Extra-pair Mating Systems Research Articles

Do female bluethroats without extra-pair offspring have more MHC-compatible social mates?

Genes of the major histocompatibility complex (MHC) are crucial for adaptive immunity in jawed vertebrates, and theory predicts that there should be mate choice for optimizing MHC constitution in the offspring. In a previous study, we demonstrated a non-random female choice of extra-pair males in the bluethroat (Luscinia svecica), yielding offspring that was closer to an intermediate MHC class II (MHCII) allele count than their within-pair halfsiblings. The present study tests whether social pairs with only within-pair young (WPY) in their brood, in the same study population, had a combined MHC-constitution closer to a presumed intermediate optimum, than social pairs with extra-pair young (EPY), with a corresponding pattern in their offspring. As expected, we found that WPY from pure WPY-broods were more MHC-optimal than WPY from mixed broods, but only in broods of young (second year) males. Correspondingly, there was a tendency for social pairs with only WPY in their brood to be more MHC-compatible than social pairs with EPY in their brood, when the male was young. Older bluethroat males have considerably larger testes than young males, and their higher sperm competitiveness could help them secure paternity in their own brood, also when they are not MHC-compatible. In other words, in the sexual conflict over paternity, females may be more likely to realise their preference for a MHC-compatible mate when paired to a young male. As a possible fitness indicator, immune responsiveness to an injected antigen (PHA) was elevated for offspring closer to “the golden mean” in MHCII allele count.Significance statementThis study contributes to our understanding of MHC-based mate choice in extra-pair mating systems, by showing that female bluethroats (Luscinia svecica) with an MHCII-compatible social mate tend to have no extra-pair young in their brood, but only when the social male is young. This elucidates a possible sexual conflict, in which older social males are able to override female preferences and prevent other males from gaining paternity in their brood through higher sperm production. Studying systems in which extra-pair paternity occurs offers an insight into the genetic benefits of mate choice, as extra-pair males, in contrast to social males, generally contribute only sperm. Further, the strict and thorough genotyping scheme applied in this study enabled us to demonstrate a preference for “the golden mean” in MHC-diversity in a species with one of the highest MHC class II-diversity known to date.

The function of seasonal song in a tropical resident species, the Red-throated Ant-tanager (Habia fuscicauda)

Recent studies of tropical birds with year-round territoriality indicate that song rate is relatively low year-round in association with lower seasonality and relatively stable social environment over the year. We examined seasonal variation in the song rate of Red-throated Ant-tanagers (Habia fuscicauda), a socially monogamous species in which males predominantly sing during the breeding season, to determine to what extent increased song rate is driven by (1) increased territory defense, (2) pair coordination of nest initiation, and (3) competition for extra-pair mating opportunities. Song was infrequent during the non-breeding season, increased dramatically prior to nesting (17 % time spent singing), and increased even more so during nesting (32 % time spent singing). Male song output was inversely related to frequency of interactions between pairs at territorial borders; however, interactions may also serve in a mating context. Extra-pair matings were common, and 17 of 41 nestlings in ten of 19 broods were extra-pair young, suggesting that high male song output may be sexually selected via extra-pair mate choice. Although males spent much less time singing prior to nesting, our results also indicate that male initiation of singing was associated with female egg-laying date, indicating also a role in within-pair coordination of reproduction. Our results suggest that high song output during the breeding season may be more common in omnivorous species that experience increased seasonality and that it may be indicative of an extra-pair mating system. More studies of species with diverse life histories are needed to examine the ecological conditions that explain interspecific variation in song output.

Vocal Communication in Androgynous Territorial Defense by Migratory Birds

Many temperate zone breeding birds spend their non-breeding period in the tropics where they defend individual territories. Unlike tropical birds that use song for breeding and non-breeding territorial defense, vocal defense differs strikingly between breeding and non-breeding territories in migrants. Song, restricted to males, is used during defense of breeding territories but callnotes are used to defend non-breeding territories. To explain why callnotes and not songs predominate in the non-breeding context, we present an empirical model based upon predictions from motivational/structural rules, ranging theory and latitudinal differences in extra-pair mating systems. Due to sex role divergence during breeding that favors singing in males, but not females, females may be unable to range male song. Ranging requires a signal to be in both the sender and receiver’s repertoire to allow the distance between them to be assessed (ranged). Non-breeding territories of migrants are defended by both males and females as exclusive individual (androgynous) territories. Ranging Theory predicts callnotes, being shared by both males and females can, in turn, be ranged by both so are effective in androgynous territoriality. Where songs are used for non-breeding territorial defense both sexes sing, supporting the evolutionary significance of shared vocalizations in androgynous territorial defense.

