The role of prey size and abundance in the geographical distribution of spider sociality

1. Social species in the spider genus Anelosimus predominate in lowland tropical rainforests, while congeneric subsocial species occur at higher elevations or higher latitudes. 2. We conducted a comparative study to determine whether differences in total biomass, insect size or both have been responsible for this pattern. 3. We found that larger average insect size, rather than greater overall biomass per se, is a key characteristic of lowland tropical habitats correlating with greater sociality. 4. Social species occupied environments with insects several times larger than the spiders, while subsocial species nearing dispersal occupied environments with smaller insects in either high or low overall biomass. 5. Similarly, in subsocial spider colonies, individuals lived communally at a time when they were younger and therefore smaller than the average insect landing on their webs. 6. We thus suggest that the availability of large insects may be a critical factor restricting social species to their lowland tropical habitats.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Maternal effect genes and the evolution of sociality in haplo-diploid organisms

Maternal care and female-biased sex ratios are considered by many to be essential prerequisites for the evolution of eusocial behaviors among the hymenoptera. Using population genetic models, I investigate the evolution of genes that have positive maternal effects but negative, direct effects on offspring fitness. I find that, under many conditions, such genes evolve more easily in haplo-diploids than in diplo-diploids. In fact, the conditions are less restrictive than those of kin selection theory, which postulate genes with negative direct effects but positive sib-social effects. For example, the conditions permitting the evolution of maternal effect genes are not affected if females mate multiply, whereas multiple mating reduces the efficacy of kin selection by reducing genetic relatedness within colonies. Inbreeding also differentially facilitates evolution of maternal effect genes in haplo-diploids relative to diplo-diploids, although it does not differentially affect the evolution of sib-altruism genes. Furthermore, when the direct, deleterious pleiotropic effect is restricted to sons, a maternal effect gene can evolve when the beneficial maternal effect is less than half (with inbreeding, much less) of the deleterious effect on sons. For kin selection, however, the sib-social benefits must always exceed the direct costs because genetic relatedness is always less than or equal to 1.0. The results suggest that haplo-diploidy facilitates (1) the evolution of maternal care, and (2) the evolution of maternal effect genes with antagonistic pleiotropic effects on sons. The latter effect may help explain the tendency toward female-biased sex ratios in haplo-diploids, especially those with inbreeding. I conclude that haplo-diploidy not only facilitates the evolution of sister-sister altruism by kin selection but also facilitates the evolution of maternal care and female-biased sex ratios, two prerequisites for eusociality.     

Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies

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.     

The other facets of family life and their role in the evolution of animal sociality

Family life forms an integral part of the life history of species across the animal kingdom and plays a crucial role in the evolution of animal sociality. Our current understanding of family life, however, is almost exclusively based on studies that (i) focus on parental care and associated family interactions (such as those arising from sibling rivalry and parent‐offspring conflict), and (ii) investigate these phenomena in the advanced family systems of mammals, birds, and eusocial insects. Here, we argue that these historical biases have fostered the neglect of key processes shaping social life in ancestral family systems, and thus profoundly hamper our understanding of the (early) evolution of family life. Based on a comprehensive survey of the literature, we first illustrate that the strong focus on parental care in advanced social systems has deflected scrutiny of other important social processes such as sibling cooperation, parent–offspring competition and offspring assistance. We then show that accounting for these neglected processes – and their changing role over time – could profoundly alter our understanding of the origin and subsequent evolution of family life. Finally, we outline how this ‘diachronic’ perspective on the evolution of family living provides novel insights into general processes driving the evolution of animal sociality. Overall, we infer that the explicit consideration of thus‐far neglected facets of family life, together with their study across the whole diversity of family systems, are crucial to advance our understanding of the processes that shape the evolution of social life.     

