Within‐group relatedness is correlated with colony‐level social structure and reproductive sharing in a social fish

In group‐living species, the degree of relatedness among group members often governs the extent of reproductive sharing, cooperation and conflict within a group. Kinship among group members can be shaped by the presence and location of neighbouring groups, as these provide dispersal or mating opportunities that can dilute kinship among current group members. Here, we assessed how within‐group relatedness varies with the density and position of neighbouring social groups in Neolamprologus pulcher, a colonial and group‐living cichlid fish. We used restriction site‐associated DNA sequencing (RADseq) methods to generate thousands of polymorphic SNPs. Relative to microsatellite data, RADseq data provided much tighter confidence intervals around our relatedness estimates. These data allowed us to document novel patterns of relatedness in relation to colony‐level social structure. First, the density of neighbouring groups was negatively correlated with relatedness between subordinates and dominant females within a group, but no such patterns were observed between subordinates and dominant males. Second, subordinates at the colony edge were less related to dominant males in their group than subordinates in the colony centre, suggesting a shorter breeding tenure for dominant males at the colony edge. Finally, subordinates who were closely related to their same‐sex dominant were more likely to reproduce, supporting some restraint models of reproductive skew. Collectively, these results demonstrate that within‐group relatedness is influenced by the broader social context, and variation between groups in the degree of relatedness between dominants and subordinates can be explained by both patterns of reproductive sharing and the nature of the social landscape.     

Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates

African wild dogs (Lycaon pictus) live in cooperative packswith a clear-cut dominance hierarchy in each sex. Reproductionis largely monopolized by the dominant male and female. Alphafemales produced 76% of all litters in the Selous Game Reserveand 81% in Kruger National Park. Only 6-17% of subordinate femalesgave birth each year, compared to 82% of dominant females. Innonmating periods, subordinate females had higher estrogen levelsand higher estrogen/progestin ratios than alpha females, apparentlypreventing ovulation. During mating periods, subordinate femaleshad lower estrogen levels than dominants, mated less often,and were less aggressive. Subordinate males mated at low rates,wore less aggressive than dominants, and had lower testosteronelevels. Beta males were similar to alpha males behavioraDy andhormonaUy, suggesting that alpha males may share paternity withbeta males. If paternity is more evenly shared than maternity,then subordinate males have a larger incentive than subordinatefemales to remain in the pack. Following this expectation, dispersalin Selous was female biased (49% versus 24% dispersing annually).Perhaps as a result of mortality associated with dispersal,the adult sex ratio was male biased, although the pup sex ratiowas unbiased. In Kruger, neither dispersal nor the adult sex-ratiowas biased. Reproductive suppression is widely thought to becaused by social stress in subordinates, but basal cortkosteronelevels were higher in dominants than in subordinates     

Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid

Kin selection can explain the evolution of cooperative breeding and the distribution of relatives within a population may influence the benefits of cooperative behaviour. We provide genetic data on relatedness in the cooperatively breeding cichlid Neolamprologus pulcher. Helper to breeder relatedness decreased steeply with increasing helper age, particularly to the breeding males. Helper to helper relatedness was age‐assortative and also declined with age. These patterns of relatedness could be attributed to territory take‐overs by outsiders when breeders had disappeared (more in breeding males), between‐group dispersal of helpers and reproductive parasitism. In six of 31 groups females inherited the breeding position of their mother or sister. These matrilines were more likely to occur in large groups. We conclude that the relative fitness benefits of helping gained through kin selection vs. those gained through direct selection depend on helper age and sex.     

Hormonal correlates of dominance in meerkats (Suricata suricatta)

In cooperatively breeding meerkats (Suricata suricatta), individuals typically live in extended family groups in which the dominant male and female are the primary reproductives, while their offspring delay dispersal, seldom breed, and contribute to the care of subsequent litters. Here we investigate hormonal differences between dominants and subordinates by comparing plasma levels of luteinizing hormone (LH), estradiol and cortisol in females, and testosterone and cortisol in males, while controlling for potential confounding factors. In both sexes, hormone levels are correlated with age. In females, levels of sex hormone also vary with body weight and access to unrelated breeding partners in the same group: subordinates in groups containing unrelated males have higher levels of LH and estradiol than those in groups containing related males only. When these effects are controlled, there are no rank-related differences in circulating levels of LH among females or testosterone among males. However, dominant females show higher levels of circulating estradiol than subordinates. Dominant males and females also have significantly higher cortisol levels than subordinates. Hence, we found no evidence that the lower levels of plasma estradiol in subordinate females were associated with high levels of glucocorticoids. These results indicate that future studies need to control for the potentially confounding effects of age, body weight, and access to unrelated breeding partners before concluding that there are fundamental physiological differences between dominant and subordinate group members.     

