Experimental evidence that brighter males sire more extra‐pair young in tree swallows

Across taxa, extra‐pair mating is widespread among socially monogamous species, but few studies have identified male ornamental traits associated with extra‐pair mating success, and even fewer studies have experimentally manipulated male traits to determine whether they are related directly to paternity. As a consequence, there is little experimental evidence to support the widespread hypothesis that females choose more ornamented males as extra‐pair mates. Here, we conducted an experimental study of the relationship between male plumage colour and fertilization success in tree swallows (Tachycineta bicolor), which have one of the highest levels of extra‐pair mating in birds. In this study, we experimentally dulled the bright blue plumage on the back of males (with nontoxic ink markers) early in the breeding season prior to most mating. Compared with control males, dulled males sired fewer extra‐pair young, and, as a result, fewer young overall. Among untreated males, brighter blue males also sired more extra‐pair young, and in paired comparisons, extra‐pair sires had brighter blue plumage than the within‐pair male they cuckolded. These results, together with previous work on tree swallows, suggest that extra‐pair mating behaviour is driven by benefits to both males and females.     

Sources of (co)variation in alternative siring routes available to male great tits (Parus major)

Males of socially monogamous species can increase their siring success via within‐pair and extra‐pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five‐year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as “interactive phenotypes” arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra‐pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra‐pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.     

EXTRA‐PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra‐pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males’ apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free‐living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within‐pair reproductive success (WPRS) and extra‐pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0–27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males’ contributions to future generations, its impact on population‐level parameters such as the opportunity for selection and effective population size was limited.     

Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra‐pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within‐pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra‐pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade‐off between male within‐pair paternity success and extra‐pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.     

Spatial distribution of nests constrains the strength of sexual selection in a warbler

In socially monogamous species, extra‐pair paternity may increase the strength of intersexual selection by allowing males with preferred phenotypes to monopolize matings. Several studies have found relationships between male signals and extra‐pair mating, but many others fail to explain variation in extra‐pair mating success. A greater appreciation for the role that ecological contingencies play in structuring behavioural processes may help to reconcile contradictory results. We studied extra‐pair mating in a spatial context in the common yellowthroat (Geothlypis trichas), a territorial wood warbler. Over the course of 6 years, we observed 158 breeding attempts by 99 males, resulting in a total of 369 nests and 520 sampled nestlings. The spatial distribution of territories varied greatly, with males having between 0 and 10 close neighbours and between three and 39 neighbouring nestlings close enough to represent extra‐pair siring opportunities. Both within‐pair and extra‐pair reproductive success increased with breeding density, but the opportunity for sexual selection and strength of selection varied with density. Total variance in reproductive success was highest at low density and was mostly explained by variation in within‐pair success. In contrast, at high density, both within‐pair and extra‐pair successes contributed substantially to variance in reproductive success. The relationships between plumage and extra‐pair mating also varied by density; plumage was under strong sexual selection via extra‐pair mating success at high density, but no selection was detected at low density. Thus, ecological factors that structure social interactions can drive patterns of sexual selection by facilitating or constraining the expression of mating preferences.     

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.     

Age‐dependent trajectories differ between within‐pair and extra‐pair paternity success

Reproductive success is associated with age in many taxa, increasing in early life followed by reproductive senescence. In socially monogamous but genetically polygamous species, this generates the interesting possibility of differential trajectories of within‐pair and extra‐pair siring success with age in males. We investigate these relationships simultaneously using within‐individual analyses with 13 years of data from an insular house sparrow (Passer domesticus) population. As expected, we found that both within‐ and extra‐pair paternity success increased with age, followed by a senescence‐like decline. However, the age trajectories of within‐ and extra‐pair paternity successes differed significantly, with the extra‐pair paternity success increasing faster, although not significantly, in early life, and showing a delayed decline by 1.5 years on average later in life compared to within‐pair paternity success. These different trajectories indicate that the two alternative mating tactics should have age‐dependent pay‐offs. Males may partition their reproductive effort between within‐ and extra‐pair matings depending on their current age to reap the maximal combined benefit from both strategies. The interplay between these mating strategies and age‐specific mortality may explain the variation in rates of extra‐pair paternity observed within and between species.     

