Nestling Begging Calls Resemble Maternal Vocal Signatures When Mothers Call Slowly to Embryos.

AbstractVocal production learning (the capacity to learn to produce vocalizations) is a multidimensional trait that involves different learning mechanisms during different temporal and socioecological contexts. Key outstanding questions are whether vocal production learning begins during the embryonic stage and whether mothers play an active role in this through pupil-directed vocalization behaviors. We examined variation in vocal copy similarity (an indicator of learning) in eight species from the songbird family Maluridae, using comparative and experimental approaches. We found that (1) incubating females from all species vocalized inside the nest and produced call types including a signature "B element" that was structurally similar to their nestlings' begging call; (2) in a prenatal playback experiment using superb fairy wrens (Malurus cyaneus), embryos showed a stronger heart rate response to playbacks of the B element than to another call element (A); and (3) mothers that produced slower calls had offspring with greater similarity between their begging call and the mother's B element vocalization. We conclude that malurid mothers display behaviors concordant with pupil-directed vocalizations and may actively influence their offspring's early life through sound learning shaped by maternal call tempo.

The effect of climate change on avian offspring production: A global meta-analysis.

Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.

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.

Sperm Numbers as a Paternity Guard in a Wild Bird.

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male's ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success.

Prenatal auditory learning in avian vocal learners and non-learners.

Understanding when learning begins is critical for identifying the factors that shape both the developmental course and the function of information acquisition. Until recently, sufficient development of the neural substrates for any sort of vocal learning to begin in songbirds was thought to be reached well after hatching. New research shows that embryonic gene activation and the outcome of vocal learning can be modulated by sound exposure in ovo. We tested whether avian embryos across lineages differ in their auditory response strength and sound learning in ovo, which we studied in vocal learning (Maluridae, Geospizidae) and vocal non-learning (Phasianidae, Spheniscidae) taxa. While measuring heart rate in ovo, we exposed embryos to (i) conspecific or heterospecific vocalizations, to determine their response strength, and (ii) conspecific vocalizations repeatedly, to quantify cardiac habituation, a form of non-associative learning. Response strength towards conspecific vocalizations was greater in two species with vocal production learning compared to two species without. Response patterns consistent with non-associative auditory learning occurred in all species. Our results demonstrate a capacity to perceive and learn to recognize sounds in ovo, as evidenced by habituation, even in species that were previously assumed to have little, if any, vocal production learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Cross-lags and the unbiased estimation of life-history and demographic parameters.

Biological processes exhibit complex temporal dependencies due to the sequential nature of allocation decisions in organisms' life cycles, feedback loops and two-way causality. Consequently, longitudinal data often contain cross-lags: the predictor variable depends on the response variable of the previous time step. Although statisticians have warned that regression models that ignore such covariate endogeneity in time series are likely to be inappropriate, this has received relatively little attention in biology. Furthermore, the resulting degree of estimation bias remains largely unexplored. We use a graphical model and numerical simulations to understand why and how regression models that ignore cross-lags can be biased, and how this bias depends on the length and number of time series. Ecological and evolutionary examples are provided to illustrate that cross-lags may be more common than is typically appreciated and that they occur in functionally different ways. We show that routinely used regression models that ignore cross-lags are asymptotically unbiased. However, this offers little relief, as for most realistically feasible lengths of time-series conventional methods are biased. Furthermore, collecting time series on multiple subjects-such as populations, groups or individuals-does not help to overcome this bias when the analysis focusses on within-subject patterns (often the pattern of interest). Simulations, a literature search and a real-world empirical example together suggest that approaches that ignore cross-lags are likely biased in the direction opposite to the sign of the cross-lag (e.g. towards detecting density dependence of vital rates and against detecting life-history trade-offs and benefits of group living). Next, we show that multivariate (e.g. structural equation) models can dynamically account for cross-lags, and simultaneously address additional bias induced by measurement error, but only if the analysis considers multiple time series. We provide guidance on how to identify a cross-lag and subsequently specify it in a multivariate model, which can be far from trivial. Our tutorials with data and R code of the worked examples provide step-by-step instructions on how to perform such analyses. Our study offers insights into situations in which cross-lags can bias analysis of ecological and evolutionary time series and suggests that adopting dynamical models can be important, as this directly affects our understanding of population regulation, the evolution of life histories and cooperation, and possibly many other topics. Determining how strong estimation bias due to ignoring covariate endogeneity has been in the ecological literature requires further study, also because it may interact with other sources of bias.

hiphop: Improved paternity assignment among close relatives using a simple exclusion method for biallelic markers.