Factors influencing and consequences of breeding dispersal and habitat choice in female grey seals (<Emphasis Type="Italic">Halichoerus grypus</Emphasis>) on Sable Island,Nova Scotia

Selection of breeding location can influence reproductive success and fitness. Breeding dispersal links habitat use and reproduction. This study investigated factors affecting breeding dispersal and its reproductive consequences in grey seals (Halichoerus grypus) on Sable Island, Nova Scotia. Breeding dispersal distance was determined in 692 individually marked, known-age female grey seals observed from 2004 to 2014. We used generalized linear mixed-effects models to test hypotheses concerning environmental and demographic factors influencing breeding dispersal distance and the consequences of dispersal distance on offspring weaning mass. Grey seal females rarely exhibited fidelity to previous breeding sites. Median dispersal distance between years was 5.1 km. Only 2.9% of females returned to a previous breeding site. Breeding dispersal distance was affected by parity and density, but effects were small and are presumably of no biological significance. Variation in dispersal distance among adult females was large. Dispersal distance had no significant influence on offspring weaning mass; however, as previously found, pup sex and maternal age did. Although breeding location was not important, heavier pups were born in habitats with no tidal or storm-surge influence indicating that breeding habitat type did influence offspring size at weaning. The lack of site fidelity in grey seals on Sable Island is associated with an unpredictable and changing landscape (sand dunes) that could make it difficult for females to locate previous breeding locations. Although breeding location within habitat type had small consequences on offspring weaning mass, we detected no evidence that breeding site selection within the habitat had consequences to females.     

Socio-genetic correlates of unbiased sex dispersal in a population of black capuchin monkeys (<Emphasis Type="Italic">Sapajus nigritus</Emphasis>)

Most social mammal species exhibit male-biased dispersal. Sex bias in dispersal leads to a higher degree of relatedness among individuals of the philopatric sex, thus an atypical dispersal pattern might lead to deviations in the typical within-group kinship structure. Kinship, in turn, influences patterns of social interactions, as widely evident by kin-biased behaviors. We investigated the link between dispersal, relatedness structure, and sociopositive interactions established by adult females of black capuchin monkeys (Sapajus nigritus) living in a population that experiences female dispersal, an unusual pattern for capuchin monkeys. The study was conducted in Parque Estadual Carlos Botelho (PECB), within the Brazilian Atlantic Forest. We addressed dispersal and relatedness patterns by genotyping 20 adults of 3 groups across 9 microsatellite loci. We also sampled the monkeys’ behavior and compared spatial association frequencies and rates of grooming among same- and opposite-sex dyads. There was no difference between males and females in genetic parameters; both males and females show low coefficients of relatedness indicating that neither sex is consistently philopatric. The mean pairwise coefficient of relatedness for co-resident females was not higher than that for co-resident males. Compared to other populations of capuchin monkeys, female bond was weak, as evident by lower spatial association frequencies, reduced rates of grooming and lack of correlation between coefficients of relatedness and measures of dyadic sociopositive interactions. Our findings thus confirm that female dispersal is a habitual process in the capuchin population of PECB, and that, as expected, dispersal by females strongly influences the relatedness structure of the population as well as the affiliative relationships among female groupmates.     

