Social Mating System Research Articles

The evolution of social bonds in primate males

Social bonds, here defined as strong, equitable and enduring social relationships, increase fitness in both male and female primates irrespective of their dispersal regime. Despite the benefits they carry for some, social bonds evolved more often among female than among male primates which is thought to be caused by the unsharable nature of males’ limiting resource, fertilizations. Here we present a structured review of variation in primate male social relationships, mating systems, and social organization. In addition to classical socio-ecological reasoning and recent models on the evolution of male coalitions, we consider the phylogenetic history of species living in multi-male groups and alternative evolutionary routes to male co-residency, which may constrain the evolution of male social bonds in some cases. We summarize our results in a conceptual framework that represents the effects of male contest competition within and between groups on male social organization, affiliation and cooperation. We conclude that male social bonds evolved as long-term alliances that gain their adaptive function in within group contests and, thus, that the evolution of male social bonds is driven by variation in within group contest competition. Between group contest competition may select for large male group size but in the end it is the narrow window of medium to low within group contest competition that promotes the evolution of political coalitions and thus is responsible for the rarity of social bonds among primate males.

Observation of intra‐group and extra‐group copulation and reproductive characters in free ranging groups of western black crested gibbon (Nomascus concolor jingdongensis)

Black crested gibbons (Nomascus concolor) are 1 of only 3 gibbon species that have been observed in long-term polygynous groups, but their mating behavior and reproductive characters have never been reported. Based on population monitoring over 7 years and direct observation for 26 months of the study groups in Wuliang Mountain, central Yunnan, we describe for the first time the copulation behavior and breeding pattern of free-ranging western black crested gibbons. The gestation period of black crested gibbons is estimated to be between 6 and 7 months. The average breeding interval is 3.5 years, with infant independence at approximately 2.5 years. We observed 2 intra-group copulations and 5 extra-group copulations. Copulations were initiated when a female gave a 'solicitation' gesture. When a male made any mating attempt, the female might refuse it. These results demonstrate direct female mate choice. Both male and female gibbons dispersed from their natal groups and sometimes replaced paired adults in other groups. We observed no evidence of infanticide during inter-group conflicts or after replacement of adults. Together with extra-group copulations, these phenomena indicate a flexible social organization and complex mating system. We also observed a male-biased sex ratio among offspring. More genetic work is necessary to describe the effects of inter-group copulation and the genetic diversity of this population.

Development and characterization of twenty-two polymorphic microsatellite markers for the leafcutter ant, Acromyrmex lundii, utilizing Illumina sequencing

We isolated and characterized a total of 22 microsatellite loci for the leafcutter ant, Acromyrmex lundii. The loci were screened for 24 individuals from southern Brazil and Uruguay. The number of alleles per locus ranged from 5 to 20, the observed heterozygosity ranged from 0.417 to 0.917, and the probability of identity values ranged from 0.011 to 0.38. These genetic markers will be useful for understanding the population and conservation biology of the leafcutter ant A. lundii and closely related species, and will provide novel insights into the evolutionary biology of social parasitism and leafcutter ant mating systems.

Social and Genetic Mating System of the American Golden-Plover

Shorebirds are exceptionally diverse in their social mating systems, and genetic analyses of a few species have revealed further variation in genetic mating systems. The ecological and evolutionary causes of this variation are largely unknown. We studied the mating system of American Golden-Plovers (Pluvialis dominica) at Barrow, Alaska, between 2004 and 2009. In this arctic population, birds bred in socially monogamous pairs, as has been seen in other populations, yet rates of philopatry and mate fidelity were low. We used microsatellite DNA markers to analyze parentage and found that most offspring originated from monogamous matings, but 8% of 131 offspring and 16% of 37 nests were the result of nonmonogamous matings. One nest was ambiguous; it was either a full clutch sired through extra-pair copulation or represented an instance of social polygyny. Despite wide variation in synchrony of breeding and density of nesting both within and among breeding seasons, these ecological variables were unrelated to mating patterns. We speculate that the low rate of pair fidelity and the high rate of extrapair paternity are linked, because the lack of familiarity between partners reduces benefits of monogamy. Further study of breeding behavior and rates of philopatry are needed to understand why, among socially monogamous shorebirds, the American Golden-Plover has high rates of extra-pair paternity.

