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.     

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.     

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.     

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.     

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.     

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet     

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

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

Extra-pair paternity in monogamous and polygynous Savannah sparrows,Passerculus sandwichensis

Extra-pair paternity can influence mating systems by affecting the fitness costs associated with polygyny. Polygyny is disadvantageous to males when the time and energetic demands of multiple pairings decrease either a male's success at gaining extra-pair fertilizations or his ability to ensure paternity among harem members. In Savannah sparrows,Passerculus sandwichensison Kent Island, New Brunswick, Canada, multilocus DNA fingerprinting of 136 adults and young revealed substantial female infidelity: overall, 31 of 92 young (33.7%) in 15 of 24 nests (62.5%) were the product of extra-pair fertilizations. Male mating status was a strong predictor of paternity. Each of seven monogamous females produced at least one extra-pair offspring, but only six of 11 primary females (54.5%) and two of six secondary females (33.3%) were unfaithful. As a result, nearly 80% of the young in nests of polygynous males resulted from within-pair fertilizations, compared with only 40% of the young in nests of monogamous males. Kent Island Savannah sparrows are simultaneously polygynous, and the absence of paternity costs associated with polygyny is surprising. The observed pattern of paternity suggests the operation of female choice, although male control of parentage cannot be excluded.     

Male extraterritorial forays, age and paternity in the socially monogamous reed bunting (Emberiza schoeniclus)

Genetic studies have shown that extra-pair paternity is widespread among socially monogamous bird species. Yet, the role of males and females and their behavior leading to this mixed reproductive strategy is poorly understood. Here, we analyze paternity in relation to male age and mating behavior in the socially monogamous reed bunting (Emberiza schoeniclus). We report a positive relation between male extraterritorial forays and success in obtaining extra-pair fertilizations. Extraterritorial forays tended to increase in frequency with male age and older males sired a larger number of extra-pair offspring than young males. Identified extra-pair sires were old in nine out of ten cases. The likelihood of being cuckolded was not affected by male age. Although based on correlative data, our results highlight age-dependent explorative male behavior as a key determinant for the understanding of extra-pair mating in the reed bunting. We do, however, emphasize the need for further studies to reveal the role of females in extra-pair copulations and fertilizations.     

Do Female Red-winged Blackbirds Engage in a Mixed Mating Strategy?

Parentage analyses of broods of nestling red-winged blackbirds (Agelaius phoeniceus) revealed that extra-pair fertilizations (EPFs) accounted for 24% of the offspring. 8% of attempted copulations and 13% of male courtship displays during observations of focal females were by extra-pair males. In addition, mates and non-mates often chased and occasionally made physical contact with females; 34% of those chases in which contact was made were extra-pair chases. Females behaved variably during both within-pair and extra-pair events; females crouched less and resisted more frequently during extra-pair courtship than during within-pair courtship. All extra-pair events, whether natural or induced by male removal, were either resisted or accepted by the female. In 318 focal female-hours of observation during the fertilizable period, no female was ever seen in another male's territory soliciting a copulation. In addition, removal of females' mates resulted in frequent extra-pair courtship and copulation; all of these occurred on the removed male's territory. Some females left their mates' territories on occasion — these forays were nearly always off the study area, no female was ever seen copulating with an extra-pair male while on these forays, and neither the frequency nor the duration of female forays correlated with the frequency of extra-pair fertilizations within broods. There were no associations between extra-pair fertilizations and female age, settlement order, nest order, or clutch size. The number of fledglings produced from a nest was significantly positively associated with the number of sires of the brood. Fewer offspring apparently starved in broods that were multiply sired, yet males did not provide courtship feedings during either within-pair or extra-pair copulations, nor was any paternal care provided to young sired through extra-pair matings. The frequency of infertile eggs was low (< 1%); in those instances of infertile eggs the territory owner sired some young in the same nest or another nest on his territory. Fewer broods were a mixture of within-pair and extra-pair paternity than expected by chance. Clear evidence implicating a mixed strategy on the part of females could not be gathered. Because females behaved variably and because not all costs and benefits to females of extra-pair copulations could be measured, it remains possible that female behavior patterns are either (1) part of a mixed strategy, or (2) part of a strategy minimizing the costs of copulation.     

