Mammalian Societies Research Articles

Epigenetic signatures of social status in wild female spotted hyenas (Crocuta crocuta)

In mammalian societies, dominance hierarchies translate into inequalities in health, reproductive performance and survival. DNA methylation is thought to mediate the effects of social status on gene expression and phenotypic outcomes, yet a study of social status-specific DNA methylation profiles in different age classes in a wild social mammal is missing. We tested for social status signatures in DNA methylation profiles in wild female spotted hyenas (Crocuta crocuta), cubs and adults, using non-invasively collected gut epithelium samples. In spotted hyena clans, female social status influences access to resources, foraging behavior, health, reproductive performance and survival. We identified 149 differentially methylated regions between 42 high- and low-ranking female spotted hyenas (cubs and adults). Differentially methylated genes were associated with energy conversion, immune function, glutamate receptor signalling and ion transport. Our results provide evidence that socio-environmental inequalities are reflected at the molecular level in cubs and adults in a wild social mammal.

Corrigendum: Editorial: Sex and gender effects on power, status, dominance, and leadership – an interdisciplinary look at human and other mammalian societies

Corrigendum: Editorial: Sex and gender effects on power, status, dominance, and leadership – an interdisciplinary look at human and other mammalian societies

Editorial: Sex and gender effects on power, status, dominance, and leadership – an interdisciplinary look at human and other mammalian societies

Editorial: Sex and gender effects on power, status, dominance, and leadership – an interdisciplinary look at human and other mammalian societies

Mechanisms of equality and inequality in mammalian societies.

The extent of (in)equality is highly diverse across species of social mammals, but we have a poor understanding of the factors that produce or inhibit equitable social organizations. Here, we adopt a comparative evolutionary perspective to test whether the evolution of social dominance hierarchies, a measure of social inequality in animals, exhibits phylogenetic conservatism and whether interspecific variation in these traits can be explained by sex, age or captivity. We find that hierarchy steepness and directional consistency evolve rapidly without any apparent constraint from evolutionary history. Given this extraordinary variability, we next consider multiple factors that have evolved to mitigate social inequality. Social networks, coalitionary support and knowledge transfer advantage to privilege some individuals over others. Nutritional access and prenatal stressors can impact the development of offspring, generating health disparities with intergenerational consequences. Intergenerational transfer of material resources (e.g. stone tools, food stashes, territories) advantage those who receive. Nonetheless, many of the same social species that experience unequal access to food (survival) and mates (reproduction) engage in levelling mechanisms such as food sharing, adoption, revolutionary coalitions, forgiveness and inequity aversion. Taken together, mammals rely upon a suite of mechanisms of (in)equality to balance the costs and benefits of group living. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Ethical standards for research on marine mammals

Conducting marine mammal research can raise several important ethical issues. For example, the continuation of whaling for commercial purposes despite the international moratorium provides opportunities for scientists to obtain data and tissue samples. In 2021 we analysed 35 peer-reviewed papers reporting research based on collaborations with Icelandic whalers. Results highlighted little consideration or understanding of the legal and ethical issues associated with the deliberate killing of whales amongst those researchers, funding bodies, universities and journals involved. Ethical statements were rarely provided. Those that were written were incomplete. Whilst research using whaling data may seem acceptable to some, it often becomes hard to justify when subject to scrutiny by the media and the public. Thus, there is a particular danger of reputational harm for early career researchers who may become unwittingly involved in such activities. Here we also consider the broader variety of ethical issues raised by non-lethal research (both historical and recent) on marine mammals including tagging and biopsy. We discuss instances where study animals were harmed or even killed and where the public mistook tags for harpoons. Without clear guidelines, reviewers and journal editors are put in an impossible position when considering whether to reject papers on ethical grounds. We propose that for such studies, universities, funders, journals, and permit issuers must require ethical assessments and that journals more effectively implement their existing policies on publishing ethical statements. The professional marine mammal societies need to work together to produce modern ethical guidance. Such guidance should require transparency in the provenance of data and samples while including advice on law, welfare issues, involvement of local scientists, and offshoring. Furthermore, it should require appraisal of and justification for the absolute necessity of invasive procedures. As is already the case in biomedical disciplines, ethical statements should be required in marine mammal science.