Interplay between various aspects in social relationships of young rhesus monkeys: Dominance,agonistic help,and affiliation

Relationships between group-living primates depend strongly on their position in the group dominance hierarchy and on their relationships with other group members. The influence of various behaviours on social relationships of immature rhesus monkeys (Macaca mulatta) was investigated here. Dominance ranks were established and related to the degree of affiliation in a dyad. Older monkeys were mostly dominant to the younger ones, regardless of kinship. Subordinate monkeys left proximity of their dominant members more often than they were left by them both among siblings and non-siblings, but the effect of dominance rank on the amount of play initiation and grooming in a dyad differed between these two types of dyads. The amount of agonistic help two individuals provided for each other was low among immatures. Nevertheless, pairs of siblings gave help to each other in agonistic conflicts more often than non-siblings, and such help was more often reciprocated between siblings than between non-siblings. Help in agonistic conflicts was positively correlated with the amount of time monkeys spent playing, grooming, or in proximity. Adults tended to interfere less in conflicts of frequent sibling play partners or non-sibling grooming partners. No evidence was found for young monkeys to exchange reciprocally grooming for agonistic help. It is argued that the time monkeys spend interacting with each other in affiliative interactions increases their familiarity and thus promotes close relationships between them. On the whole, young monkeys' relationships, like those between adults, are influenced strongly by their kinship, and position in the dominance hierarchy.     

Synthesizing perspectives on the evolution of cooperation within and between species

Cooperation is widespread both within and between species, but are intraspecific and interspecific cooperation fundamentally similar or qualitatively different phenomena? This review evaluates this question, necessary for a general understanding of the evolution of cooperation. First, we outline three advantages of cooperation relative to noncooperation (acquisition of otherwise inaccessible goods and services, more efficient acquisition of resources, and buffering against variability), and predict when individuals should cooperate with a conspecific versus a heterospecific partner to obtain these advantages. Second, we highlight five axes along which heterospecific and conspecific partners may differ: relatedness and fitness feedbacks, competition and resource use, resource‐generation abilities, relative evolutionary rates, and asymmetric strategy sets and outside options. Along all of these axes, certain asymmetries between partners are more common in, but not exclusive to, cooperation between species, especially complementary resource use and production. We conclude that cooperation within and between species share many fundamental qualities, and that differences between the two systems are explained by the various asymmetries between partners. Consideration of the parallels between intra‐ and interspecific cooperation facilitates application of well‐studied topics in one system to the other, such as direct benefits within species and kin‐selected cooperation between species, generating promising directions for future research.     

Between-group competition and human cooperation

A distinctive feature of human behaviour is the widespread occurrence of cooperation among unrelated individuals. Explaining the maintenance of costly within-group cooperation is a challenge because the incentive to free ride on the efforts of other group members is expected to lead to decay of cooperation. However, the costs of cooperation can be diminished or overcome when there is competition at a higher level of organizational hierarchy. Here we show that competition between groups resolves the paradigmatic 'public goods' social dilemma and increases within-group cooperation and overall productivity. Further, group competition intensifies the moral emotions of anger and guilt associated with violations of the cooperative norm. The results suggest an important role for group conflict in the evolution of human cooperation and moral emotions.     

Social Contact Following Severe Aggression in Rhesus Macaques (Macaca mulatta): A New Test of the Consolation Hypothesis

Previous studies on macaque species revealed no evidence of consolation: affiliative contact between the loser of an aggressive interaction and a third party. However, typically, the researchers used short observation periods and latency to make first affiliative contact as a dependent measure. Based on social stress buffering literature, I predicted that by employing longer observation periods and percentage of time in affiliative contact as a dependent measure, I would be more likely to detect increases in affiliative contact following aggression. I observed adult female rhesus macaques for 1 hr after they received severe aggression and for 1 hr after some affiliative contact, and measured time spent in affiliative contact using instantaneous recording at 30-sec intervals. Contrary to prediction, victims of attack did not spend a greater percentage of time in affiliative contact postaggression as compared to postaffiliation. Subjects were also less likely to initiate contact with other individuals and were more likely to have contact with individuals that were dominant to their aggressor, following aggression. These results provide converging evidence that affiliative contact is not increased following aggression in macaques. I discuss the failure to bear out the predictions based on the social stress buffering literature in terms of rhesus social dynamics, the nature of aggression as a stressor, and possible mechanisms for the social stress buffering effect.     