Assignment of parentage with molecular markers is most difficult when the true parents have close relatives in the adult population. Here, we present an efficient solution to that problem by extending simple exclusion approaches to parentage analysis with single nucleotide polymorphic markers (SNPs). We augmented the previously published homozygote opposite test (hot), which counts mismatches due to the offspring and candidate parent having different homozygous genotypes, with an additional test. In this case, parents homozygous for the same SNP are incompatible with heterozygous offspring (i.e., "Homozygous Identical Parents, Heterozygous Offspring are Precluded": hiphop). We tested this approach in a cooperatively breeding bird, the superb fairy-wren, Malurus cyaneus, where rates of extra-pair paternity are exceptionally high, and where paternity assignment is challenging because breeding males typically have first-order adult relatives in their neighbourhood. Combining the tests and conditioning on the maternal genotype with a set of 1376 autosomal SNPs always allowed us to distinguish a single most likely sire from his relatives, and also to identify cases where the true sire must have been unsampled. In contrast, if just the hot test was used, we failed to identify a single most-likely sire in 2.5% of cases. Resampling enabled us to create guidelines for the number of SNPs required when first-order relatives coexist in the mating pool. Our method, implemented in the R package hiphop, therefore provides unambiguous parentage assignments even in systems with complex social organisation. We also identified a suite of Z- and W-linked SNPs that always identified sex correctly.

Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy-wrens.

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male-female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year-round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine-fairy-wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life-history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male-female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure.

Fluctuating optimum and temporally variable selection on breeding date in birds and mammals.

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.

Experimental vacancies do not induce settlement despite habitat saturation in a cooperative breeder.

The paradox of cooperative breeding, whereby individuals assist others instead of reproducing independently, is generally explained through ecological constraints, but experimental evidence is scant. Here we performed the crucial test of the role of habitat saturation through the experimental creation of vacancies and found that, despite abundant presence of potential mates, subordinates are reluctant to disperse into suitable vacant habitat where conspecifics are absent. We argue that sudden disappearance of multiple group members might indicate a heightened risk of predation. Thereby the results of this study are consistent with the 'perceptual trap' hypothesis: the avoidance of habitats because cues do not accurately reflect their quality. Interestingly, this hypothesis can also explain previous findings, which were widely interpreted as evidence for ecological constraints as a driver of cooperative breeding. Our results can have considerable implications for conservation as they mean that opportunities for colonization might go unexploited.

Integrating Fitness Components Reveals That Survival Costs Outweigh Other Benefits and Costs of Group Living in Two Closely Related Species.

Group living can be beneficial when individuals reproduce or survive better in the presence of others, but, simultaneously, there might be costs due to competition for resources. Positive and negative effects on various fitness components might thus counteract each other, so integration is essential to determine their overall effect. Here, we investigated how an integrated fitness measure (reproductive values [RVs]) based on six fitness components varied with group size among group members in cooperatively breeding red-winged and superb fairy wrens (Malurus elegans and Malurus cyaneus, respectively). Despite life-history differences between the species, patterns of RVs were similar, suggesting that the same behavioral mechanisms are important. Group living reduced RVs for dominant males, but for other group members, this was true only in large groups. Decomposition analyses showed that our integrated fitness proxy was most strongly affected by group size effects on survival and was amplified through carryover effects between years. Our study shows that integrative consideration of fitness components and subsequent decomposition analysis provide much needed insights into the key behavioral mechanisms shaping the costs and benefits of group living. Such attribution is crucial if we are to synthesize the relative importance of the myriad group size costs and benefits currently reported in the literature.

Extra-pair paternity in birds.

Since the first molecular study providing evidence for mating outside the pair bond in birds over 30 years ago, >500 studies have reported rates of extra-pair paternity (EPP) in >300 bird species. Here, we give a detailed overview of the current literature reporting EPP in birds and highlight the sampling biases and patterns in the data set with respect to taxonomy, avian phylogeny and global regions, knowledge of which will be crucial for correct interpretation of results in future comparative studies. Subsequently, we use this comprehensive dataset to simultaneously test the role of several ecological and life history variables. We do not find clear evidence that variation in EPP across socially monogamous species can be explained by latitude, density (coloniality), migration, generation length, genetic structuring (dispersal distance), or climatic variability, after accounting for phylogeny. These results contrast previous studies, most likely due to the large heterogeneity within species in both EPP and the predictor of interest, indicating that using species averages might be unreliable. Despite the absence of broadscale ecological drivers in explaining interspecific variation in EPP, we suggest that certain behaviours and ecological variables might facilitate or constrain EPP, as indicated by our finding that EPP was negatively associated with latitude within noncolonial species, suggesting a role of breeding synchrony. Thus, rather than focussing on general explanations for variation in EPP across all species, a future focus should be on how various aspects of ecology or life history might have driven variation in EPP among groups of species or populations of the same species. Hence, we argue that variation in EPP can be partly explained when taking the right perspective. This comprehensive overview, and particularly the dataset provided herein will create a foundation for further studies.