Social and genetic mating system of Ridgway's hawk (Buteo ridgwayi), an endemic raptor on Hispaniola

Abstract:Patterns of social organization and mating systems have been shown to be functions of ecological factors such as resource allocation and breeding density. In some species, particularly birds, social organization and genetic mating systems differ with molecular studies providing evidence of extra-pair young frequently occurring within broods of socially monogamous species. Here we examine the social and genetic mating system of an ecologically little-known forest raptor endemic to the island of Hispaniola in the Caribbean. From 2005–2009, our field observations of over 60 breeding pairs verified a social mating system of monogamy for the species. During the same time period, we collected blood samples (n= 146 birds, 48 nests) and used microsatellite profiles from 10 loci to estimate genetic relatedness among nestlings in a brood and assign putative fathers. We found no evidence of extra-pair paternity in 41 broods. We had one instance where a social male was not assigned as the putative father, however, the confidence level of this assignment was not significant since the genotypes of the social and assigned males were very similar. Our results support our hypothesis that genetic monogamy would be exhibited by Ridgway's hawk, an island-endemic tropical raptor.

Female ornamentation in Malurus fairy-wrens: a hidden evolutionary gem for understanding female perspectives on social and sexual selection

Phylogeny, ecological environment, social organisation, and mating system are expected to affect degree of female ornamentation, either directly or indirectly, but our understanding of how female ornaments respond to these forces remains incomplete. This article evaluates the evolutionary history and adaptive significance of three putative ornaments—plumage colouration, bill colouration and tail-length—in female fairy-wrens. Despite considerable research on these traits in male fairy-wrens, they have yet to be studied in any detail in females. Phylogeographic analyses in combination with life-history data suggest that female plumage colouration and bill colouration are under active selection, independent of that experienced by males. Social organisation and mating system, as mediated by ecological environment, may shape degree of ornamentation in these traits among females. In contrast, tail-length appears to be driven directly by natural ecological selection imposed by environmental conditions, leading to parallel trait evolution among the sexes within each species. More refined comparative and population-level investigations of adaptive consequences and proximate mechanisms are future research priorities. The study of female fairy-wrens holds great promise to advance our collective understanding of how the ecological environment interacts with sexual selection and social competition to shape ornament evolution in complex social organisms.

Extra‐pair paternity confirmed in wild white‐handed gibbons

Knowledge of the genetic mating system of animal species is essential for our understanding of the evolution of social systems and individual reproductive strategies. In recent years, genetic methods have uncovered an unexpected diversity of paternal genetic contributions across diverse animal social mating systems, but particularly in pair-living species. In most pair-living birds, for example, genetic and behavioral observations have confirmed a previously unknown significance of extra-pair copulations (EPCs) and extra-pair paternity. Among mammals, white-handed gibbons (Hylobates lar) are also known to live in pairs and are traditionally believed to be single-male single-female breeders. However, at Khao Yai National Park, Thailand, behavioral observations have confirmed the occurrence of both EPCs and functional multi-male grouping, but knowledge about the genetic mating system is still unavailable. In this study, we genotyped 89 white-handed gibbons of the Khao Yai population based on fecal samplings and were able to determine paternity for 41 offspring through short tandem repeat analysis. We found that females' stable social partners sired the majority (90.5%) of offspring (N = 38), while only a few (7.1%) offspring (n = 2 confirmed cases; n = 1 inferred case) were conceived with extra-pair partners. The paternity of one offspring remained inconclusive (2.4%), because the offspring's genotype did not mismatch with the genotypes of two potential sires. Like other predominantly pair-living species, gibbons appear to follow a mixed-reproductive strategy. The genetic mating system of wild white-handed gibbons is best described as flexible, primarily monogamous and opportunistically promiscuous. Inc.