Sex and dominance: How to assess and interpret intersexual dominance relationships in mammalian societies

The causes and consequences of being in a particular dominance position have been illuminated in various animal species, and new methods to assess dominance relationships and to describe the structure of dominance hierarchies have been developed in recent years. Most research has focused on same-sex relationships, however, so that intersexual dominance relationships and hierarchies including both sexes have remained much less studied. In particular, different methods continue to be employed to rank males and females along a dominance hierarchy, and sex biases in dominance are still widely regarded as simple byproducts of sexual size dimorphism. However, males and females regularly compete over similar resources when living in the same group, and sexual conflict takes a variety of forms across societies. These processes affect the fitness of both sexes, and are mitigated by intersexual hierarchies. In this study, we draw on data from free-ranging populations of nine species of mammals that vary in the degree to which members of one sex dominate members of the other sex to explore the consequences of using different criteria and procedures for describing intra- and intersexual dominance relationships in these societies. Our analyses confirmed a continuum in patterns of intersexual dominance, from strictly male-dominated species to strictly female-dominated species. All indices of the degree of female dominance were well correlated with each other. The rank order among same-sex individuals was highly correlated between the intra- and intersexual hierarchies, and such correlation was not affected by the degree of female dominance. The relative prevalence of aggression and submission was sensitive to variation in the degree of female dominance across species, with more submissive signals and fewer aggressive acts being used in societies where female dominance prevails. Thus, this study provides important insights and key methodological tools to study intersexual dominance relationships in mammals.

An Evolutionary Explanation for the Female Leadership Paradox

Social influence is distributed unequally between males and females in many mammalian societies. In human societies, gender inequality is particularly evident in access to leadership positions. Understanding why women historically and cross-culturally have tended to be under-represented as leaders within human groups and organizations represents a paradox because we lack evidence that women leaders consistently perform worse than men. We also know that women exercise overt influence in collective group-decisions within small-scale human societies, and that female leadership is pervasive in particular contexts across non-human mammalian societies. Here, we offer a transdisciplinary perspective on this female leadership paradox. Synthesis of social science and biological literatures suggests that females and males, on average, differ in why and how they compete for access to political leadership in mixed-gender groups. These differences are influenced by sexual selection and are moderated by socioecological variation across development and, particularly in human societies, by culturally transmitted norms and institutions. The interplay of these forces contributes to the emergence of female leaders within and across species. Furthermore, females may regularly exercise influence on group decisions in less conspicuous ways and different domains than males, and these underappreciated forms of leadership require more study. We offer a comprehensive framework for studying inequality between females and males in access to leadership positions, and we discuss the implications of this approach for understanding the female leadership paradox and for redressing gender inequality in leadership in humans.

Reproduction Within a Hierarchical Society from a Female's Perspective.

The reproductive biology of many female mammals is affected by their social environment and their interactions with conspecifics. In mammalian societies structured by linear dominance hierarchies, such as that of the spotted hyena (Crocuta crocuta), a female's social rank can have profound effects on both her reproductive success and her longevity. In this species, social rank determines priority of access to food, which is the resource limiting reproduction. Due largely to rank-related variation in access to food, reproduction from the perspective of a female spotted hyena can only be understood in the context of her position in the social hierarchy. In this review, we examine the effects of rank on the various phases of reproduction, from mating to weaning. Summed over many individual reproductive lifespans, the effect of rank at these different reproductive phases leads to dramatic rank-related variation in fitness among females and their lineages. Finally, we ask why females reproduce socially despite these apparent costs of group living to low-ranking females. Gregariousness enhances the fitness of females regardless of their positions in the social hierarchy, and females attempting to survive and reproduce without clanmates lose all their offspring. The positive effects of gregariousness appear to result from having female allies, both kin and non-kin, who cooperate to advertise and defend a shared territory, acquire, and defend food resources, maintain the status quo, and occasionally also to rise in social rank.