Variation in social organization influences the opportunity for sexual selection in a social lizard

Social monogamy has traditionally been suggested to be maintained because of weak sexual selection on male partner acquisition. However, the ubiquitous incidence of extra-pair paternity suggests that sexual selection can be strong in monogamous systems, although studies partitioning variance in male reproductive success have come to mixed conclusions. Here, we use detailed field data to examine variance in male reproductive success and its implications for the maintenance of sociality in a population of the socially monogamous lizard Egernia whitii. We show that both within-pair and, to a lesser extent, extra-pair partner acquisition contribute to the variance in male reproductive success, resulting in considerable opportunity for sexual selection. Despite this, levels of multiple mating are lower in Egernia compared to other reptiles, suggesting that male partner acquisition is constrained. We suggest that this constraint may be a result of strong territoriality combined with sexual conflict over multiple mating generated by costs of extra-pair paternity to females as a result of facultative male care. This has the potential to limit sexual selection by reducing variance in male reproductive success and therefore contribute to the maintenance of complex social organization.     

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.     

Little effect of extrapair paternity on the opportunity for sexual selection in Savannah sparrows (Passerculus sandwichensis)

Extrapair paternity (EPP) can dramatically increase the opportunity for sexual selection if relatively few males are able to monopolize the majority of fertilizations in a population. Although recent work with birds suggests that EPP can increase the standardized variance in male reproductive success (Is) as much as 13-fold, only a male's within-pair success is typically quantified with any accuracy. In most cases, nearly half of all extrapair young are of unknown parentage. A strong, negative correlation across studies between the proportion of extrapair young for which parentage is known and the apparent effect of EPP on Is (r(s) = -0.71, P = 0.013, N = 13 studies) suggests that the incomplete sampling of extrapair sires has greatly exaggerated the influence of EPP. To achieve a more thorough accounting of EPP and its importance to variation in male fitness, we used a suite of four to six microsatellite loci to identify extrapair young and their sires in a polygynous population of Savannah sparrows (Passerculus sandwichensis). Pooling over the 2002 and 2003 breeding seasons, 79 of 116 females (68.1%) produced young outside of the pairbond and 194 of 411 offspring (47.2%) were extrapair. We identified sires for 96.4% of all young (N = 396), including sires for 92.3% of the extrapair young (N = 179), allowing us to partition Is into within-pair and extrapair components. In both years, EPP-related fitness components generated more variation in male reproductive success than the number or quality of within-pair mates. Differences among males in the number of extrapair mates alone accounted for 56.6% of Is in 2002 and for 23.6% of Is in 2003. Nonetheless, in absolute terms, the occurrence of EPP on Kent Island increased the opportunity for sexual selection less than two-fold. Averaging over the two years, Is was only 78% higher than Is,app, the variance in male reproductive success that would have occurred had EPP been nonexistent and males sired all young on their territories. Likewise, across nine socially monogamous species, we found no correlation between the extent of EPP and its effect on the opportunity for sexual selection (Is/Is,app) and only a marginally significant positive correlation between EPP and Is itself. Taken together, our results suggest that the relationship between EPP and sexual selection in birds may be much less strong and much less straightforward than commonly thought.     

The heterozygosity theory of extra-pair mate choice in birds: a test and a cautionary note

Although extra-pair fertilizations (EPF) are common in socially monogamous systems, the benefits to females remain elusive. One potential benefit that recently has begun to receive empirical attention is increased offspring heterozygosity. We tested the heterozygosity hypothesis in the black-throated blue warbler Dendroica caerulescens using a panel of five microsatellite loci. We did not find any evidence that male heterozygosity influenced female extra-pair mating patterns, that females choose genetically dissimilar extra-pair mates, nor that extra-pair offspring were more heterozygous than within-pair offspring. However, simple Monte Carlo simulations indicated that the number of microsatellite loci used in this study, and most other recent studies, would detect an effect of heterozygosity only if that effect is pronounced. Thus, we were unable to demonstrate any effect of offspring heterozygosity in our study species, but a more subtle effect remains possible. Researchers wishing to test this hypothesis should use a large number of genetic markers and interpret negative results cautiously.     