Social systems and life‐history characteristics of mongooses

The diversity of extant carnivores provides valuable opportunities for comparative research to illuminate general patterns of mammalian social evolution. Recent field studies on mongooses (Herpestidae), in particular, have generated detailed behavioural and demographic data allowing tests of assumptions and predictions of theories of social evolution. The first studies of the social systems of their closest relatives, the Malagasy Eupleridae, also have been initiated. The literature on mongooses was last reviewed over 25 years ago. In this review, we summarise the current state of knowledge on the social organisation, mating systems and social structure (especially competition and cooperation) of the two mongoose families. Our second aim is to evaluate the contributions of these studies to a better understanding of mammalian social evolution in general. Based on published reports or anecdotal information, we can classify 16 of the 34 species of Herpestidae as solitary and nine as group-living; there are insufficient data available for the remainder. There is a strong phylogenetic signal of sociality with permanent complex groups being limited to the genera Crossarchus, Helogale, Liberiictis, Mungos, and Suricata. Our review also indicates that studies of solitary and social mongooses have been conducted within different theoretical frameworks: whereas solitary species and transitions to gregariousness have been mainly investigated in relation to ecological determinants, the study of social patterns of highly social mongooses has instead been based on reproductive skew theory. In some group-living species, group size and composition were found to determine reproductive competition and cooperative breeding through group augmentation. Infanticide risk and inbreeding avoidance connect social organisation and social structure with reproductive tactics and life histories, but their specific impact on mongoose sociality is still difficult to evaluate. However, the level of reproductive skew in social mongooses is not only determined by the costs and benefits of suppressing each other's breeding attempts, but also influenced by resource abundance. Thus, dispersal, as a consequence of eviction, is also linked to the costs of co-breeding in the context of food competition. By linking these facts, we show that the socio-ecological model and reproductive skew theory share some determinants of social patterns. We also conclude that due to their long bio-geographical isolation and divergent selection pressures, future studies of the social systems of the Eupleridae will be of great value for the elucidation of general patterns in carnivore social evolution.

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.

Non‐Monogamous Copulations and Potential Within‐Group Mating Competition in White‐Faced Saki Monkeys (Pithecia pithecia)

Many primates display within-species variation in social organization and mating system. Individuals of these species may be confronted with both the challenges of between-group competition to exclude same-sex competitors as well as within-group competition for mating opportunities. Free-ranging white-faced saki monkeys (Pithecia pithecia) live in both male-female pairs and small multi-male, multi-female groups. Despite commonly held views that this species is monogamous, there are currently no published accounts of mating patterns in the genus Pithecia. I recorded copulations and sexual behavior from three free-ranging groups of white-faced sakis at Brownsberg Naturepark, Suriname over a period of 17 months. Groups displayed both monogamous and polygynandrous mating. Individuals in polygynandrous groups were not observed to mate more frequently with certain partners. Copulation harassment occurred in 8.6% of copulations (total N = 81) and was performed by both sexes. This harassment successfully prevented ejaculation in six out of seven instances and harassment by males resulted in male-male aggression on four occasions. Two cases of female-directed sexual aggression by males were also observed, which may indicate that males use sexual coercion to influence female mating behavior. Although based on a small number of groups, these data show that white-faced sakis display variability in mating system and that this variability is not directly dictated by social organization. Furthermore, groups with promiscuous copulations exhibit behaviors indicative of within-group mating competition.

Constraints and flexibility in mammalian social behaviour: introduction and synthesis.