Contrasts in kinship structure in mammalian societies

AbstractComparative studies of mammals confirm Hamilton’s prediction that differences in cooperative and competitive behavior across species will be related to contrasts in kinship between group members. Although theoretical models have explored the factors affecting kinship within social groups, few have analyzed the causes of contrasts in kinship among related species. Here, we describe interspecific differences in average kinship between group members among social mammals and show that a simple mathematical model that includes the number of breeding females, male reproductive skew, and litter size successfully predicts ~95% of observed variation in average kinship between group members across a sample of mammals. Our model shows that a wide range of conditions can generate groups with low average relatedness but only a small and rather specific set of conditions are likely to generate high average levels of relatedness between their members, providing insight into the relative rarity of advanced forms of cooperation in mammalian societies.

A framework for conceptualizing dimensions of social organization in mammals.

Mammalian societies represent many different types of social systems. While some aspects of social systems have been extensively studied, there is little consensus on how to conceptualize social organization across species. Here, we present a framework describing eight dimensions of social organization to capture its diversity across mammalian societies. The framework uses simple information that is clearly separated from the three other aspects of social systems: social structure, care system, and mating system. By applying our framework across 208 species of all mammalian taxa, we find a rich multidimensional landscape of social organization. Correlation analysis reveals that the dimensions have relatively high independence, suggesting that social systems are able to evolve different aspects of social behavior without being tied to particular traits. Applying a clustering algorithm allows us to identify the relative importance of key dimensions on patterns of social organization. Finally, mapping mating system onto these clusters shows that social organization represents a distinct aspect of social systems. In the future, this framework will aid reporting on important aspects of natural history in species and facilitate comparative analyses, which ultimately will provide the ability to generate new insights into the primary drivers of social patterns and evolution of sociality.

Causes and consequences of female centrality in cetacean societies.

Cetaceans are fully aquatic predatory mammals that have successfully colonized virtually all marine habitats. Their adaptation to these habitats, so radically different from those of their terrestrial ancestors, can give us comparative insights into the evolution of female roles and kinship in mammalian societies. We provide a review of the diversity of such roles across the Cetacea, which are unified by some key and apparently invariable life-history features. Mothers are uniparous, while paternal care is completely absent as far as we currently know. Maternal input is extensive, lasting months to many years. Hence, female reproductive rates are low, every cetacean calf is a significant investment, and offspring care is central to female fitness. Here strategies diverge, especially between toothed and baleen whales, in terms of mother-calf association and related social structures, which range from ephemeral grouping patterns to stable, multi-level, societies in which social groups are strongly organized around female kinship. Some species exhibit social and/or spatial philopatry in both sexes, a rare phenomenon in vertebrates. Communal care can be vital, especially among deep-diving species, and can be supported by female kinship. Female-based sociality, in its diverse forms, is therefore a prevailing feature of cetacean societies. Beyond the key role in offspring survival, it provides the substrate for significant vertical and horizontal cultural transmission, as well as the only definitive non-human examples of menopause. This article is part of the theme issue 'The evolution of female-biased kinship in humans and other mammals'.