Proximate mechanisms and evolution of caste polyphenism in social insects: From sociality to genes

Evidence has accumulated over several decades to prove the kin selection theory of evolution of social insects, however, proximate mechanisms of social behavior, and/or caste differentiation remain obscure. Genes that regulate these mechanisms are apparently selected through kin selection, and organisms have consequently acquired sociality. Here, I will discuss several studies that were performed recently by Matsumoto Laboratory, University of Tokyo, Tokyo, Japan, in various social insects, such as termites and ants, in order to reveal the regulatory mechanisms of social behavior and the evolutionary processes of sociality. First, I will review the foraging behavior of the black marching termite Hospitalitermes medioflavus, where well-organized task allocation among castes is apparent. This suggests that regulation of postembryonic development is important in social behavior. Next, I will summarize recent progress in identifying caste-specific gene expression in the damp-wood termite Hodotermopsis sjostedti. This constitutes the basis for molecular mechanisms of caste differentiation, and moreover, the genes identified might be good markers for social evolution. Finally, the mechanism underlying winglessness in ant workers is reviewed. Apoptotic cell death was detected at the stage of pupation in wingless worker castes. Furthermore, the areas of study recently designated as sociogenomics and ecological developmental biology are discussed.     

Genetic differentiation and the evolution of cooperation in chimpanzees and humans

It has been proposed that human cooperation is unique among animals for its scale and complexity, its altruistic nature and its occurrence among large groups of individuals that are not closely related or are even strangers. One potential solution to this puzzle is that the unique aspects of human cooperation evolved as a result of high levels of lethal competition (i.e. warfare) between genetically differentiated groups. Although between-group migration would seem to make this scenario unlikely, the plausibility of the between-group competition model has recently been supported by analyses using estimates of genetic differentiation derived from contemporary human groups hypothesized to be representative of those that existed during the time period when human cooperation evolved. Here, we examine levels of between-group genetic differentiation in a large sample of contemporary human groups selected to overcome some of the problems with earlier estimates, and compare them with those of chimpanzees. We find that our estimates of between-group genetic differentiation in contemporary humans are lower than those used in previous tests, and not higher than those of chimpanzees. Because levels of between-group competition in contemporary humans and chimpanzees are also similar, these findings suggest that the identification of other factors that differ between chimpanzees and humans may be needed to provide a compelling explanation of why humans, but not chimpanzees, display the unique features of human cooperation.     

Reply to Lawler: feeding competition, cooperation, and the causes of primate sociality

This is a reply to Richard Lawler's commentary on our previous work [Lawler, 2011; this issue] in which he develops a set of operational models to test socioecological theories of the evolutionary importance of feeding competition. We strongly agree that we need to critically re-evaluate the basic assumptions of all models of primate sociality, and to verify the explanatory power of alternative models. We also feel Lawler's commentary provides an important opportunity to broaden the debate concerning the fundamental roles of cooperation, competition, and aggression in understanding primate social systems. Lawler provides a number of suggestions as to how models developed in primate socioecology might be tested. We agree with these suggestions, make further suggestions, and call for specific operational definitions so that researchers might begin to develop and test various methodologies. However, we also call for testing alternative theories. Current socioecological theory is based on the assumption that competition and positive selection is always in operation and has driven the evolution of living organisms. We believe that this "explanation of choice" often is treated as an assumed truth to which data are forced to fit, rather than being seen as a theory to be tested. Furthermore, we agree with Weiss and Buchanan [2009. The Mermaid's Tale: Four Billion Years of Cooperation in the Making of Living Things] that on ecological and developmental scales, where organisms actually live out their lives, cooperation may play a more fundamental role than competition.     