Heterozygosity and fitness benefits of extrapair mate choice in White-rumped Swallows (Tachycineta leucorrhoa)

Female birds that engage in extrapair mating may choose extrapair mates that are genetically compatible, increasing their fitness through genetic benefits, such as increased heterozygosity, to their offspring; or choose mates that are heterozygous at one or more loci. Here, we describe the extrapair mating system, explore the fitness benefits of extrapair mating and test the heterozygosity hypothesis in White-rumped Swallows (Tachycineta leucorrhoa) breeding in Argentina using a panel of microsatellite loci. Extrapair offspring accounted for 56% of the nestlings and 77% of the broods in our population. Within broods, 1–4 males fathered extrapair offspring, and in 29% of nests, all offspring were from extrapair sires. We found that broods with extrapair offspring fledged overall more young than broods with no extrapair offspring but that the young that died were more heterozygous than the ones that fledged. Although extrapair offspring had a higher probability of surviving than within-pair offspring, these 2 groups did not differ in their level of heterozygosity. Neither the heterozygosity of the social mate nor the genetic similarity of the social pair predicted the presence of extrapair young. Instead, females chose social mates that were significantly less genetically similar to them. Our results do not support the heterozygosity hypothesis and contradict 2 of its main predictions.

Variation in the extra-pair mating systems of Acadian Flycatchers and Wood Thrushes in forest fragments in southern Ontario

The application of molecular tools to studies of avian mating systems has revealed that most songbird species engage in extra-pair matings. However, little is known about the possible effects of habitat fragmentation on extra-pair mating systems. During the breeding seasons of 2002 and 2003, we quantified the frequency of extra-pair matings in Acadian Flycatchers (Empidonax virescens) and Wood Thrushes (Hylocichla mustelina) nesting in forest fragments in southern Ontario. Acadian Flycatchers are at the limit of their northern range in southern Ontario and occurred at low densities (0.005-0.015 males/ha). Across forest fragments, 14% of young Acadian Flycatchers were the result of extra-pair fertilizations. In contrast, Wood Thrushes were common in forest fragments, with breeding densities ranging from 0.37 to 1 males/ha. Extra-pair mating was common among Wood Thrushes, with 40% of young the result of extra-pair matings. Compared to populations studied in less fragmented habitats in Pennsylvania, rates of extra-pair paternity in Ontario were lower for Acadian Flycatchers and higher for Wood Thrushes. Our results demonstrate that rates of extra-pair mating can vary across landscapes. However, the extra-pair mating systems of Acadian Flycatchers and Wood Thrushes appear to respond differently to fragmentation. We suggest that low breeding densities on fragments may be mediating the low rates of extra-pair mating observed in Acadian Flycatchers in southern Ontario, whereas changes to the behavioral tactics of male and female Wood Thrushes in southern Ontario may explain the high levels of extra-pair mating.

Radical loss of an extreme extra-pair mating system

BackgroundMating outside the pair-bond is surprisingly common in socially monogamous birds, but rates of extra-pair paternity (EPP) vary widely between species. Although differences in life-history and contemporary ecological factors may explain some interspecific variation, evolutionary forces driving extra-pair (EP) mating remain largely obscure. Also, since there is a large phylogenetic component to the frequency of EPP, evolutionary inertia may contribute substantially to observed EP mating patterns. However, the relative importance of plasticity and phylogenetic constraints on the incidence of EP mating remains largely unknown.ResultsWe here demonstrate very low levels of EPP (4.4% of offspring) in the purple-crowned fairy-wren Malurus coronatus, a member of the genus with the highest known levels of EPP in birds. In addition, we show absence of the suite of distinctive behavioral and morphological adaptations associated with EP mating that characterize other fairy-wrens. Phylogenetic parsimony implies that these characteristics were lost in one speciation event. Nonetheless, many life-history and breeding parameters that are hypothesized to drive interspecific variation in EPP are not different in the purple-crowned fairy-wren compared to its promiscuous congeners.ConclusionSuch radical loss of an extreme EP mating system with all associated adaptations from a lineage of biologically very similar species indicates that evolutionary inertia does not necessarily constrain interspecific variation in EPP. Moreover, if apparently minor interspecific differences regularly cause large differences in EPP, this may be one reason why the evolution of EP mating is still poorly understood.

