Social complexity has been one of the recent emerging topics in the study of animal and human societies, but the concept remains both poorly defined and understood. In this paper, I critically review ...definitions and studies of social complexity in invertebrate and vertebrate societies, arguing that the concept is being used inconsistently in studies of vertebrate sociality. Group size and cohesion define one cornerstone of social complexity, but the nature and patterning of social interactions contribute more to interspecific variation in social complexity in species with individual recognition and repeated interactions. Humans provide the only example where many other unique criteria are used, and they are the only species for which intraspecific variation in social complexity has been studied in detail. While there is agreement that complex patterns emerge at the group level as a result of simple interactions and as a result of cognitive abilities, there is consensus neither on their relative importance nor on the role of specific cognitive abilities in different lineages. Moreover, aspects of reproduction and parental care have also been invoked to characterize levels of social complexity, so that no single comprehensive measure is readily available. Because even fundamental components of social complexity are difficult to compare across studies and species because of inconsistent definitions and operationalization of key social traits, I define and characterize social organization, social structure, mating system, and care system as distinct components of a social system. Based on this framework, I outline how different aspects of the evolution of social complexity are being studied and suggest questions for future research.
Theoretical models and empirical studies in various taxa have identified important links between variation in sex roles and the number of adult males and females (adult sex ratio (ASR)) in a ...population. In this review, I examine these relationships in non-human primates. Because most existing theoretical models of the evolution of sex roles focus on the evolutionary origins of sex-biased behaviour, they offer only a general scaffold for predicting variation in sex roles among and within species. I argue that studies examining sex role variation at these more specific levels need to take social organization into account to identify meaningful levels for the measurement of ASR and to account for the fact that ASR and sex roles mutually influence each other. Moreover, taxon-specific life-history traits can constrain sex role flexibility and impact the operational sex ratio (OSR) by specifying the minimum length of female time outs from reproduction. Using examples from the primate literature, I highlight practical problems in estimating ASR and OSR. I then argue that interspecific variation in the occurrence of indirect forms of paternal care might indeed be linked to variation in ASR. Some studies also indicate that female aggression and bonding, as well as components of inter-sexual relationships, are sensitive to variation in ASR. Thus, links between primate sex roles and sex ratios merit further study, and such studies could prompt the development of more specific theoretical models that make realistic assumptions about taxon-specific life history and social organization.
This article is part of the themed issue ‘Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies’.
In animal societies, control over resources and reproduction is often biased towards one sex. Yet, the ecological and evolutionary underpinnings of male-female power asymmetries remain poorly ...understood. We outline a comprehensive framework to quantify and predict the dynamics of male-female power relationships within and across mammalian species. We show that male-female power relationships are more nuanced and flexible than previously acknowledged. We then propose that enhanced reproductive control over when and with whom to mate predicts social empowerment across ecological and evolutionary contexts. The framework explains distinct pathways to sex-biased power: coercion and male-biased dimorphism constitute a co-evolutionary highway to male power, whereas female power emerges through multiple physiological, morphological, behavioural, and socioecological pathways.
This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from ...insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research.
Abstract
Biomedical and social scientists are increasingly calling the biological sex into question, arguing that sex is a graded spectrum rather than a binary trait. Leading science journals have ...been adopting this relativist view, thereby opposing fundamental biological facts. While we fully endorse efforts to create a more inclusive environment for gender‐diverse people, this does not require denying biological sex. On the contrary, the rejection of biological sex seems to be based on a lack of knowledge about evolution and it champions species chauvinism, inasmuch as it imposes human identity notions on millions of other species. We argue that the biological definition of the sexes remains central to recognising the diversity of life. Humans with their unique combination of biological sex and gender are different from non‐human animals and plants in this respect. Denying the concept of biological sex, for whatever cause, ultimately erodes scientific progress and may open the flood gates to “alternative truths.”
Even after the 150th anniversary of sexual selection theory, the drivers and mechanisms of female sexual selection remain poorly studied. To understand demographic circumstances favoring ...female-female competition, trade-offs with kin selection and interactions with male reproductive strategies, we investigated female evictions in redfronted lemurs (
Eulemur rufifrons
). Based on 24 years of demographic data of known individuals, we show that female redfronted lemurs target close female kin for forcible, permanent, and presumably lethal eviction, even though groups contain multiple unrelated males whose voluntary emigration actually mitigated the probability of future female evictions. Female eviction and male emigration were predicted by group size, but male emigration was primarily driven by a proportional increase of male rivals. Female evictions were more likely than male emigrations when there were more juvenile females in a group, but the identity of evicted females was not predicted by any intrinsic traits. While birth rates were reduced by the number of juvenile females, they were higher when there were more adult females in a group and in years with more rainfall. Early infant survival was reduced with increasing numbers of juvenile females, but variation in female lifetime reproductive success was not related to any of the predictors examined here. Thus, there seems to be a limit on female group size in this lemur species. More generally, our study demonstrates a balanced interplay between female reproductive competition, competition over group membership between both sexes, and kin selection, contributing new insights into the causes and consequences of female competition in animal societies.
