No evidence of immediate fitness benefits of within-season divorce in monogamous birds

Individuals of socially monogamous species can correct for suboptimal partnerships via two secondary mating strategies: divorce and extra-pair mating, with the former potentially providing both genetic and social benefits. Divorcing between breeding seasons has been shown to be generally adaptive behaviour across monogamous birds. Interestingly, some pairs also divorce during the breeding season, when constraints on finding a new partner are stronger. Despite being important for a comprehensive understanding of the evolution of social monogamy, whether within-season divorce is adaptive and how it relates to extra-pair mating remains unknown. Here, we meta-analysed 90 effect sizes on within-season divorce and breeding success, extracted from 31 studies on 24 species. We found no evidence that within-season divorce is adaptive for breeding success. However, the large heterogeneity of effect sizes and strong phylogenetic signal suggest social and environmental factors—which have rarely been considered in empirical studies—may play an important role in explaining variation among populations and species. Furthermore, we found no evidence that within-season divorce and extra-pair mating are complementary strategies. We discuss our findings within the current evidence of the adaptiveness of secondary mating strategies and their interplay that ultimately shapes the evolution of social monogamy.     

Mate fidelity in a polygamous shorebird,the snowy plover (Charadrius nivosus)

Social monogamy has evolved multiple times and is particularly common in birds. However, it is not well understood why some species live in long‐lasting monogamous partnerships while others change mates between breeding attempts. Here, we investigate mate fidelity in a sequential polygamous shorebird, the snowy plover (Charadrius nivosus), a species in which both males and females may have several breeding attempts within a breeding season with the same or different mates. Using 6 years of data from a well‐monitored population in Bahía de Ceuta, Mexico, we investigated predictors and fitness implications of mate fidelity both within and between years. We show that in order to maximize reproductive success within a season, individuals divorce after successful nesting and re‐mate with the same partner after nest failure. Therefore, divorced plovers, counterintuitively, achieve higher reproductive success than individuals that retain their mate. We also show that different mating decisions between sexes predict different breeding dispersal patterns. Taken together, our findings imply that divorce is an adaptive strategy to improve reproductive success in a stochastic environment. Understanding mate fidelity is important for the evolution of monogamy and polygamy, and these mating behaviors have implications for reproductive success and population productivity.     

Functional infertility in a wild passerine bird

Information about male infertility in free‐living bird populations and its underlying causes are poorly documented in the literature. Here, we assessed sperm quality and infertility among males in a wild population of Blue Tits Cyanistes caeruleus, a socially monogamous passerine with frequent extra‐pair mating. One of 30 males (3.3%) studied across two breeding seasons had morphologically abnormal and nearly immotile spermatozoa in combination with zero annual fertilization success. Demonstration of male functional infertility suggests the possibility that socially monogamous females of the study population could obtain a direct fitness benefit by mating polyandrously to increase fertilization success, which could contribute to selection on extra‐pair mating behaviour.     

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.     

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.     

Survival costs of within‐ and between‐season mate change in the European blackbird Turdus merula

Many studies of socially monogamous birds discuss the adaptive role of between‐season partner change, but only a handful of them refer to the benefits of pair fidelity in terms of increased survival. Moreover, there are no studies describing the benefits of within‐season mate retention. Our data relating to an urban population of European blackbirds Turdus merula enabled us to test the dependence of survival on pair faithfulness. Because blackbirds divorce within and between seasons, we were able to test the influence of pair faithfulness on their within‐ and between‐season survival and mate fidelity. For this purpose, we used a multievent capture–mark–recapture (MECMR) statistical model, which is based on recapture rates and different pair states (faithful to mate, paired with new partner, or dead). Our study indicated that between‐ and within‐season survival depends on pair states: pair‐bond duration increases survival to the next capture occasion in both sexes. We found that the pair‐bond duration to the current partner increased the chances of being with the same partner during the next breeding occasion, although we failed to find any within‐season pair‐bond influence for females. Our results showed sex differences in mating at the end of the season: females had a much smaller chance of breeding with the current new partner in the next year. This study has demonstrated that within‐ and between‐season survival is dependent on mate retention, and we discuss this in the context of how searching for a new partner could affect the birds’ survival.     