High rates of infidelity in the Grey Fantail Rhipidura albiscapa suggest that testis size may be a better correlate of extra‐pair paternity than sexual dimorphism

The Grey Fantail Rhipidura albiscapa is a socially monogamous passerine endemic to Australia. Behavioural and morphological clues point to opposing conclusions as to its breeding system; sexual monomorphism and monochrome colorations suggest monogamy, whereas relatively large testes and a prominent cloacal protruberance are more indicative of multiple mating and sperm competition. We used five highly variable microsatellite loci to investigate the genetic breeding system of this species. Paternity was assigned to 49 of 69 (71%) offspring tested and the overall rate of partner infidelity was high, with 55% of offspring being sired by an extra‐pair male and 64% of all clutches containing extra‐pair young. This puts the Grey Fantail amongst the most promiscuous socially monogamous species yet studied. Where extra‐pair fathers were identified, these were invariably in neighbouring territories, and although larger males did not gain more paternities overall, extra‐pair offspring tended to be fathered by larger males than expected by chance. We interpret our findings in light of some of the potential costs and benefits associated with extra‐pair paternity.     

FEMALE AND MALE GENETIC EFFECTS ON OFFSPRING PATERNITY: ADDITIVE GENETIC (CO)VARIANCES IN FEMALE EXTRA‐PAIR REPRODUCTION AND MALE PATERNITY SUCCESS IN SONG SPARROWS (MELOSPIZA MELODIA)

Ongoing evolution of polyandry, and consequent extra‐pair reproduction in socially monogamous systems, is hypothesized to be facilitated by indirect selection stemming from cross‐sex genetic covariances with components of male fitness. Specifically, polyandry is hypothesized to create positive genetic covariance with male paternity success due to inevitable assortative reproduction, driving ongoing coevolution. However, it remains unclear whether such covariances could or do emerge within complex polyandrous systems. First, we illustrate that genetic covariances between female extra‐pair reproduction and male within‐pair paternity success might be constrained in socially monogamous systems where female and male additive genetic effects can have opposing impacts on the paternity of jointly reared offspring. Second, we demonstrate nonzero additive genetic variance in female liability for extra‐pair reproduction and male liability for within‐pair paternity success, modeled as direct and associative genetic effects on offspring paternity, respectively, in free‐living song sparrows (Melospiza melodia). The posterior mean additive genetic covariance between these liabilities was slightly positive, but the credible interval was wide and overlapped zero. Therefore, although substantial total additive genetic variance exists, the hypothesis that ongoing evolution of female extra‐pair reproduction is facilitated by genetic covariance with male within‐pair paternity success cannot yet be definitively supported or rejected either conceptually or empirically.     

Digest: Extra‐pair mating and inbreeding avoidance in a socially monogamous fairy‐wren*

Infidelity in socially monogamous birds may be a mechanism of inbreeding avoidance and may be impacted by cooperative breeding. Hajduk et al. (2018) find that relatedness increases extra‐pair mating only in mother‐son social pairs of Malurus cyaneus, while a greater number of nest helpers consistently increases the proportion of extra‐pair offspring. These findings suggest that there may be multiple explanations for extra‐pair mating within a single population.     

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.     

Trading up: the fitness consequences of divorce in monogamous birds

Social and genetic mating systems play an important role in natural and sexual selection, as well as in the dynamics of populations. In socially monogamous species different genetic mating patterns appear when individuals mate outside the breeding pair within a breeding season (extra‐pair mating) or when they change partners between two breeding seasons (widowing or divorce). Divorce can be defined as having occurred when two previously paired individuals are alive during the next breeding season and at least one of them has re‐mated with a new partner. In socially monogamous birds divorce is widespread, but it is not clear whether it is a behavioural adaptation to improve the quality of a mating decision or whether, alternatively, it results as a non‐selected consequence of other processes: existing studies suggest a heterogeneous set of results with respect to this central question. This heterogeneity could result from a number of factors, ranging from the methodological approaches used, to population‐ or species‐specific characters. In this review we use phylogenetic meta‐analyses to assess the evidence that divorce is adaptive (in terms of breeding success) across 64 species of socially monogamous birds. Second, we explore biological and methodological reasons for the heterogeneity in the results of previous studies. Results of our analyses supported the hypothesis that divorce is, in general, an adaptive behavioural strategy as: (1) divorce is triggered by relatively low breeding success; (2) there is a positive change in breeding success as a result of divorce. More specifically, while controlling for methodological moderators, we show that: (i) earlier stages of breeding are better predictors of divorce than later stages (r = 0.231; 95% CI: 0.061–0.391 for clutch size; similar for laying date); (ii) females benefited from divorce more than males in terms of increasing breeding success between successive breeding attempts, with different stages of the breeding cycle improving at different rates (e.g. r = 0.637; 95% CI: 0.328–0.817 for brood‐level measures). We show that the effect size was dependent on the methodological approach used across studies and argue that research on the adaptive nature of divorce should be cautious when designing the study and interpreting the results. Altogether, by providing strong evidence that divorce is an adaptive strategy across monogamous birds, the results of our analysis provide a firm ground for further exploration of external covariates of divorce (e.g. demographic factors) and the mechanisms underlying the differences in the effect sizes of the proximal fitness causes and consequences of divorce.     