No evidence of genetic benefits from extra-pair fertilisations in female sand martins (Riparia riparia)

Genetic parentage studies of socially monogamous birds reveal a widespread prevalence of extra-pair paternity. Variation in extra-pair paternity among individuals may depend on how different individuals benefit from extra-pair fertilisations and on the opportunity to pursue extra-pair copulations. A long-term study of sand martins (Riparia riparia) in Hungary allowed us to examine patterns of extra-pair fertilisations in a large colony of over 3,000 breeding pairs with many known age individuals. We used multi-locus DNA fingerprinting to determine whether extra-pair fertilisations occur when females are paired to (1) presumably low quality mates, or (2) genetically similar or dissimilar mates, and whether extra-pair fertilisations result in offspring of higher quality. Extra-paternal young were found in 38% of 47 broods and comprised 19% of 190 offspring. Males that lost paternity did not differ significantly from others in age or body condition. Social mates of broods containing extra-pair offspring did not differ in genetic similarity from pairs without extra-pair offspring. Furthermore, there was no significant difference in body condition between extra-pair young and their maternal half-siblings. We were unable to assign paternity and therefore cannot exclude the possibility that extra-pair males differed from the within-pair males they cuckolded, in age, body condition or genetic similarity with the female. We found a positive relationship between paternity losses and breeding density, suggesting that low breeding density may constrain opportunities for seeking extra-pair copulations.     

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

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

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.     

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.     

Low frequency of extra-pair paternity in two colonies of the socially monogamous short-tailed shearwater Puffinus tenuirostris

The short-tailed shearwater is a colonially nesting, socially monogamous seabird. Little is known about mate fidelity and breeding behaviour in this species because breeding birds are nocturnal on land and spend much of their time within subterranean nesting burrows. Colonial breeding and extended sperm storage create opportunities for extra-pair copulations which may form a significant component of the mating strategy in this species. Multilocus DNA fingerprinting was used to examine the genetic relationship between nestlings and the male and female nest attendants in 83 burrows from two distinct breeding colonies. Genetic analyses identified nine nestlings, approximately equally distributed between the two colonies, that were not related to the attendant pair male in those burrows, implying extra-pair paternity through extra-pair copulations. These results are used retrospectively to discuss the characteristics of extra-pair copulations and extra-pair fertilizations and the implications for estimates of life-time reproductive success in the short-tailed shearwater.     

Additive genetic variance, heritability, and inbreeding depression in male extra-pair reproductive success

The hypothesis that female extra-pair reproduction in socially monogamous animals reflects indirect genetic benefits requires that there be additive and/or nonadditive genetic variance in fitness. However, the specific hypotheses that male extra-pair reproductive success (EPRS) shows additive genetic variance (V(A)), heritability (h2), or inbreeding depression, and hence that females could acquire indirect genetic benefits through increased EPRS of sons, have not been explicitly tested. We used comprehensive genetic pedigree data from song sparrows (Melospiza melodia) to estimate V(A), h2, and inbreeding depression in the number of extra-pair offspring a male sired per year and the probability that a male would sire any extra-pair offspring per year. Inbreeding depression was substantial: more inbred males sired fewer extra-pair offspring and were less likely to sire any extra-pair offspring. In contrast, estimates of V(A) and h2 were close to 0, although 95% credible intervals were relatively wide. These data suggest that females could accrue indirect genetic benefits, in terms of increased EPRS of outbred sons, by mating with unrelated social or extra-pair mates. In contrast, any indirect benefit of extra-pair reproduction in terms of producing sons with high additive genetic value for EPRS is most likely to be small.