Conspicuous Plumage Does Not Increase Predation Risk: A Continent-Wide Test Using Model Songbirds.

The forces shaping female plumage color have long been debated but remain unresolved. Females may benefit from conspicuous colors but are also expected to suffer costs. Predation is one potential cost, but few studies have explicitly investigated the relationship between predation risk and coloration. The fairy-wrens show pronounced variation in female coloration and reside in a wide variety of habitats across Australasia. Species with more conspicuous females are found in denser habitats, suggesting that conspicuousness in open habitat increases vulnerability to predators. To test this, we measured attack rates on 3-D-printed models mimicking conspicuously colored males and females and dull females in eight different fairy-wren habitats across Australia. Attack rates were higher in open habitats and at higher latitudes. Contrary to our predictions, dull female models were attacked at similar rates to the conspicuous models. Further, the probability of attack in open habitats increased more for both types of female models than for the conspicuous male model. Across models, the degree of contrast (chromatic and achromatic) to environmental backgrounds was unrelated to predation rate. These findings do not support the long-standing hypothesis that conspicuous plumage, in isolation, is costly due to increased attraction of predators. Our results indicate that conspicuousness interacts with other factors in driving the evolution of plumage coloration.

Indirect fitness benefits through extra-pair mating are large for an inbred minority, but cannot explain widespread infidelity among red-winged fairy-wrens.

Extra-pair paternity (EPP) has been suggested to improve the genetic quality of offspring, but evidence has been equivocal. Benefits of EPP may be only available to specific individuals or under certain conditions. Red-winged fairy-wrens have extremely high levels of EPP, suggesting fitness benefits might be large and available to most individuals. Furthermore, extreme philopatry commonly leads to incestuous social pairings, so inbreeding avoidance may be an important selection pressure. Here, we quantified the fitness benefits of EPP under varying conditions and across life-stages. Extra-pair offspring (EPO) did not appear to have higher fitness than within-pair offspring (WPO), neither in poor years nor in the absence of helpers-at-the-nest. However, EPP was beneficial for closely related social pairs, because inbred WPO suffered an overall 75% reduction in fitness. Inbreeding depression was nonlinear and reduced nestling body condition, first year survival and reproductive success. Our comprehensive study indicates that EPP should be favored for the 17% of females paired incestuously, but cannot explain the widespread infidelity in this species. Furthermore, our finding that fitness benefits of EPP only become apparent for a small part of the population could potentially explain the apparent absence of fitness differences in population wide comparisons of EPO and WPO.

Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family.

Extra-pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.

Effects of extreme weather on two sympatric Australian passerine bird species.

Despite abundant evidence that natural populations are responding to climate change, there are few demonstrations of how extreme climatic events (ECEs) affect fitness. Climate warming increases adverse effects of exposure to high temperatures, but also reduces exposure to cold ECEs. Here, we investigate variation in survival associated with severity of summer and winter conditions, and whether survival is better predicted by ECEs than mean temperatures using data from two coexisting bird species monitored over 37 years in southwestern Australia, red-winged fairy-wrens, Malurus elegans and white-browed scrubwrens, Sericornis frontalis Changes in survival were associated with temperature extremes more strongly than average temperatures. In scrubwrens, winter ECEs were associated with survival within the same season. In both species, survival was associated with body size, and there was evidence that size-dependent mortality was mediated by carry-over effects of climate in the previous season. For fairy-wrens, mean body size declined over time but this could not be explained by size-dependent mortality as the effects of body size on survival were consistently positive. Our study demonstrates how ECEs can have individual-level effects on survival that are not reflected in long-term morphological change, and the same climatic conditions can affect similar-sized, coexisting species in different ways.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'.

Social pairing of Seychelles warblers under reduced constraints: MHC, neutral heterozygosity, and age.

The prevalence and significance of precopulatory mate choice remains keenly debated. The major histocompatibility complex (MHC) plays a key role in vertebrate adaptive immunity, and variation at the MHC influences individual survival. Although MHC-dependent mate choice has been documented in certain species, many other studies find no such pattern. This may be, at least in part, because in natural systems constraints may reduce the choices available to individuals and prevent full expression of underlying preferences. We used translocations to previously unoccupied islands to experimentally reduce constraints on female social mate choice in the Seychelles warbler (Acrocephalus sechellensis), a species in which patterns of MHC-dependent extrapair paternity (EPP), but not social mate choice, have been observed. We find no evidence of MHC-dependent social mate choice in the new populations. Instead, we find that older males and males with more microsatellite heterozygosity are more likely to have successfully paired. Our data cannot resolve whether these patterns in pairing were due to male-male competition or female choice. However, our research does suggest that female Seychelles warblers do not choose social mates using MHC class I to increase fitness. It may also indicate that the MHC-dependent EPP observed in the source population is probably due to mechanisms other than female precopulatory mate choice based on MHC cues.