Dispersal and extra-territorial prospecting by slender-tailed meerkats (Suricata suricatta) in the south-western Kalahari

Dispersal in slender-tailed meerkats or suricates, Suricata suricatta, in the south-western Kalahari occurred mainly during the early breeding season, and was age- and sex-dependent. Among yearlings, more males than females were immigrants, but more females than males disappeared. There were no sex differences in dispersal among two-year-olds, but among animals aged three years or older, more males than females emigrated. Most dispersers moved into adjacent bands or joined other transients, and females apparently suffered higher rates of mortality than males. Kinship with the same-sex or opposite-sex breeder had no discernible effect on the likelihood of dispersing. Both males and females made prospecting forays to other groups, apparently to assess dispersal and breeding opportunities. Males made frequent and repeated forays, often in coalitions with other band members or transients, whereas prospecting by females was generally solitary, and they were not known to make multiple forays. Prospecting males successfully took over dominance of two bands, and attempted to take over bands on three other occasions. Animals attempting to join or follow a band ( trailers ) behaved submissively and were readily chased by residents, whereas those attempting a dominance takeover ( invaders ) scent-marked at a high rate and showed no submissive behaviours. Dispersing meerkats maximized reproductive success by increasing their mating opportunities, while animals which delayed dispersal received indirect benefits by helping to raise kin.     

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

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

Inclusive fitness and reproductive strategies in dwarf mongooses

Dwarf mongooses (Helogale parvula) are small, communally breedingcarnivores found in woodland and tree-savanna throughout Africa.Within a pack, socially subordinate mongooses do not normallybreed, yet they invariably participate in all aspects of parentalcare. The primary alternative to tolerating reproductive suppressionis dispersal, which shortens the wait for dominance and breeding.Here, we calculate the annual inclusive fitness payoffs to thedispersing and nondispersing strategies for males and femalesof ages one to seven, using data from a 14-year study in SerengetiNational Park, Tanzania. Factors with effects on inclusive fitnessincluded relatedness to pack mates before and after dispersal,the effect of help on recipients' reproductive success, theprobability of dispersing successfully, the probability of attainingdominance, and reproductive success after attaining dominance.All of these factors differed between male and female dwarfmongooses. We compared the contributions of direct and indirectfitness to the total fitness of mongooses pursuing each of thestrategies, across a range of ages. In our population, dispersaland nondispersal both yielded direct and indirect payoffs atmost ages. For dispersers of both sexes, direct fitness wasthe primary component of total fitness but indirect fitnesswas substantial for young (< 2 years old) dispersers. Fornondispersers of both sexes, indirect fitness was the majorcomponent of total fitness among young mongooses (up to 2 or3 years), but direct fitness was the major component among oldermongooses. By comparing the inclusive fitness payoffs for thetwo strategies, we determined the range of ages at which dispersalshould be favored for each sex. These comparisons correctlypredicted that males should be more dispersive than femalesat all ages, and that males should disperse over a broader rangeof ages.     

Seasonal variation of reproductive success under female philopatry and male-biased dispersal in a common vole population

Variation of reproductive success, an important determinant of the opportunity for sexual selection, is an outcome of competition within one sex for mating with members of the other sex. In promiscuous species, males typically compete for access to females, and their reproductive strategies are strongly related to the spatial distribution of females. I used 10 microsatellite loci and the mtDNA control region to determine seasonal differences in the reproductive success of males and females of the common vole (Microtus arvalis), one of the most numerous mammals in Europe. The sex-related spatial structure and bias in dispersal between genders were also assessed. Standardized variance of the reproductive success of females did not vary seasonally due to the continuity of female philopatry throughout the breeding season and to the constancy of the number of females reproducing successfully in each season. The males are the dispersing sex, undergoing both natal and breeding dispersal. Their standardized variance of reproductive success was significantly higher than that for females in July, when only two males monopolized 80% of the females in the population and when variance of male reproductive success was highest (I_m = 7.70). The seasonally varying and high standardized variance of male reproductive success may be explained by male-male competition for matings, coupled with seasonal changes in the age structure of the population.     