Fine‐scale sociality reveals female–male affiliations and absence of male alliances in bottlenose dolphins (Tursiops truncatus) in the Shannon Estuary, Ireland

AbstractKnowledge of social behavior at an individual level is central to our understanding of complex mammalian societies. In this study, we analyzed the fine‐scale sociality of wild bottlenose dolphins in the Shannon Estuary, Ireland, by examining associations between members of the whole population and between specific female and male dolphins. We carried out 51 boat‐based individual focal follows on 18 identifiable bottlenose dolphins over 90.8 hr (39 days) between 2014 and 2016. Additionally, we conducted 353 boat‐based surveys (with 607 sightings) between 2012 and 2015, and identified 121 distinct adult/juvenile dolphins. The mean group size of focal dolphin groups was 7.2 ± 4.1 (range = 1–20) and the mean fission‐fusion rate was 3.06 ± 1.35 changes/hr. The most frequent composition of within‐group affiliate pairs was female–male. Focal males spent more time with female nearest‐neighbors than male nearest‐neighbors (p = .013). Differences between female and male activity budgets were not strongly supported (p = .13). There was no evidence for male alliance formation in the Shannon Estuary population, and all of the known‐sex top‐ranked associates (7) of known males (n = 10) were females. This research reveals a distinct bottlenose dolphin society with female–male affiliations and an absence of male alliances.

Genetic relatedness delineates the social structure of southern Australian bottlenose dolphins

AbstractSocial relationships represent an adaptive behavioral strategy that can provide fitness benefits to individuals. Within mammalian societies, delphinids are known to form diverse grouping patterns and show a variety of social systems. However, how ecological and intrinsic factors have shaped the evolution of such diverse societies is still not well understood. In this study, we used photo-identification data and biopsy samples collected between March 2013 and October 2015 in Coffin Bay, a heterogeneous environment in South Australia, to investigate the social structure of southern Australian bottlenose dolphins (Tursiops cf. australis). Based on the data from 657 groups of dolphins, we used generalized affiliation indices, and applied social network and modularity methods to study affiliation patterns among individuals and investigate the potential presence of social communities within the population. In addition, we investigated genetic relatedness and kinship relationships within and between the communities identified. Modularity analysis revealed that the Coffin Bay population is structured into 2 similar sized, mixed-sex communities which differed in ranging patterns, affiliation levels and network metrics. Lagged association rates also indicated that nonrandom affiliations persisted over the study period. The genetic analyses suggested that there was higher relatedness, and a higher proportion of inferred full-sibs and half-sibs, within than between communities. We propose that differences in environmental conditions between the bays and kinship relationships are important factors contributing to the delineation and maintenance of this social structure.

Obstacles and opportunities for female leadership in mammalian societies: A comparative perspective

Women remain universally underrepresented in the top leadership positions. A comparative evolutionary framework may offer new insights into the value of and potential barriers to female leadership. Here we define leaders as individuals who impose a disproportional influence on the collective behaviors of group members. We reviewed data for 76 social species of non-human mammals to reveal the circumstances favoring female leadership and species exhibiting female-biased leadership in two or more contexts (e.g., collective movements, group foraging, conflict resolution within groups, or conflicts between groups). Although rare across the lineage, female-biased leadership is pervasive in killer whales, lions, spotted hyenas, bonobos, lemurs, and elephants; leaders emerge without coercion and followers benefit from the social support and/or ecological knowledge from elder females. Our synthesis elucidates barriers to female leadership, but also reveals that traditional operationalizations of leadership are themselves male-biased. We therefore propose a new agenda for assessing the overlooked ways that females exert influence in groups.

Jealous females? Female competition and reproductive suppression in a wild promiscuous primate.

Female-female competition over paternal care has rarely been investigated in promiscuous mammals, where discreet forms of male care have recently been reported despite low paternity certainty. We investigated female competition over paternal care in a wild promiscuous primate, the chacma baboon (Papio ursinus), where pregnant and lactating females establish strong social bonds (friendships) with males that provide care to their offspring. We tested whether pregnant and lactating females interfere with the sexual activity of their male friend to prevent new conceptions that might lead to the subsequent dilution of his paternal care. We found that pregnant and lactating females were more aggressive towards oestrous females when they had recently conceived themselves, and when the oestrous female was mate-guarded by, and showed greater sexual activity with, their male friend. This aggression also reduced the likelihood of conception of the targeted female. These findings indicate that females can aggressively prevent further conceptions with their offspring's carer through reproductive suppression. Competition over access to paternal care may play an important and underestimated role in shaping female social relationships and reproductive strategies in promiscuous mammalian societies.