Significance statement
The evolutionary causes of female competition in vertebrate societies remain poorly known. Evictions represent an extreme form of female competition because even close kin are evicted when same-sized unrelated males are theoretically also available as victims. We studied drivers and consequences of evictions in redfronted lemurs (
Eulemur rufifrons
) using 24 years of demographic data from multiple groups. We show that while voluntary male emigration mitigates the probability of future female evictions, females nonetheless appear to accept the fitness costs of evicting female kin. While group size seems to be the main driver of departures by either sex, the number of juvenile females present in groups is the key variable triggering eviction events as well as physiological responses that could be interpreted as female reproductive restraint. Our study therefore revealed that competition does trump cooperation under some circumstances in the intricate interplay between sexual selection and kin selection on females.
Pheromones mediate a wide range of functions across the animal kingdom 1, and such chemosensory communication is especially widespread among mammals 2. In a recent paper in Current Biology, Shirasu, ...Ito et al. 3 describe the results of a series of chemical and behavioral studies that identified three aldehyde odors released from the wrist gland of ring-tailed lemurs (Lemur catta) that could represent the first identified sex pheromones in male primates. Observations of a captive group and controlled presentations of isolated male scent samples showed captive female lemurs sniffing antebrachial scent marks longer on average during the breeding season. Comparison of the chemical profiles of antebrachial secretions between breeding- and non-breeding-season samples revealed three aldehydes putatively responsible for the female response, the concentration of one of these subsequently shown to increase following testosterone injection of one male. Average sniffing duration of two females increased slightly with increasing concentrations of two of the three aldehydes in one experiment, and so did the response of seven other females to swabs with mixtures of the three compounds, compared to individually presented aldehydes. From these results, the authors conclude that “it is conceivable that the identified C12 and C14 aldehydes are putative sex pheromones that aid male–female interactions among lemurs.” Here, I argue that, in fact, more data are needed to determine whether antebrachial marking and these substances are actually involved in mediating the attractiveness of males to females during the breeding season. My specific concerns pertain to several aspects of the methods that produce ambiguous results and conclusions that are too strong, especially when considering the broader context of lemur biology.
Kappeler challenges the conclusions of a recent study by Shirasu, Ito et al. that male glandular odorants of ring-tailed lemurs act as a sex pheromone that attract females.
The endemic lemurs of Madagascar (Lemuriformes: Primates) exhibit great social and communicative diversity. Given their independent evolutionary history, lemurs provide an excellent opportunity to ...identify fundamental principles in the coevolution of social and communicative traits. We conducted comparative phylogenetic analyses to examine patterns of interspecific variation among measures of social complexity and repertoire sizes in the vocal, olfactory and visual modality, while controlling for environmental factors such as habitat and number of sympatric species. We also examined potential trade-offs in signal evolution as well as coevolution between body mass or brain size and communicative complexity. Repertoire sizes in the vocal, olfactory and visual modality correlated positively with group size, but not with environmental factors. Evolutionary changes in social complexity presumably antedated corresponding changes in communicative complexity. There was no trade-off in the evolution of signals in different modalities and neither body mass nor brain size correlated with any repertoire size. Hence, communicative complexity coevolved with social complexity across different modalities, possibly to service social relationships flexibly and effectively in pair- and group-living species. Our analyses shed light on the requirements and adaptive possibilities in the coevolution of core elements of social organization and social structure in a basal primate lineage.
This article is part of the theme issue ‘Cognition, communication and social bonds in primates’.
Abstract
Sex-specific reproductive strategies are shaped by the distribution of potential mates in space and time. Labord’s chameleon (
Furcifer labordi
) from southwestern Madagascar is the ...shortest-lived tetrapod whose life-time mating opportunities are restricted to a few weeks. Given that these chameleons grow to sexual maturity within about three months and that all individuals die soon after breeding, their mating strategies should be adapted to these temporal constraints. The reproductive tactics of this or any other Malagasy chameleon species have not been studied, however. Radio-tracking and observations of 21 females and 18 males revealed that females exhibit high site fidelity, move small cumulative and linear distances, have low corresponding dispersal ratios and small occurrence distributions. In contrast, males moved larger distances in less predictable fashion, resulting in dispersal ratios and occurrence distributions 7–14 times larger than those of females, and males also had greater ranges of their vertical distribution. Despite synchronous hatching, males exhibited substantial inter-individual variation in body mass and snout-vent length that was significantly greater than in females, but apparently unrelated to their spatial tactics. Females mated with up to 6 individually-known mates, but frequent encounters with unmarked individuals indicate that much higher number of matings may be common, as are damaging fights among males. Thus, unlike perennial chameleons,
F. labordi
males do not seem to maintain and defend territories. Instead, they invest vastly more time and energy into locomotion for their body size than other species. Pronounced variation in key somatic traits may hint at the existence of alternative reproductive tactics, but its causes and consequences require further study. This first preliminary study of the mating system of a Malagasy chameleon indicates that, as in other semelparous tetrapods, accelerated life histories are tied to a mating system with intense contest and scramble competition among males.
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