Malaria infection status predicts extra‐pair paternity in the blue tit

Extra‐pair matings comprise a common reproductive strategy among socially monogamous bird species. However, it remains unclear why females decide to mate with extra‐pair males. Indirect benefits in terms of improving offspring genetic quality are usually invoked to explain this phenomenon. Parasite resistance genes are often considered as a female target of seeking extra‐pair matings, but the direct test of this hypothesis is generally lacking. Here, we report on a relationship between the status of infection with malaria parasites (Plasmodium and Haemoproteus) and occurrence of extra‐pair paternity in a wild population of the blue tit Cyanistes caeruleus inhabiting Gotland (Sweden). We found that the probability of extra‐pair paternity is significantly related to the infection status of social parents. Infected males showed higher probability of being cuckolded than uninfected ones. However, this was observed only among males mated to uninfected females. Thus, avian malaria may potentially contribute to explanation of extra‐pair mating behaviour.     

Extra‐pair paternity in relation to breeding synchrony in ground tits: an individual‐based approach

Previous studies thought that at the within‐population level, whether a female bird engages in extra‐pair (EP) mating depends on how synchronous she is in breeding time with all other females around her, presumably the synchronization might affect the female's opportunities to meet potential EP sires who socially pair with these other females. However, when females or males are choosy about EP partners and mate with one EP individual only, the probability of EP mating may be most influenced by breeding synchrony between the EP partners. In such a case, the ‘individual‐level’ synchrony should act to determine EP mating success. We test this idea in a socially monogamous passerine, the ground tit Parus humilis. Fifty‐five out of 172 sampled females produced 122 EP offspring, each mating with one EP sire in most cases (92%), usually her intermediately‐related kin. As expected, the broader‐scale synchrony did not predict the probability of EP paternity but the individual‐level did, for females having EP offspring bred more synchronously with their EP than with their nearest neighbors, and females without EP offspring were least synchronous with their nearest neighbors. We argue that this kind of individual‐based approaches will shine light on the synchrony‐EP mating relationship in birds.     

Occurrence of extra‐pair paternity is connected to social male's MHC‐variability in the scarlet rosefinch Carpodacus erythrinus

Genes of the Major Histocompatibility Complex (MHC) represent an essential component of the vertebrate acquired immune system. In the last decades, the role of MHC genes in mate choice has been subject of particular scientific interest. However, results of studies dealing with this topic in different species are equivocal and mechanisms conducting MHC‐based mate choice are still puzzling. We investigated the impact of MHC class I variability on within‐pair and extra‐pair fertilisation success in a wild population of a socially monogamous passerine bird with considerable rates of extra‐pair paternity, the scarlet rosefinch Carpodacus erythrinus. We found some support for the ‘good‐genes‐as‐heterozygosity model’, as social males of high MHC‐heterozygosity were cheated by their females less frequently than less MHC‐heterozygous males. However, cuckolding males were not more MHC‐heterozygous than the cheated social males, nor were extra‐pair young more MHC‐heterozygous than within‐pair young. We did not find any evidence for mating preferences according to the complementarity model.     

Does competition for nests affect genetic monogamy in Cory's shearwater Calonectris diomedea?

Most bird species are socially monogamous. However, extra‐pair copulations (EPCs), resulting in extra‐pair paternity (EPP), commonly occur. EPCs should allow females to adjust social mate choice and allow males that fail to obtain a nest a chance to avoid missing a breeding season, especially when poor nest supply constrains social mate choice. Procellariiformes (albatrosses and petrels) are socially monogamous seabirds which seldom divorce, even when nest availability constrains social mate choice. In Cory's shearwater Calonectris diomedea, a burrow‐nesting petrel, two studies conducted in the Mediterranean, where competition for nests is weak, detected no EPP. EPP remains to be investigated at localities where competition for nests is much stronger, such as Vila islet, Azores archipelago, Atlantic Ocean. We conducted a genetic (microsatellites) study over two successive years on Vila, involving the breeding pairs of the same 65 nests each year and their single chick. EPPs occurred each year, the overall rate being 11.6%. Coupling genetic analyses to a 7‐year demographic survey provided additional data on pair bonds and competition for nests. Overall, cuckoldry was unrelated to divorce, nest density and inbreeding avoidance, but was more frequent when the social male was small. Nest changes were more costly for males than for females, and some apparently unpaired males attempted to dislodge social males during within‐pair copulations. These results are compatible with the existence of a link between poor nest availability and EPP and confirm that even species considered strongly monogamous can adopt flexible mating strategies.     