Variability in the estimation of ungulate group sizes complicates ecological inference

1. Foundational work has examined adaptive social behavior in animals in relation to the costs and benefits of group living. Within this context, a “group” of animals represents an organizational unit that is integral to the study of animal ecology and evolution.
2. Definitions of animal group sizes are often subjective with considerable variability within and across species. However, investigations of both the extent and implications of such variability in the estimation of animal group sizes are currently lacking.
3. Selecting ungulates as a case study, we conducted a literature review to assess prevailing practices used to determine group sizes among terrestrial Cetartiodactyla and Perissodactyla. Via this process, we examined group size definitions for 61 species across 171 peer‐reviewed studies published between 1962 and 2018.
4. These studies quantified group sizes via estimation of ungulate aggregations in space and time. Spatial estimates included a nearest neighbor distance ranging from 1.4 m to 1,000 m, and this variation was partially explained by a weak positive correlation (|r| = .4, p < .003) with the body size of the ungulate research subjects. The temporal extent over which group size was estimated was even broader, ranging from three minutes to 24 hr.
5. The considerable variability in ungulate group size estimation that we observed complicates efforts to not only compare and replicate studies but also to evaluate underlying theories of group living. We recommend that researchers: (a) clearly describe the spatiotemporal extents over which they define ungulate group sizes, (b) highlight foundational empirical and ecological rationale for these extents, and (c) seek to align such extents among individual species so as to facilitate cross‐system comparisons of ungulate group size dynamics. We believe an integrative approach to ungulate group size estimation would readily facilitate replication, comparability, and evaluation of competing hypotheses examining the tradeoffs of animal sociality.

     

Ecological generalism facilitates the evolution of sociality in snapping shrimps

Evidence from insects and vertebrates suggests that cooperation may have enabled species to expand their niches, becoming ecological generalists and dominating the ecosystems in which they occur. Consistent with this idea, eusocial species of sponge‐dwelling Synalpheus shrimps from Belize are ecological generalists with a broader host breadth and higher abundance than non‐eusocial species. We evaluate whether sociality promotes ecological generalism (social conquest hypothesis) or whether ecological generalism facilitates the transition to sociality (social transition hypothesis) in 38 Synalpheus shrimp species. We find that sociality evolves primarily from host generalists, and almost exclusively so for transitions to eusociality. Additionally, sponge volume is more important for explaining social transitions towards communal breeding than to eusociality, suggesting that different ecological factors may influence the independent evolutionary origins of sociality in Synalpheus shrimps. Ultimately, our results are consistent with the social transition hypothesis and the idea that ecological generalism facilitates the transition to sociality.     

Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques.

Social housing, whether continuous, intermittent, or partial contact, typically provides many captive primates with opportunities to express affiliative behaviors, important components of the species-typical behavioral repertoire. Positive reinforcement training techniques have been successfully employed to shape many behaviors important for achieving primate husbandry goals. The present study was conducted to determine whether positive reinforcement training techniques could also be employed to alter levels of affiliative interactions among group-housed rhesus macaques. Twenty-eight female rhesus were divided into high (n = 14) and low (n = 14) affiliators based on a median split of the amount of time they spent affiliating during the baseline phase of the study. During the subsequent training phase, half of the low affiliators (n = 7) were trained to increase their time spent affiliating, and half of the high affiliators (n = 7) were trained to decrease their time spent affiliating. Trained subjects were observed both during and outside of training sessions. Low affiliators significantly increased the amount of time they spent affiliating, but only during nontraining sessions. High affiliators on the other hand, significantly decreased the amount of time they spent affiliating, but only during training sessions. These data suggest that positive reinforcement techniques can be used to alter the affiliative behavior patterns of group-housed, female rhesus monkeys, although the two subgroups of subjects responded differently to the training process. Low affiliators changed their overall behavioral repertoire, while high affiliators responded to the reinforcement contingencies of training, altering their proximity patterns but not their overall behavior patterns. Thus, positive reinforcement training can be used not only as a means to promote species-typical or beneficial behavior patterns, but also as an important experimental manipulation to facilitate systematic analyses of the effects of psychosocial factors on behavior and potentially even immunology.     

Acute changes in social composition and agonistic behavior in male vervet monkeys (Cercopithecus aethiops sabaeus)

Among nonhuman primates the composition of social groups influences the interactions of group members. We assessed the effects of acute changes in social composition on behavior among 15 adult male vervet monkeys (Cercopithecus aethiops sabaeus). Subjects were observed in their basal social groups which comprised 3 adult males, 2–4 adult females, and offspring; and in two subgroups consisting of either two or three adult males. Agonism and vigilance increased in smaller groups relative to basal conditions, while subjects in two-male groups displayed more aggression than those in three-male groups. These findings suggest that, among male vervet monkeys, acute disruption of stable social groups increases aggressive behavior, and that the amount of agonism is influenced by the composition of the consequent subgroups. © 1992 Wiley-Liss, Inc.     