Vocal complexity and sociality in spotted paca (Cuniculus paca).

The evolution of sociality is related to many ecological factors that act on animals as selective forces, thus driving the formation of groups. Group size will depend on the payoffs of group living. The Social Complexity Hypothesis for Communication (SCHC) predicts that increases in group size will be related to increases in the complexity of the communication among individuals. This hypothesis, which was confirmed in some mammal societies, may be useful to trace sociality in the spotted paca (Cuniculus paca), a Neotropical caviomorph rodent reported as solitary. There are, however, sightings of groups in the wild, and farmers easily form groups of spotted paca in captivity. Thus, we aimed to describe the acoustic repertoire of captive spotted paca to test the SCHC and to obtain insights about the sociability of this species. Moreover, we aimed to verify the relationship between group size and acoustic repertoire size of caviomorph rodents, to better understand the evolution of sociality in this taxon. We predicted that spotted paca should display a complex acoustic repertoire, given their social behavior in captivity and group sightings in the wild. We also predicted that in caviomorph species the group size would increase with acoustic repertoire, supporting the SCHC. We performed a Linear Discriminant Analysis (LDA) based on acoustic parameters of the vocalizations recorded. In addition, we applied an independent contrasts approach to investigate sociality in spotted paca following the social complexity hypothesis, independent of phylogeny. Our analysis showed that the spotted paca’s acoustic repertoire contains seven vocal types and one mechanical signal. The broad acoustic repertoire of the spotted paca might have evolved given the species’ ability to live in groups. The relationship between group size and the size of the acoustic repertoires of caviomorph species was confirmed, providing additional support for the SCHC in yet another group of diverse mammals–caviomorph rodents.

The evolution of a rare mammalian trait \u2013 benefits and costs of male philopatry in proboscis bats

While inbreeding avoidance is widely accepted as the major driver of female natal dispersal, the evolution of male philopatry is still poorly understood and discussed to be driven by male mating strategy, mate competition among male kin and kin cooperation. During a twelve-year study, we gathered detailed genetic and observational data of individually marked proboscis bats to assess the degree of male philopatry as well as its costs and benefits to improve the understanding of its evolution. Our results reveal several patrilines with simultaneous presence of closely related males and a small proportion of unrelated immigrant males in their colonies. Philopatric males benefit from avoiding the costs of immigration into foreign colonies through significantly longer tenure, better integration (i.e. frequent nocturnal presence in the colonies) and consequently significantly higher reproductive success compared to immigrant males. Finally, we illustrate that despite a high proportion of philopatric males in the groups, the number of closely related competing males is low. Thus, the hypothesised costs of mate competition among male kin seem to be low in promiscuous mammalian societies with unrelated females and a small degree of male immigration and are readily outweighed by the benefits of staying in the natal group.

Comparative studies need to rely both on sound natural history data and on excellent statistical analysis.

We certainly agree with Schradin [1] that comparative studies need to use the best information available—as well as clear definitions, up-to-date statistical techniques and common sense. We have divided our response into two sections: the first dealing with Schradin's critique of our 2017 paper and the classification of the social organization of shrews; the second dealing with three general issues that his commentary raises. The paper that Schradin is commenting on [2] asks whether cooperative breeders (which we define as species where non-breeding helpers assist breeders to raise their young) in mammals are more commonly found in arid environments than monogamous species (defined as species where breeding pairs of males and females remain together for more than one season) from which cooperative breeders appear to be derived [3]. It shows that, as in birds, cooperative breeders tend to live in relatively arid habitats compared to monogamous species. As we describe below, these conclusions are unaffected by differences between our classification of the social organization of shrews and the classification suggested by Schradin. Schradin's first criticism is that the categorizations of shrews that we have used in this analysis were based on one paper on a single species. This is incorrect, for our categorization of shrews was based on more than 70 separate sources (see electronic supplementary material, appendix S1). When we published our dataset [4], we were required to reduce the associated reference list by the editors of the journal and, to comply, we removed around 75% of our 2000+ sources, often listing a single reference per species or group of species, and frequently using generic reviews for particular groups where these were available: for example, for many rodent species, we simply listed Wolff and Sherman's Rodent Societies [5], and …