Variation in parent–offspring kinship in socially monogamous systems with extra‐pair reproduction and inbreeding

Female extra‐pair reproduction in socially monogamous systems is predicted to cause cuckolded socially‐paired males to conditionally reduce paternal care, causing selection against extra‐pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially‐paired female and/or to her extra‐pair mate, and therefore be related to extra‐pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra‐pair reproduction, might then be weakened. We derive metrics that quantify allele‐sharing between within‐pair and extra‐pair offspring and their mother and her socially‐paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra‐pair reproduction and inbreeding on a brood's total allelic value to its socially‐paired parents. Cuckolded male song sparrows were almost always detectably related to extra‐pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra‐pair reproduction, this decrease was reduced by within‐pair and extra‐pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra‐pair reproduction, parental care, and inbreeding.     

Lack of evidence for improved immune response of extra‐pair nestlings in collared flycatcher Ficedula albicollis

Extra‐pair paternity is common in many socially monogamous bird species. Increasing evidence suggests that extra‐pair copulations are female‐driven, but benefits for females mating outside social pair‐bonds are still poorly understood. The most influential explanation, “good genes” hypothesis, states that females mated socially with low quality males, engage in extra‐pair copulations to obtain genetic benefits for their progeny. According to this model, enhanced performance of extra‐pair offspring is expected. Here, based on 4‐year study of collared flycatcher Ficedula albicollis, we compared the condition of extra‐pair and within‐pair young. We found no difference in immune response and body size between maternal half‐siblings raised in the same nests. Additionally sex ratio was not biased among extra‐pair nestlings, and paternity was not associated with hatching rank. Our results failed to reveal “good genes” effects in the studied population. These effects might be hard to detect, but other hypotheses should also be studied more thoroughly in the future.     

Breeding Biology and Variable Mating System of a Population of Introduced Dunnocks (Prunella modularis) in New Zealand

Species with variable mating systems provide a unique opportunity to investigate whether females receive direct fitness benefits from additional male partners. The direct benefits provide an obvious explanation for why females would breed polyandrously, in a situation where males clearly do not attain their optimal reproductive success. Evidence for these direct benefits is, however, mixed. Here, we present a detailed study of the breeding biology of the dunnock, Prunella modularis, which inform an investigation into the effects of the social mating system on the reproductive success in a population of dunnocks in Southern New Zealand. We studied 80 different social groups over the course of three breeding seasons. Dunnocks in our population presented a variable mating system, with socially monogamous (45%), socially polyandrous (54%) and socially polygynandrous (1%) groups being observed in the same breeding season. We did not observe any polygynous social units in our study period although polygyny exists in the population. We found little difference in the numbers of eggs laid, and egg volume between monogamous and polyandrous nests. However, polyandrous groups had better hatching and fledging success than monogamous groups (composite d = 0.385, 95% CI: 0.307 to 0.463). Overall our results support the notion that polyandry is beneficial for females.     

Extra‐pair fertilizations contribute to selection on secondary male ornamentation in a socially monogamous passerine

Despite considerable research effort, it remains unclear whether extra‐pair fertilizations (EPF) drive the evolution of male secondary ornamentation in socially monogamous systems. In this study, we test the hypothesis that EPF contribute to the evolution or maintenance of male feather ornamentation in a sexually dichromatic passerine, the Scarlet Rosefinch, Carpodacus erythrinus. We show that the colouration of ornamental breast feathers is a good predictor of basic sources of variation in male annual reproductive output in rosefinches and that the annual realized reproductive success of males is positively associated with measures of ornamental colouration only when gains and losses because of EPF are considered. The results indicate that EPF in rosefinches may rely on absolute (good genes) rather than self referential (genetic complementarity) criteria of mate choice. Our study corroborates the potentially important role of EPF in the evolution and/or maintenance of elaborate male ornaments in socially monogamous taxa.