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.     

Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Rates of extra‐pair paternity (EPP) have frequently been associated with genetic relatedness between social mates in socially monogamous birds. However, evidence is limited in mammals. Here, we investigate whether dominant females use divorce or extra‐pair paternity as a strategy to avoid the negative effects of inbreeding when paired with a related male in meerkats Suricata suricatta, a species where inbreeding depression is evident for several traits. We show that dominant breeding pairs seldom divorce, but that rates of EPP are associated with genetic similarity between mates. Although extra‐pair males are no more distantly related to the female than social males, they are more heterozygous. Nevertheless, extra‐pair pups are not more heterozygous than within‐pair pups. Whether females benefit from EPP in terms of increased fitness of the offspring, such as enhanced survival or growth, requires further investigations.     

Assessing the reproductive consequences of mate retention and pair bond duration in Thorn-tailed Rayadito (Aphrastura spinicauda), a short-lived,socially monogamous neotropical bird

The adaptive value of mate retention has been studied in several socially monogamous birds but evidence of reproductive benefits for short-lived species is inconclusive. Most studies come from northern latitudes but more research on tropical birds is needed, as these species typically show higher survival rates and longer pair bonds than those from temperate regions. We gathered data on the reproductive biology of a subtropical, isolated population of Thorn-tailed Rayadito Aphrastura spinicaudaduring 2008–2017 to evaluate the reproductive consequences of mate retention. We examined data from 243 breeding attempts made by 159 breeding pairs. We found that ~30% of all breeding pairs bred together during at least two consecutive years, and some were mated for 6 years. The main cause of pair dissolution was mate loss, not divorce. Mixed-effects models provided moderate evidence for positive effects of mate retention and successive remating on reproductive success. Newly formed pairs laid eggs later and had slightly smaller clutches than remated pairs. Furthermore, clutch size seemed to increase with successive remating. Overall, our results suggest that newly formed pairs are less efficient in reproduction and that minor yearly reproductive benefits of mate retention might accumulate for birds that are able to breed with the same partner over many years. Because breeding habitat is limited in our study population, Thorn-tailed Rayaditos could benefit from remating if the number of individuals that can breed exceeds the number of available breeding positions. Profitable long-term pair bonds might be more frequent in tropical birds and therefore more studies are needed to assess the prevalence of remating-mediated effects on reproduction in relatively short-lived monogamous species breeding in tropical regions.     

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.     

Mate and territory availability affect breeding dispersal and divorce in a resident Southern House Wren Troglodytes aedon musculus population

Breeding dispersal is the movement of an individual between breeding attempts and is usually associated with the disruption of the social pair bond, although mates may disperse together as a social unit. In monogamous territorial species, the decision to disperse may be affected by individual attributes such as sex, age and condition of the disperser. However, environmental and social contexts may also play a crucial role in the decision to disperse. We analysed capture‐resighting data collected over 9 years to study breeding dispersal and divorce rates of a Southern House Wren Troglodytes aedon musculus population in South Temperate Argentina. Between‐season dispersal was more frequent than within‐season dispersal, with females dispersing more often than males, both between and within seasons. Both within‐season and between‐season breeding dispersal probability was affected by territory availability, but not by previous breeding success. When the adult sex ratio (ASR) was more skewed towards males, male between‐season dispersal was also affected by mating status, with widowed and single males dispersing more often than paired males. Within‐season divorce increased the reproductive success of females but not males, and was affected by the availability of social partners (with increasingly male‐skewed ASR). Our results suggest that territorial vacancies and mating opportunities affect dispersal and divorce rates in resident Southern House Wrens, highlighting the importance of social and environmental contexts for dispersal behaviour and the stability of social pair bonds.     