This paper introduces a Theme Issue presenting the latest developments in research on the interplay between flexibility and constraint in social behaviour, using comparative datasets, long-term field studies and experimental data from both field and laboratory studies of mammals. We first explain our focus on mammals and outline the main components of their social systems, focusing on variation within- and among-species in numerous aspects of social organization, mating system and social structure. We then review the current state of primarily ultimate explanations of this diversity in social behaviour. We approach the question of how and why the balance between behavioural flexibility and continuity is achieved by discussing the genetic, developmental, ecological and social constraints on hypothetically unlimited behavioural flexibility. We introduce the other contributions to this Theme Issue against this background and conclude that constraints are often crucial to the evolution and expression of behavioural flexibility. In exploring these issues, the enduring relevance of Tinbergen's seminal paper 'On aims and methods in ethology', with its advocacy of an integrative, four-pronged approach to studying behaviour becomes apparent: an exceptionally fitting tribute on the 50th anniversary of its publication.

Sex steroid hormones modulate responses to social challenge and opportunity in males of the monogamous convict cichlid, Amatitliana nigrofasciata

Steroid hormones play an important role in modulating behavioral responses to various social stimuli. It has been suggested that variation in the hormonal regulation of behavior across species is associated with social organization and/or mating system. In order to further elucidate the interplay of hormones and behavior in social situations, we exposed males of the monogamous convict cichlid Amatitliana nigrofasciata to three social stimuli: gravid female, intruder male, and a nonsocial stimulus. We used a repeated measure design to create behavioral profiles and explore how sex steroid hormones respond to and regulate social behavior. Results show distinct behavioral responses to different social situations, with circulating 11-ketotestosterone increasing in response to social stimuli. Pharmacological manipulations using specific androgen and estrogen receptor agonists and antagonists exposed complex control over digging behavior in the social opportunity context. In the social challenge context, aggressive behaviors decreased in response to blocking the androgen receptor pathway. Our results extend our understanding of sex steroid regulation of behavioral responses to social stimulation.

Decomposing variation in male reproductive success: age‐specific variances and covariances through extra‐pair and within‐pair reproduction

Age-specific variances and covariances in reproductive success shape the total variance in lifetime reproductive success (LRS), age-specific opportunities for selection, and population demographic variance and effective size. Age-specific (co)variances in reproductive success achieved through different reproductive routes must therefore be quantified to predict population, phenotypic and evolutionary dynamics in age-structured populations. While numerous studies have quantified age-specific variation in mean reproductive success, age-specific variances and covariances in reproductive success, and the contributions of different reproductive routes to these (co)variances, have not been comprehensively quantified in natural populations. We applied 'additive' and 'independent' methods of variance decomposition to complete data describing apparent (social) and realised (genetic) age-specific reproductive success across 11 cohorts of socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia). We thereby quantified age-specific (co)variances in male within-pair and extra-pair reproductive success (WPRS and EPRS) and the contributions of these (co)variances to the total variances in age-specific reproductive success and LRS. 'Additive' decomposition showed that within-age and among-age (co)variances in WPRS across males aged 2-4 years contributed most to the total variance in LRS. Age-specific (co)variances in EPRS contributed relatively little. However, extra-pair reproduction altered age-specific variances in reproductive success relative to the social mating system, and hence altered the relative contributions of age-specific reproductive success to the total variance in LRS. 'Independent' decomposition showed that the (co)variances in age-specific WPRS, EPRS and total reproductive success, and the resulting opportunities for selection, varied substantially across males that survived to each age. Furthermore, extra-pair reproduction increased the variance in age-specific reproductive success relative to the social mating system to a degree that increased across successive age classes. This comprehensive decomposition of the total variances in age-specific reproductive success and LRS into age-specific (co)variances attributable to two reproductive routes showed that within-age and among-age covariances contributed substantially to the total variance and that extra-pair reproduction can alter the (co)variance structure of age-specific reproductive success. Such covariances and impacts should consequently be integrated into theoretical assessments of demographic and evolutionary processes in age-structured populations.

Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis.