Female-mediated causes and consequences of status change in a social fish

In highly social species, dominant individuals often monopolize reproduction, resulting in reproductive investment that is status dependent. Yet, for subordinates, who typically invest less in reproduction, social status can change and opportunities to ascend to dominant social positions are presented suddenly, requiring abrupt changes in behaviour and physiology. In this study, we examined male reproductive anatomy, physiology and behaviour following experimental manipulations of social status in the cooperatively breeding cichlid fish, Neolamprologus pulcher. This unusual fish species lives in permanent social groups composed of a dominant breeding pair and 1-20 subordinates that form a linear social dominance hierarchy. By removing male breeders, we created 18 breeding vacancies and thus provided an opportunity for subordinate males to ascend in status. Dominant females play an important role in regulating status change, as males successfully ascended to breeder status only when they were slightly larger than the female breeder in their social group. Ascending males rapidly assumed behavioural dominance, demonstrated elevated gonadal investment and androgen concentrations compared with males remaining socially subordinate. Interestingly, to increase gonadal investment ascending males appeared to temporarily restrain somatic growth. These results highlight the complex interactions between social status, reproductive physiology and group dynamics, and underscore a convergent pattern of reproductive investment among highly social, cooperative species.     

Masculinized dominant females in a cooperatively breeding species

The molecular mechanisms underlying complex social behaviours such as dominance are largely unknown. Studying the cooperatively breeding African cichlid Neolamprologus pulcher, we show that dominant females were similar to dominant males in dominance behaviour, high testosterone levels and brain arginine vasotocin expression (a neuropeptide involved in vertebrate territorial, reproductive and social behaviours) compared to subordinate helpers, but had lower levels of 11-ketotestosterone than males. Furthermore, brain gene expression profiles of dominant females were most similar to those of the males (independent of social rank). Dominant breeder females are masculinized at the molecular and hormonal level while being at the same time reproductively competent, suggesting a modular organization of molecular and endocrine functions, allowing for sex-specific regulation.     

Sex differences in dispersal and the evolution of helping and harming

In this article, we explore the impact of sex-biased dispersal on local relatedness and on selection for helping and harming behavior among males and females. We show that in a patch-structured population, when there is a marked sex bias in dispersal, selection will almost always favor harming behavior among individuals of the sex more prone to dispersal. This result holds regardless of the effects of mating skew or overlapping generations. Selection may well also favor helping behavior among individuals of the philopatric sex, particularly if there is generational overlap, but this is less likely to occur if individuals of the philopatric sex compete more intensely for fewer breeding opportunities. In this last case, if generational overlap is low and mating skew pronounced, the result may be selection for harming behavior among both males and females. In general, the rate of dispersal and the level of relatedness among individuals of one sex do not reliably predict their level of helping or harming behavior; selection on either males or females depends on the dispersal of both sexes.     

Social control of reproduction in banded mongooses

Recent theoretical work suggests that the distribution of reproduction, or degree of reproductive skew, in animal societies depends crucially on (1) whether dominant individuals can fully control subordinate reproduction, and (2) how subordinate reproduction affects the fitness of dominants. I investigated these two factors in cooperatively breeding banded mongooses, Mungos mungo. Female packmates entered oestrus together and were closely guarded by dominant males. These males were aggressive to subordinate males who attempted to mate, but females still managed to mate with males other than their mate guard. Older females were guarded and mated a few days before their younger packmates, yet all females usually gave birth on the same day, suggesting that older females may have a longer gestation period. Moreover, older females carried more fetuses. Overall, ca. 83% of adult females conceived in each breeding attempt and 71% carried to term. These results indicate that, among males, dominant individuals did not have full control over the mating attempts of subordinates (since they could not fully control the mating behaviour of the females they guarded), while among females there was little or no attempt to prevent subordinates from breeding (at least, prior to parturition). Two within-group infanticides by males suggested that some control over reproduction may be exercised postpartum. Per capita survivorship of young in the den increased with the number of females who gave birth. Thus, dominant females may benefit from subordinate reproduction, providing a possible explanation for the lack of reproductive suppression among females in this species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high‐skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long‐term genetic and observational data to examine factors affecting reproductive skew in the high‐skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within‐group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate‐guarding and potentially reproductive restraint (for males). Ecological conditions or “outside options” affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.     

To what extent does living in a group mean living with kin?