Increased hatching success as a direct benefit of polyandry in birds

Multiple mating by females is difficult to explain in primarily socially monogamous taxa such as birds because mating outside the pair bond often provides no obvious benefit to females. Although indirect selection is often invoked to explain the evolution of polyandry, current evidence suggests that selection on indirect benefits of mating is weak. Here, I consider a direct benefit of remating in birds: increased fertilization success. I test whether increased hatching success of a female's eggs is related to rates of extra-pair paternity (EPP), a proxy of polyandry, across 113 bird species. I use two statistical approaches, control for phylogenetic uncertainty, and assess the fit of competing evolutionary models. Results show there is indeed a positive relationship between rates of EPP and hatching success in birds. I propose that by mating with many males, females may increase their fertility. I end by discussing the biological rationale for this explanation, alternative interpretations of the results, and how this study furthers our understanding of polyandry and mating system evolution.     

Parental care and social mating system in the Lesser Spotted Woodpecker Dendrocopos minor

The sexes’ share in parental care and the social mating system in a marked population of the single‐brooded Lesser Spotted Woodpecker Dendrocopos minor were studied in 17 woodpecker territories in southern Sweden during 10 years. The birds showed a very strong mate fidelity between years; the divorce rate was 3.4%. In monogamous pairs, the male provided more parental care than the female. The male did most of the nest building and all incubation and brooding at night. Daytime incubation and brooding were shared equally by the sexes, and biparental care at these early breeding stages is probably necessary for successful breeding. In 42% of the nests, however, though still alive the female deserted the brood the last week of the nestling period, whereas the male invariably fed until fledging and fully compensated for the absent female. Post‐fledging care could not be quantified, but was likely shared by both parents. Females who ceased feeding at the late nestling stage resumed care after fledging. We argue that the high premium on breeding with the same mate for consecutive years and the overall lower survival of females have shaped this male‐biased organisation of parental care. In the six years with best data, most social matings were monogamous, but 8.5% of the females (N=59) exhibited simultaneous multi‐nest (classical) polyandry and 2.9% of the males (N=68) exhibited multi‐nest polygyny. Polyandrous females raised 39% more young than monogamous pairs. These females invested equal amounts of parental care at all their nests, but their investment at each nest was lower than that of monogamous females. The polyandrously mated males fully compensated for this lower female investment. Polygynous males invested mainly in their primary nest and appeared to be less successful than polyandrous females. Polyandry and polygyny occurred only when the population sex ratio was biased, and due to strong intra‐sexual competition this is likely a prerequisite for polygamous mating in Lesser Spotted Woodpeckers.     

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.     

Pair bond and breeding success in Blue Tits Parus caeruleus and Great Tits Parus major

Data from 939 nests of the Blue Tit Parus caeruleus and 1008 nests of the Great Tit P. major from nestboxes provided in superabundance in mixed forest study sites between 1976 and 2001 were analysed to examine the effects of mate retention on breeding success and the relationship between mate fidelity and site fidelity. Most birds retained their former partner (76% in Great Tits and 65% in Blue Tits). The probability of a pair divorcing was affected by male age in Great Tits, divorce being more likely in pairs with first‐year males. Great Tit pairs breeding together for a second season bred earlier, but had no higher breeding success than pairs breeding together for the first time. In Blue Tits laying date and start of incubation tended to be earlier in pairs breeding together for a second season, but hatching and fledging dates were not earlier than in other pairs. Great Tit pairs breeding together for two consecutive seasons bred earlier in the second season than in the first, but breeding success did not differ significantly between years. In both species, breeding performance did not differ between pairs that divorced after a season and pairs that stayed together. Thus breeding success did not determine whether a pair divorced or bred together again. Neither Blue Tits nor Great Tits improved their breeding performance through divorce. Blue Tit females even had fewer fledglings in the year after divorce than in the year before. Mate retention affected breeding site fidelity. Blue Tit females had greater breeding dispersal distances between consecutive years when re‐mating than when breeding again with the same mate. In Great Tits both males and females dispersed more when re‐mating than when retaining the former partner, suggesting that mate retention increased the chance of retaining the breeding site. In both species, breeding dispersal distances did not differ between pairs that divorced and pairs in which one mate disappeared. Because no major advantage of mate retention was evident, we suggest that mate retention evolved under different conditions than those found in study sites with high breeding densities and a superabundance of artificial nesting sites.     