The hypothesis that patterns of sex-biased dispersal are related to social mating system in mammals and birds has gained widespread acceptance over the past 30 years. However, two major complications have obscured the relationship between these two behaviors: 1) dispersal frequency and dispersal distance, which measure different aspects of the dispersal process, have often been confounded, and 2) the relationship between mating system and sex-biased dispersal in these vertebrate groups has not been examined using modern phylogenetic comparative methods. Here, we present a phylogenetic analysis of the relationship between mating system and sex-biased dispersal in mammals and birds. Results indicate that the evolution of female-biased dispersal in mammals may be more likely on monogamous branches of the phylogeny, and that females may disperse farther than males in socially monogamous mammalian species. However, we found no support for a relationship between social mating system and sex-biased dispersal in birds when the effects of phylogeny are taken into consideration. We caution that although there are larger-scale behavioral differences in mating system and sex-biased dispersal between mammals and birds, mating system and sex-biased dispersal are far from perfectly associated within these taxa.

Development of a multiplex panel of microsatellite markers for two species of gliding marsupials, Petaurus breviceps and Petaurus norfolcensis

Here, we describe the development of seven new microsatellite loci from Petaurus breviceps. Together with eight loci from previous studies of gliders, we tested their utility for amplification, multiplexing and polymorphism in two glider species, P. breviceps and P. norfolcensis. Of the 15 loci tested, all were polymorphic in P. breviceps and 12 were polymorphic in P. norfolcensis. Overall, 260 sugar gliders from 13 sites in south-eastern South Australia and 106 squirrel gliders collected throughout south-east Queensland were used in analyses. Numbers of alleles per locus ranged from 4 to 27 in P. breviceps and from 2 to 44 in P. norfolcensis. Observed heterozygosity ranged between 0.438 and 0.904 in P. breviceps and between 0.189 and 0.981 in P. norfolcensis. Within the populations analysed, one of the 15 loci for P. breviceps and two of the 12 loci for P. norfolcensis deviated from Hardy–Weinberg equilibrium. The microsatellite loci will provide valuable tools for further study of social organisation, mating systems and population biology of these gliding marsupials.

Mating strategies, parental investment and mutual ornamentation in Iberian Rock Sparrows (Petronia petronia)

Relatively few bird species show complex social mating systems whose preponderance in a population is likely to affect the patterns of parental care observed there. In turn, parental investment is likely to be related to the expression of certain ornaments, which may reveal information on the bearer’s individual quality. Here we address both issues in a species characterised by several forms of parental care (both biparental and uniparental care) and in which both sexes possess a yellow breast patch, the rock sparrow (Petronia petronia). In our population, males contributed more to the care of the young in comparison with other populations. Social monogamy was the most frequent mating pattern and the percentage of cases of female (or male) brood desertion was lower with respect to that reported in previous studies, suggesting a flexible behaviour of this species to deal with different social environments. Birds did not pair assortatively with respect to the size of the yellow breast patch and we found no significant relationship between this trait and the frequency with which parents provisioned their chicks. However, we observed a positive relationship between male yellow patch size and nestling tarsus length, which suggests that more ornamented males are better parents. Males, but not females, differentially allocated parental investment in response to female ornamentation, although the benefits that males may gain from choosing more attractive females remain unidentified. Our results on paternal care investment along with previous studies on this species, reinforcing the view that the rock sparrow constitutes a good model to study sexual conflict over parental care under different social environments.

Unexpected strong polygyny in the brown-throated three-toed sloth.

Promiscuous mating strategies are much more common than previously appreciated. So much so, that several authors have proposed that promiscuity is the “rule” rather than the exception in vertebrate mating systems. Decreasing species mobility and increasing habitat fragmentation have both been suggested to reduce the “polygyny potential” of the environment and promote other mating strategies like promiscuity in females. We explored the social and genetic mating system for one of the most sedentary extant mammals, the brown-throated three-toed sloth (Bradypus variegatus), within a highly fragmented Neotropical habitat. Surprisingly, we found that three-toed sloths were strongly polygynous, with males excluding male competitors from their core ranges, and exhibiting strong reproductive skew. Indeed, only 25% of all resident adult males sired offspring and one individual sired half of all sampled juveniles. Paradoxically, a sedentary life-history strategy seems to facilitate polygyny in fragmented landscapes because multiple females can persist within small patches of habitat, and be monopolized by a single male. Our work demonstrates that strong polygyny can arise in systems in which the polygyny potential should be extremely low, and other strategies, including promiscuity, would be favoured. Mating systems can be influenced by a multitude of factor and are dynamic, varying among taxa, over time, and across habitats; consequently, mating systems remain difficult to predict based on general ecological principles.