Age‐related variation in primary sexual characters in a passerine with male age‐related fertilization success, the bluethroat Luscinia svecica

In passerine species with frequent extrapair mating, young (second calendar year) males often have a lower fertilization success than older (after second calendar year) males. This pattern might be explained by male‐ or female‐driven mechanisms, such as female preference for older males or higher competitive ability of older males. In this study we measured the size of the testes, the seminal glomera and the cloacal protuberance as well as the size and motility of the sperm, in individual bluethroats Luscinia svecica. In this species, nearly all extrapair fertilizations (EPFs) are obtained by older males. We found that the mass of the testes and the seminal glomera were highly positively correlated and that older males had significantly larger testes (38%), seminal glomera (15%) and cloacal protuberance (23%) than young males. In contrast, there was no difference between age groups in average sperm size or sperm motility. Our results are consistent with the idea that higher fertilization success by older males in this species is due to their higher rate of sperm production, allowing larger ejaculates and/or more frequent copulations. Unequal sperm production capacities by young and older males have important implications for the interpretation of paternity patterns in extrapair mating systems.

OFF-TERRITORY FORAYS AND GENETIC MATING SYSTEM OF THE WOOD THRUSH (HYLOCICHLA MUSTELINA)

Abstract Extrapair fertilizations (EPFs) are an important component of many socially monogamous mating systems. However, information about the reproductive tactics used by male and female birds in extrapair mating systems is still rare. We used radiotelemetry to measure territory use, forays, and mate association in Wood Thrush (Hylocichla mustelina) when females were fertile and not fertile. We also conducted paternity analysis to determine the frequency of EPFs in our study population. Socially paired male and female Wood Thrush maintained a close physical association while on their own territory. Most of the off-territory forays observed during the fertile stage were conducted by social pairs. Lone males rarely engaged in off-territory forays during their mate's fertile period but made relatively frequent off-territory forays when their mates were not fertile. Male Wood Thrush may trade-off investment into paternity assurance and extrapair tactics by favoring a mate-guarding tactic when their within-pa...

PATERNAL GENETIC EFFECTS ON OFFSPRING FITNESS ARE CONTEXT DEPENDENT: WITHIN THE EXTRAPAIR MATING SYSTEM OF A SOCIALLY: MONOGAMOUS PASSERINE

Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half-siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within-pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness-related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half-siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.

PATERNAL GENETIC EFFECTS ON OFFSPRING FITNESS ARE CONTEXT DEPENDENT WITHIN THE EXTRAPAIR MATING SYSTEM OF A SOCIALLY MONOGAMOUS PASSERINE

Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half-siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within-pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness-related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half-siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.

Patterns of extrapair mating in relation to male dominance status and female nest placement in black-capped chickadees

In sexually promiscuous animals, females may benefit by nesting close to the edge of their partner's territory to facilitate extrapair copulations. In the present study, we describe the extrapair mating system of black-capped chickadees, Poecile atricapillus, and test whether nest locations are influenced by conspecific attraction to extrapair partners. We conducted a spatial analysis of female mating strategies by using microsatellite paternity analysis in conjunction with geographic information system (GIS) analysis of nest and territory locations. Extrapair offspring comprised 52 of 351 offspring (14.8%) and were present in 19 of 57 broods (33.3%). Females paired to males with low dominance status in the previous winter's flock hierarchy were more likely to engage in a mixed reproductive strategy than were females paired to males with high dominance status. Females had extrapair copulations and extrapair fertilizations with high-ranking males more often than with low-ranking males. Not all extrapair copulations resulted in extrapair fertilizations. Females constructed their nests within 16.8 ± 1.0 m of the edge of their partner's territory, significantly closer to the edge of their nearest neighbor's territory than to the center of their own partner's territory. Extrapair males usually shared territory boundaries with cuckolded males. Females paired to low-ranking males constructed nests near the territory edges of neighboring high-ranking males. However, females did not have extrapair copulations with the neighbor nearest to their nest or even with the high-ranking neighbor nearest to their nest. We conclude that conspecific attraction to neighbors may influence nesting location in black-capped chickadees; however, it does not operate by facilitating extrapair copulations.

