful. Contrary to our prediction, high EPP rates were associated with increased wing length dimorphism in species with both male- and female-biased dimorphism. The results support a role for EPP in the evolution of both size and plumage colour dimorphism. The two forms of dimorphism were weakly correlated and predicted by different reproductive, social and life-history traits, suggesting an independent evolution.     

Extrapair paternity and egg hatchability in tree swallows: evidence for the genetic compatibility hypothesis?

Tree swallows (Tachycineta bicolor) show one of the highestlevels of extrapair paternity in birds, and there is evidencethat females have control over who fathers their offspring.However, it is unclear which benefits female tree swallows obtainfrom mating with multiple males. Using microsatellite DNA fingerprinting,we studied extrapair paternity in relation to nesting successand male, female, and offspring characteristics. More than 70%of all nests contained extrapair young, and more than half ofall offspring were extrapair. Within broods, the extrapair youngwere often fathered by several males. Despite screening allresident and some floater males, we could identify the biologicalfather of only 21% of all extrapair offspring. All identifiedextrapair males were close neighbors. Extrapair males did notdiffer from within-pair males in any of the measured characteristics,except that the former had larger cloacal protuberances than thelatter. Extrapair males were equally successful in gaining paternityin their own broods as males that did not father extra young.In nests with mixed paternity, extrapair young did not differfrom within-pair young in body size or mass. However, nestswith extrapair young had higher hatching success than nestswithout extrapair young. All examined unhatched eggs were fertilizedand thus hatch failure resulted from embryo mortality. The availabledata are in accordance with the genetic diversity and the geneticcompatibility hypothesis, but not with the good genes hypothesis.     

Genetic similarity, extrapair paternity, and offspring quality in Savannah sparrows (Passerculus sandwichensis)

The occurrence of extrapair paternity (EPP) in birds is oftenattributed to the action of good-genes sexual selection wherebyfemales "trade up" on male genetic quality by allocating fertilizationsto males with better genes than those possessed by their socialmate. To date, most studies of EPP in birds focus on absolutemeasures of male quality as a criterion for female choice, althoughmultiple mating by females in other taxa is more commonly ascribedto benefits associated with the individual optimization of offspringgenotypes. Here, we examine whether the genetic similarity ofsocial mates predicts female mating patterns in a populationof Savannah sparrows (Passerculus sandwichensis) where as manyas 70% of adults produce extrapair young (EPY). We considerthe influence of genetic similarity across all stages of a female'sdecision-making process, from pair formation through the decisionto produce EPY, to the allocation of fertilizations to specificextrapair sires. In a 4-year study of 175 males, 206 females,and 506 offspring, females were more likely to produce EPY whenpaired to genetically similar males, but they did not appearto be influenced by the size, age, mass, individual heterozygosity,and genetic diversity of their social mates. In paired comparisons,females were almost twice as likely to decrease their geneticsimilarity to males when producing EPY as they were to increaseit. Nonetheless, females did not select especially dissimilarmales when mating outside the pair-bond nor did they pair disassortativelywith respect to genetic similarity. Relative measures of malequality may influence mating patterns in birds, but only atsome points in a female's decision-making process.