The role of social environment on parental care: offspring benefit more from the presence of female than male helpers.

Investment in offspring depends on the costs and benefits to the carer, which can vary with sex and social status. Investment also depends on the effort of others by allowing for compensation (load-lightening), with biparental care studies showing that this depends on the state and type of the other carer. By contrast, studies on cooperative breeders have solely focussed on the effects of group size rather than its composition (i.e. social environment). Here we propose and provide the first test of the 'Social Environment' hypothesis, that is, how the characteristics (here the sex) of other helpers present in the group affect parental care and how this in turn affects offspring fitness in cooperatively breeding red-winged fairy-wrens (Malurus elegans). Breeders provisioned nestlings at a higher rate than helpers, but there was no sex difference in provisioning rate. Compensation to increasing group size varied little with sex and status, but strongly depended on social environment. All group members reduced their provisioning rates in response to an increasing number of male (load-lightening), but not female helpers (additive care). As a result, nestlings received more food and grew faster in the presence of female helpers. The increased nestling growth did convey a fitness advantage due to a higher post-fledging survival to adulthood. Our study provides the first evidence that parental care can depend on social environment. This could be an important overlooked aspect to explain variation in parental care in cooperative breeders in general and in particular the enormous variation between the sexes, which we reveal in a literature overview.

Helpers at the nest improve late-life offspring performance: evidence from a long-term study and a cross-foster experiment.

BACKGROUND: Conditions during an individual's rearing period can have far reaching consequences for its survival and reproduction later in life. Conditions typically vary due to variation in parental quality and/or the environment, but in cooperative breeders the presence of helpers adds an important component to this. Determining the causal effect of helpers on offspring fitness is difficult, since high-quality breeders or territories are likely to produce high-quality offspring, but are also more likely to have helpers because of past reproductive success. This problem is best resolved by comparing the effect of both helping and non-helping subordinates on offspring fitness, however species in which both type of subordinates commonly occur are rare. METHODOLOGY/PRINCIPAL FINDINGS: We used multi-state capture-recapture models on 20 years of data to investigate the effect of rearing conditions on survival and recruitment in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), with both helping and non-helping subordinates. The number of helpers in the rearing territory, but not territory quality, group- or brood size, was positively associated with survival of offspring in their first year, and later in life. This was not a result of group size itself since the number of non-helpers was not associated with offspring survival. Furthermore, a nestling cross-foster experiment showed that the number of helpers on the pre-foster territory was not associated with offspring survival, indicating that offspring from territories with helpers do not differ in (genetic) quality. CONCLUSIONS/SIGNIFICANCE: Our results suggest that the presence of helpers not only increase survival of offspring in their first year of life, but also subsequent adult survival, and therefore have important fitness consequences later in life. This means that when calculating the fitness benefits of helping not only short-term but also the late-life benefits have to be taken into account to fully understand the evolution of cooperative breeding.

Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric.

In cooperative breeders, the tension between the opposing forces of kin selection and kin competition is at its most severe. Although philopatry facilitates kin selection, it also increases the risk of inbreeding. When dispersal is limited, extra-pair paternity might be an important mechanism to avoid inbreeding, but evidence for this is equivocal. The red-winged fairy-wren is part of a genus of cooperative breeders with extreme levels of promiscuity and male philopatry, but is unique in that females are also strongly philopatric. Here, we test the hypothesis that promiscuity is an important inbreeding avoidance mechanism when both sexes are philopatric. Levels of extra-pair paternity were substantial (70% of broods), but did not arise through females mating with their helpers, but via extra-group mating. Offspring were more likely to be sired by extra-pair males when the social pair was closely related, and these extra-pair males were genetically less similar to the female than the social male and thus, inbreeding is avoided through extra-pair mating. Females were consistent in their choice of the extra-pair sire over time and preferred early moulting males. Despite neighbouring males often being close kin, they sired 37% of extra-pair offspring. However, females that gained paternity from neighbours were typically less related to them than females that gained paternity further away. Our study is the first to suggest that mating with both closely related social partners and neighbours is avoided. Such sophistication in inbreeding avoidance strategies is remarkable, as the extreme levels of promiscuity imply that social context may provide little cue to relatedness.