Chimpanzees live in large groups featuring remarkable levels of gregariousness and cooperation among the males. Because males stay in their natal communities their entire lives and are hence expected to be living with male relatives, cooperation is therefore assumed to occur within one large 'family' group. However, we found that the average relatedness among males within several chimpanzee groups as determined by microsatellite analysis is in fact rather low, and only rarely significantly higher than average relatedness of females in the groups or of males compared across groups. To explain these findings, mathematical predictions for average relatedness according to group size, reproductive skew and sex bias in dispersal were derived. The results show that high average relatedness among the philopatric sex is only expected in very small groups, which is confirmed by a comparison with published data. Our study therefore suggests that interactions among larger number of individuals may not be primarily driven by kin relationships.     

Two breeding females within free-living groups may not always indicate polygyny: alternative subordinate female strategies in common marmosets (Callithrix jacchus)

The mating system of callitrichids has been reported to be monogamous, polygynous and polyandrous. In Callithrix jacchus, groups with 2 breeding females and groups with 1 breeding female have been reported. Our purpose was to evaluate the occurrence of occasional reproduction by subordinate females in free-ranging C. jacchus groups characterized as monogamous. Four groups were monitored at a field site of IBAMA-Brazil for between 20 and 72 months. We recorded the birth of 7 sets of twins to subordinate females that had never reproduced before. Sexual activities were recorded opportunistically: dominant females copulated with only the resident male, while subordinates copulated with extra-group males. We suggest these were essentially monogamous groups that occasionally had 2 reproductive females. Between-group copulations seem to be an alternative strategy used by the subordinates. Despite the costs, there would probably be benefits as a result of scanning for vacancies for reproductive positions in neighbouring groups and the establishment of ties with extra-group males that might become a reproductive partner in the future.     

Molecular insight into patterns of colony composition and paternity in the common mole-rat Cryptomys hottentotus hottentotus

We report the discovery of intraspecific variation in both colony composition and patterns of paternity in two populations of the social common mole-rat Cryptomys hottentotus hottentotus. These two populations represent the mesic and arid habitat extremes of the species' broad ecological range in South Africa. Until recently colonies of the common mole-rat were thought to consist of familial groups whereby all colony members were the offspring of a monogamous reproductive pair. The remaining colony members were thought to forego reproduction until both social and ecological conditions favoured dispersal and opportunities for independent outbreeding. Results from genetic assignment tests using microsatellite markers indicate that while colony composition is dominated by familial groups, colonies within both populations included both adult and subadult foreign conspecifics. Analysis of parentage reveals that the social organization of C. h. hottentotus is not that of strict monogamy; paternity of offspring was not assigned consistently to the largest, most dominant male within the colony. Moreover, a number of significantly smaller males were found to sire offspring, suggesting a sneak-mating strategy by subordinate within-colony males. Extra-colony extra-pair paternity (ECP) was also found to characterize C. h. hottentotus colonies, occurring with similar frequencies in both habitats. Both dominant established breeding males and subordinate males were identified as siring young in nonsource colonies. Furthermore, established breeding males were found to sire extra-colony young in the same season as siring young within their source colonies. We discuss the significance of these results within the context of the divergent ecological regimes characterizing the two sites and observe that our results revisit the accuracy of using behavioural and morphological characters, which have structured the basis of our understanding of the behavioural ecology of this species, as indicators of breeding status in mark-recapture studies.     

No evidence of inbreeding avoidance or inbreeding depression in a social carnivore

Dispersal by young mammals away from their natal site is generallythought to reduce inbreeding, with its attendant negative fitnessconsequences. Genetic data from the dwarf mongoose, a pack-livingcarnivore common in African savannas, indicate that there areexceptions to this generalization. In dwarf mongoose populationsin the Serengeti National Park, Tanzania, breeding pairs arecommonly related, and close inbreeding has no measurable effecton offspring production or adult survival. Inbreeding occursbecause average relatedness among potential mates within a packis high, because mating patterns within the pack are randomwith respect to the relatedness of mates, and because dispersaldoes little to decrease the relatedness among mates. Young femalesare more likely to leave a pack when the dominant male is aclose relative but are relatively infrequent dispersers. Youngmales emigrate at random with respect to the relatedness ofthe dominant female and tend to disperse to packs that containgenetically similar individuals.[Behav Ecol 7: 480–489(1996)]