The social evolution of dispersal with public goods cooperation

Selection can favour the evolution of individually costly dispersal if this alleviates competition between relatives. However, conditions that favour altruistic dispersal also mediate selection for other social behaviours, such as public goods cooperation, which in turn is likely to mediate dispersal evolution. Here, we investigate – both experimentally (using bacteria) and theoretically – how social habitat heterogeneity (i.e. the distribution of public goods cooperators and cheats) affects the evolution of dispersal. In addition to recovering the well‐known theoretical result that the optimal level of dispersal increases with genetic relatedness of patch mates, we find both mathematically and experimentally that dispersal is always favoured when average patch occupancy is low, but when average patch occupancy is high, the presence of public goods cheats greatly alters selection for dispersal. Specifically, when public goods cheats are localized to the home patch, higher dispersal rates are favoured, but when cheats are present throughout available patches, lower dispersal rates are favoured. These results highlight the importance of other social traits in driving dispersal evolution.     

Does Innovation Success Influence Social Interactions? An Experimental Test in House Sparrows

In group‐living animals, individuals may benefit from the presence of an innovative group‐mate because new resources made available by innovators can be exploited, for example by scrounging or social learning. As a consequence, it may pay off to take the group‐mates' problem‐solving abilities into account in social interactions such as aggression or spatial association, for example because dominance over an innovative group‐mate can increase scrounging success, while spatial proximity may increase the chance of both direct exploitation and social learning. In this study, we tested whether the individuals' innovation success influences their social interactions with group‐mates in small captive flocks of house sparrows (Passer domesticus). First, we measured the birds' actual problem‐solving success in individual food‐extracting tasks. Then, we manipulated their apparent problem‐solving success in one task (by allowing or not allowing them to open a feeder repeatedly) while a new, unfamiliar group‐member (focal individual) had the opportunity to witness their performance. After this manipulation, we observed the frequency and intensity of aggression and the frequency of spatial associations between the focal individuals and their manipulated flock‐mates. Although flock‐mates behaved according to their treatments during manipulations, their apparent problem‐solving success did not affect significantly the focal individuals' agonistic behaviour or spatial associations. These results do not support that sparrows take flock‐mates' problem‐solving abilities into account during social interactions. However, focal individuals attacked those flock‐mates more frequently that had higher actual problem‐solving success (not witnessed directly by the focal individuals), although aggression intensity and spatial association by the focal birds were unrelated to the flock‐mates' actual success. If this association between flock‐mates' actual innovativeness and focal individuals' aggression is not due to confounding effects, it may imply that house sparrows can use more subtle cues to assess the group‐mates' problem‐solving ability than direct observation of their performance in simple foraging tasks.     

Convergent evolution of kin-based sociality in a lizard

Studies of social birds and mammals have produced extensive theory regarding the formation and dynamics of kin-based social groups in vertebrates. However, comparing kin dynamics in birds and mammals to social reptiles provides the opportunity to identify selective factors that promote independent origins of kin sociality across vertebrates. We combined a 5-year mark-recapture study with a DNA microsatellite analysis of relatedness in a social lizard (Xantusia vigilis) to examine the formation and stability of kin groups. We found that these lizards are highly sedentary and that groups often form through the delayed dispersal of offspring. Groups containing juveniles had higher relatedness than adult-only groups, as juveniles were commonly found in aggregations with at least one parent and/or sibling. Groups containing nuclear family members were more stable than groups of less-related lizards, as predicted by social theory. We conclude that X. vigilis aggregations conform to patterns of kin sociality observed in avian and mammalian systems and represent an example of convergent evolution in social systems. We suggest that kin-based sociality in this and other lizards may be a by-product of viviparity, which can promote delayed juvenile dispersal by allowing prolonged interaction between a neonate and its mother.