Extrapair paternity and offspring immunocompetence in the reed bunting, Emberiza schoeniclus

Female promiscuity is widespread in birds, as well as in other taxa. It is often assumed that in bird species with a socially monogamous mating system, females engage in extrapair copulations to obtain indirect (genetic) benefits. ‘Good genes’ and ‘compatible genes’ models predict that extrapair young (EPY) should be of higher quality than within-pair young (WPY), but the empirical evidence for this effect is limited. A recent study, however, indicated an enhanced cellular immunity in EPY in a passerine bird, the bluethroat, Luscinia svecica. To assess the generality of that finding, we replicated the study using the reed bunting, a passerine with an extrapair mating system similar to that of the bluethroat. Using the same immune assay protocol, we found no indication of enhanced cellular immunity in EPY compared with WPY. Female reed buntings thus do not seem to engage in extrapair copulations to achieve the same type of genetic benefit as in bluethroats. Furthermore, EPY in mixed-paternity broods did not grow faster and were not in better body condition close to fledging than WPY. We conclude that our results do not support the hypotheses assuming indirect benefits to female extrapair copulations. It appears that the adaptive value for females of pursuing extrapair fertilizations varies, even between species with similar extrapair mating systems.

Differential responses of yellow-breasted chats, Icteria virens, to male and female conspecific model presentations

A detailed understanding of the behavioural interactions between males and females is crucial for elucidating the selection pressures shaping mating system evolution; however, these interactions are often difficult to observe, particularly in free-living populations. We simulated extraterritorial intrusions by presenting conspecific models on to territories of a Neotropical migratory passerine, the yellow-breasted chat, Icteria virens. Simulated intrusions elicited different responses based on the sex of the focal individual and the sex and species of the model. Behavioural responses of the focal individuals were largely directed towards conspecific models, whereas simulated heterospecific intrusions, using a Carolina wren, Thryothorus ludovicianus, model, elicited minimal response. Male song was not related to any particular model presentation. Males directed mating behaviours, including courtship displays and copulations, exclusively towards the female conspecific model. Males behaved aggressively towards the conspecific male model. In contrast, females never showed any courtship behaviour towards the male model and showed significant aggression towards the conspecific female model. The results of this study reveal that territorial aggression in yellow-breasted chats is strongly intrasexual. Additionally, simulated female extraterritorial intrusions, but not male intrusions, resulted in extrapair courtship and copulation. This pattern is likely to be typical of many socially monogamous species and points to the behavioural mechanisms underlying both monogamy and extrapair mating systems.

Extrapair Mating System of an Asynchronously Breeding Tropical Songbird: The Mangrove Swallow

Variation in the extent of extrapair paternity among avian species could result from ecological differences in breeding synchrony and/or density, or the existence or absence of paternity guards. We studied the extrapair mating system and paternity-assurance behaviors of an asynchronously breeding tropical songbird, the Mangrove Swallow (Tachycineta albilinea), and compared this species with the synchronously breeding temperate zone Tree Swallow (Tachycineta bicolor). Mangrove Swallows had a moderate level of extrapair paternity (26% of broods, 15% of nestlings), low breeding synchrony (8% of females fertile simultaneously), and low breeding density (average nearest-neighbor distance 313 m). The spatial and temporal distribution of nests with and without extrapair young did not differ significantly. Males did not follow their mates closely during the female's fertile period, and within-pair copulation frequency was low (0.33 copulations/h). Mangrove Swallows had a significantly lower proportion of extrapair young compared with Tree Swallows. Differences in breeding synchrony may explain the difference in extrapair paternity between the two congeners.

Breeding synchrony best explains variation in extra-pair mating system among avian species