Correlates of complete brood failure in blue tits: could extra‐pair mating provide unexplored benefits to females?

Behavioural ecologists have for decades investigated the adaptive value of extra‐pair copulation (EPC) for females of socially monogamous species. Despite extensive effort testing for genetic benefits, there now seems to be a consensus that the so‐called ‘good genes’ effects are at most weak. In parallel the search for direct benefits has mostly focused on the period surrounding egg laying, thus neglecting potential correlates of EPC that might be expressed at later stages in the breeding cycle. Here we used Bayesian methods to analyse data collected over four years in a population of blue tits Cyanistes caeruleus, where no support was previously found for ‘good genes’ effects. We found that broods with mixed paternity experienced less brood failure at the nestling stage than broods with single paternity, and that females having experienced complete brood failure in their previous breeding attempt had higher rates of mixed paternity than either yearling or previously successful females. To better understand these observations we also explored relationships between extra‐pair mating, male and female phenotype, and local breeding density. We found that in almost all cases the sires of extra‐pair offspring were close neighbours, and that within those close neighbourhoods extra‐pair sires were older than other males not siring extra‐pair offspring. Also, females did not display consistent EPC status across years. Taken together our results suggest that multiple mating might be a flexible female behaviour influenced by previous breeding experience, and motivate further experimental tests of causal links between extra‐pair copulation and predation.     

Divorce in the barn owl: securing a compatible or better mate entails the cost of re‐pairing with a less ornamented female mate

Two nonmutually exclusive hypotheses can explain why divorce is an adaptive strategy to improve reproductive success. Under the ‘better option hypothesis’, only one of the two partners initiates divorce to secure a higher‐quality partner and increases reproductive success after divorce. Under the ‘incompatibility hypothesis’, partners are incompatible and hence they may both increase reproductive success after divorce. In a long‐term study of the barn owl (Tyto alba), we address the question of whether one or the two partners derive fitness benefits by divorcing. Our results support the hypothesis that divorce is adaptive: after a poor reproductive season, at least one of the two divorcees increase breeding success up to the level of faithful pairs. By breeding more often together, faithful pairs improve coordination and thereby gain in their efficiency to produce successful fledglings. Males would divorce to obtain a compatible mate rather than a mate of higher quality: a heritable melanin‐based signal of female quality did not predict divorce (indicating that female absolute quality may not be the cause of divorce), but the new mate of divorced males was less melanic than their previous mate. This suggests that, at least for males, a cost of divorce may be to secure a lower‐quality but compatible mate. The better option hypothesis could not be formally rejected, as only one of the two divorcing partners commonly succeeded in obtaining a higher reproductive success after divorce. In conclusion, incompatible partners divorce to restore reproductive success, and by breeding more often together, faithful partners improve coordination.     

Serial monogamy in the European long-snouted seahorse Hippocampus guttulatus

Seahorses (Hippocampus spp.) are non-sex-role-reversed members of the Syngnathidae family that provide extensive brood care. Previous studies of seahorses have revealed monogamy within a single brood, but their longer term mating system had not been comprehensively evaluated. The parental contribution to 29 wild-born broods of Hippocampus guttulatus, sampled from six Portuguese populations with differing seahorse densities and sex ratios, was assessed using microsatellite DNA markers. To assess the longer term genetic mating system of this species parentage was determined in eleven broods sampled from a captive population over two breeding seasons. Genetic data suggest that this socially polygamous seahorse is serially monogamous across breeding seasons, i.e. monogamous within a season but may switch mates between seasons, and that differing population densities and sex ratios do not affect the mating system.     

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.     

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.