Similar Patterns of Parental Provisioning in a Monogamous and a Polygynous Population of the House Wren

Abstract. In the House Wren (Troglodytes aedon), polygyny is characterized by males' partial desertion, males providing little or no help in feeding the nestlings of one of their mates. We evaluated whether contributions to feeding nestlings and patterns of provisioning by partially deserted females can explain geographic variation in the species' rate of polygyny. From 2003 to 2007, we studied two populations differing in polygyny rate (U.S., 40%; Argentina, 2%). We induced polygyny in the monogamous population by removing males from their territories before the onset of egg laying. We predicted that if patterns of parental care are related to variation in the social mating system, monogamous males should contribute more in the monogamous population than in the polygynous population, in the monogamous population partially deserted females should not compensate for the lack of help by feeding at rates higher than do aided females, and partial desertion should be more costly in the monogamous population. M...

Promiscuous mating in the harem‐roosting fruit bat,Cynopterus sphinx

Observations on mating behaviours and strategies guide our understanding of mating systems and variance in reproductive success. However, the presence of cryptic strategies often results in situations where social mating system is not reflective of genetic mating system. We present such a study of the genetic mating system of a harem-forming bat Cynopterus sphinx where harems may not be true indicators of male reproductive success. This temporal study using data from six seasons on paternity reveals that social harem assemblages do not play a role in the mating system, and variance in male reproductive success is lower than expected assuming polygynous mating. Further, simulations reveal that the genetic mating system is statistically indistinguishable from promiscuity. Our results are in contrast to an earlier study that demonstrated high variance in male reproductive success. Although an outcome of behavioural mating patterns, standardized variance in male reproductive success (I(m)) affects the opportunity for sexual selection. To gain a better understanding of the evolutionary implications of promiscuity for mammals in general, we compared our estimates of I(m) and total opportunity for sexual selection (I(m) /I(f), where I(f) is standardized variance in female reproductive success) with those of other known promiscuous species. We observed a broad range of I(m) /I(f) values across known promiscuous species, indicating our poor understanding of the evolutionary implications of promiscuous mating.

Intraspecific variability in the social and genetic mating systems of prairie voles, Microtus ochrogaster

Intraspecific variability in mating systems has been documented previously, but there are few studies where investigators have used intraspecific comparisons to investigate the influence of ecological or demographic factors on social and genetic mating systems. We studied two populations of prairie voles, Microtus ochrogaster, one near Lawrence, Kansas, U.S.A., and the other in Bloomington, Indiana, U.S.A. We examined differences in spatial structuring of vegetation between sites, which might contribute to intraspecific variation in social and genetic mating patterns. Since space use is often related to the mating system, we calculated home range size of a subset of adult males and females in both populations and used live trapping to examine the number of same- or opposite-sex conspecifics sharing capture locations. We applied social network analysis to live-trapping data to quantify the number and strength of social ties with opposite-sex conspecifics. Genetic parentage analysis provided an estimate of the number of mates per individual. We found that space use and overlap with members of the same and opposite sex were best explained by effects of site and sex. The relative strength of social associations with opposite-sex conspecifics was best predicted by site, density and sex. The genetic mating system was best explained by population density. Although we cannot disentangle population density from ecological variables related to site (e.g. distribution of vegetation) that may have affected social monogamy in our study populations, our study shows that extrinsic variables do affect differences in social and genetic mating systems between populations.