Stutchbury (1998) used new data and a comparative pairwise test to confirm that there is a strong correlation between breeding synchrony and extra-pair fertilization (EPF) frequency in passerines, as first reported by Stutchbury and Morton (1995). Although a pairwise test is a legitimate and powerful comparative method, Weatherhead and Yezerinac (1998) call for "better analyses to assess the correlation between synchrony and EPFs." There is a strong correlation between breeding synchrony and EPF frequency regardless of the comparative method used (Stutchbury and Morton 1995; Stutchbury 1998). Here I present a linear contrasts analysis on the 34 species given in Stutchbury (1998) using the phylogeny shown in Westneat and Sherman (1997) with other species added using the phylogeny in Sibley and Ahlquist (1990). I used version 2.0 of the Comparative Analysis by Independent Contrasts (CAIC) program (Purvis and Rambaut 1995), and assumed equal branch lengths. As expected, there was a strong positive correlation between contrasts in arcsinetransformed EPF frequency (proportion of broods with EPFs) and the synchrony index (r = 0.52, n = 33 contrasts, P < 0.002). The results for breeding density were similar to Westneat and Sherman (1997), with no correlation between contrasts of arcsine-transformed EPF frequency and nearest-neighbor distance (r -0.10, n 28 contrasts, P = 0.60). The relationship between breeding synchrony and EPFs across species demands explanation; either synchrony causally affects the evolution of extra-pair mating systems as argued by Stutchbury and Morton (1995), or both synchrony and EPF frequency are correlated with some unidentified causal factor. Weatherhead and Yezerinac (1998) favor the explanation that "both breeding synchrony and extra-pair mating [are] corre-

Extra-Pair Mating System of a Synchronously Breeding Tropical Songbird

Extra-pair matings are now recognized as a fundamental component of avian mating systems. However, in tropical regions where breeding is typically asynchronous socially monogamous species appear to have low sperm competition and few extrapair matings. We predicted that if breeding synchrony promotes the evolution of extra-pair matings, then tropical species that breed synchronously, like the Claycolored Robin Turdus grayi, should have abundant extra-pair young (EPY). Breeding began relatively abruptly during the dry season (Feb-Mar) in this non-migratory species, with a mean of 25% of females fertile on a given day. Overall, 53% of females produced EPY, and 38% of nestlings were EPY. Males have a long and conspicuous dawn chorus, which could be a result of intense male-male competition for extra-pair matings. Male songs are individually recognizable and males vary greatly in song output. Male song output declined significantly from the pre-nesting stage through the incubation stage, as would be expected if song is important in mate choice. Our results support the idea that breeding synchrony favors extra-pair matings, however further studies of tropical songbirds are needed to fully explore how ecology is tied to extra-pair mating systems.

The Effect of Breeding Synchrony On Extra-Pair Mating Systems in Songbirds

Extra-pair mating systems are now considered to be typical of songbirds because DNA fingerprinting has revealed high rates of extra-pair fertilizations (EPFs) in so many species previously thought to be monogamous. However, there is no general framework to explain the tremendous variability among songbirds in EPF rate. Here, in a comparison of EPF rates and temporal patterns of nesting among songbirds, we show that EPFs are most common in species where females breed synchronously. We argue that for both males and females, a temporal concentration of female fertility (breeding synchrony) increases the net benefits of seeking EPFs. One implication of this finding is that tropical songbirds, most of which breed asynchronously, are predicted to have low levels of extra-pair matings. Testes size is positively correlated with frequency of EPFs, and as predicted, tropical songbirds had small testes size relative to temperate zone species. The few DNA fingerprinting studies that exist for socially monogamous tropical songbirds support the correlation between breeding synchrony and EPFs. We believe that breeding synchrony is the most important factor promoting the evolution of extra-pair mating systems.

Helpers liberate female fairy-wrens from constraints on extra-pair mate choice

In cooperatively breeding superb fairy-wrens (Malurus cyaneus), all males contribute to the feeding and defence of young. Despite the expectation that such paternal care should be directed only to relatives, DNA fingerprinting revealed that most offspring (76%, 138 out of 181) were sired by extra-group males that contributed no care, and that almost all broods (95%, 38 out of 40) contained young sired by extra-group fathers. This is the highest known incidence of cuckoldry. This remarkable mating system is produced by female control of fertilization and consistent preference for certain extra-group male genotypes. This choice leads to the production of sons that also gain extra-group fertilizations. One constraint on the extra-pair mate choice of females is the level of parental assistance received from males. Males living in pairs contribute relatively more parental care and are more likely to gain paternity in one of their broods (85%, 11 out of 13) than dominant males in multi-male cooperative groups (30%, 8 out of 27). In groups helpers compensate for the lower parental assistance of dominant males, so the total feeding rate is similar between pairs and groups. This suggests that females allow males in pairs more paternity to ensure their assistance with parental care. Helpers provide an alternative source of paternal investment, and allow females to express unrestricted mate choice. Mating options for females in other species with female control of fertilization may also reflect a trade-off between acquiring the genes of high-quality males for their offspring and parental care of those offspring.