Mating in a bisexually philopatric society: bottlenose dolphin females associate with adult males but not adult sons during estrous

In fission-fusion societies, group size and composition change dynamically, reflecting social preferences and pressures. Most notably during reproduction, intersexual group dynamics reflect a balance between female choice for optimal mates and male competition for mating access. In systems where males and females remain in their natal area for life (bisexual philopatry), females can reduce the risk of incest by avoiding mating or associating with male kin. Shark Bay bottlenose dolphins (Tursiops aduncus) live in fission-fusion societies that enable them to exercise age, sex, and kin association biases. To determine how the balance between female choice and male competition is achieved, we examined adult female association with juvenile and adult males, including sons during female receptive periods, using 30 years of longitudinal data. Adult females demonstrated an increase in adult male association just prior to known conceptions, while juvenile male association consistently remained low. A decline in male association post-conception suggests that one or both sexes detect pregnancy early on. When we examined female association with juvenile and adult sons, a distinct pattern emerged. Adult females preferentially associated with sons compared to non-sons of the same age class post-weaning. Strikingly, females rarely associated with their adult sons when cycling. Our results suggest that (1) adult males either out-compete juvenile males in gaining access to fertile females or females prefer adult to juvenile males and (2) females mitigate the risk of close inbreeding by reducing association with sons when cycling. No study has investigated behavioral strategies for reducing close inbreeding in bisexually philopatric, fluid mammal societies outside of humans. Using over 30 years of longitudinal data, we document how association dynamics change with female reproductive state. Post-weaning, mothers and sons associate, but almost never during conceptive periods. Adult male–female association is frequent during estrous, with a sharp decline after conception. Our study provides evidence for long-term kin recognition and detection of both estrous and early pregnancy among wild bottlenose dolphins. These findings have implications for the evolution of bisexual philopatry, fission-fusion dynamics, and infanticide—or lack thereof—in mammals.

Male Violence and Sexual Intimidation in a Wild Primate Society

Sexual violence occurring in the context of long-term heterosexual relationships, such as sexual intimidation, is widespread across human populations [1-3]. However, its evolutionary origins remain speculative because few studies have investigated the existence of comparable forms of sexual coercion in animals [4, 5], in which repeated male aggression toward a female provides the aggressor with delayed mating benefits [6]. Here, we test whether male aggression toward females functions as sexual coercion in wild chacma baboons (Papio ursinus). We found support for all three main predictions of the sexual coercion hypothesis [7]: male aggression (1) is greatest against cycling females, (2) is costly and represents the main source of injuries for cycling females, and (3) increases male mating success with their victims in the future. Detailed analysis of chronological sequences between aggression and matings ruled out other coercive mechanisms, such as short-term harassment and punishment, by showing that aggression and matings are temporally decoupled. This decoupling may explain why some forms of sexual violence have been largely overlooked in well-studied animal populations despite their likely impact on the fitness of both sexes. Finally, we found no support for alternative hypotheses such as a female preference for aggressive males[8, 9]. This new, detailed study of the forms and intensity of sexual intimidation in a wild primate suggests that it may be widespread across mammalian societies, with important implications for understanding the evolution of mate choice and sexual conflict in mammals, as well as the origins of human sexual violence.