Loren D. Hayes

An evolutionary framework for studying mechanisms of social behavior

Social interactions are central to most animals and have a fundamental impact upon the phenotype of an individual. Social behavior (social interactions among conspecifics) represents a central challenge to the integration of the functional and mechanistic bases of complex behavior. Traditionally, studies of proximate and ultimate elements of social behavior have been conducted by distinct groups of researchers, with little communication across perceived disciplinary boundaries. However, recent technological advances, coupled with increased recognition of the substantial variation in mechanisms underlying social interactions, should compel investigators from divergent disciplines to pursue more integrative analyses of social behavior. We propose an integrative conceptual framework intended to guide researchers towards a comprehensive understanding of the evolution and maintenance of mechanisms governing variation in sociality.

Fitness consequences of group living in the degu Octodon degus, a plural breeder rodent with communal care

The fitness consequences of plural breeding vary considerably among social vertebrates. We tested three hypotheses for the direct reproductive fitness consequences of group living in the degu Octodon degus, a social rodent endemic to central Chile. To test the ‘benefits of communal care’ hypothesis, we determined the relationship between the number of females per group, per capita direct fitness and offspring survival. To test the ‘food abundance and quality’ hypothesis, we determined the relationship between the biomass of preferred foods at burrow systems, group size, per capita direct fitness and offspring survival. To test the ‘predation risk’ hypothesis, we determined the relationship between group size, the density of burrow entrances to which social groups had access, per capita direct fitness, and survival of adults and offspring. Group size of core females (i.e. those with 50% or more nightly overlap) was negatively correlated with per capita direct fitness, but not with the number of females per group or total group size. Group living did not enhance the survival of offspring. Greater biomass of food (at 3 m and 9 m) and burrow density were not linked to larger groups and offspring survival. Our results did not support predictions of the ‘benefits of communal care’, ‘food abundance and quality’ or ‘predation risk’ hypothesis. Pending microsatellite analyses, we hypothesize that survival benefits linked to foraging group size and not reproductive fitness benefits may explain the evolution of sociality in degus.

Toward an integrative understanding of social behavior: New models and new opportunities

Social interactions among conspecifics are a fundamental and adaptively significant component of the biology of numerous species. Such interactions give rise to group living as well as many of the complex forms of cooperation and conflict that occur within animal groups. Although previous conceptual models have focused on the ecological causes and fitness consequences of variation in social interactions, recent developments in endocrinology, neuroscience, and molecular genetics offer exciting opportunities to develop more integrated research programs that will facilitate new insights into the physiological causes and consequences of social variation. Here, we propose an integrative framework of social behavior that emphasizes relationships between ultimate-level function and proximate-level mechanism, thereby providing a foundation for exploring the full diversity of factors that underlie variation in social interactions, and ultimately sociality. In addition to identifying new model systems for the study of human psychopathologies, this framework provides a mechanistic basis for predicting how social behavior will change in response to environmental variation. We argue that the study of non-model organisms is essential for implementing this integrative model of social behavior because such species can be studied simultaneously in the lab and field, thereby allowing integration of rigorously controlled experimental manipulations with detailed observations of the ecological contexts in which interactions among conspecifics occur.

Reproductive correlates of social network variation in plurally breeding degus (Octodon degus)

Studying the causes and reproductive consequences of social variation can provide insight into the evolutionary basis of sociality. Individuals are expected to behave adaptively to maximize reproductive success, but reproductive outcomes can also depend on group structure. Degus (Octodon degus) are plurally breeding rodents, in which females allonurse indiscriminately. However, communal rearing does not appear to enhance female reproductive success, and larger group sizes are correlated with decreasing per capita pup production. To further investigate mechanisms underlying these patterns, we asked how differences in sex, season and average group reproductive success are related to degu association networks. We hypothesized that if reproductive differences mirror social relationships, then females (core group members) should show stronger and more stable associations than males, and female association strength should be strongest during lactation. We also hypothesized that, at the group level, social cohesion would increase reproductive output, while social conflict would decrease it. Females did have higher association strength and more preferred partners than males, but only during lactation, when overall female associations increased. Females also had more stable preferred social partnerships between seasons. A measure of social cohesion (average association strength) was not related to per capita pup production of female group members, but potential social conflict (heterogeneity of association strengths) was negatively related to per capita pup production of female group members. Our results highlight temporal and multilevel patterns of social structure that may reflect reproductive costs and benefits to females.

Sociality, glucocorticoids and direct fitness in the communally rearing rodent, Octodon degus

While ecological causes of sociality (or group living) have been identified, proximate mechanisms remain less clear. Recently, close connections between sociality, glucocorticoid hormones (cort) and fitness have been hypothesized. In particular, cort levels would reflect a balance between fitness benefits and costs of group living, and therefore baseline cort levels would vary with sociality in a way opposite to the covariation between sociality and fitness. However, since reproductive effort may become a major determinant of stress responses (i.e., the cort-adaptation hypothesis), cort levels might also be expected to vary with sociality in a way similar to the covariation between sociality and fitness. We tested these expectations during three years in a natural population of the communally rearing degu, Octodon degus. During each year we quantified group membership, measured fecal cortisol metabolites (a proxy of baseline cort levels under natural conditions), and estimated direct fitness. We recorded that direct fitness decreases with group size in these animals. Secondly, neither group size nor the number of females (two proxies of sociality) influenced mean (or coefficient of variation, CV) baseline cortisol levels of adult females. In contrast, cortisol increased with per capita number of offspring produced and offspring surviving to breeding age during two out of three years examined. Together, our results imply that variation in glucocorticoid hormones is more linked to reproductive challenge than to the costs of group living. Most generally, our study provided independent support to the cort-adaptation hypothesis, according to which reproductive effort is a major determinant, yet temporally variable, influence on cort-fitness covariation.

The influence of group size on natal dispersal in the communally rearing and semifossorial rodent, Octodon degus

In social or group living species, members of groups are expected to be affected differentially by competition through the effect of group size (i.e., the “social competition hypothesis”). This hypothesis predicts an increase in the probability of dispersal with increasing size of social groups. At a more mechanistic level and based on the known effects of competition on stress hormone levels, a positive relationship between group size and glucocorticoids of juveniles should be observed. We used a demographic approach to test these predictions on a natural population of the communally rearing and semifossorial rodent—Octodon degus. Burrow systems provide degus with places to rear offspring and to evade stressful thermal conditions and predators. Thus, we predicted dispersal to increase with increasing number of degus per main burrow system used, a measure of habitat saturation in degus. The probability of dispersal increased with increasing number of degus per main burrow system used. Mean fecal metabolites of cortisol in offspring increased, yet not statistically significantly, with the number of juveniles in groups. These results were consistent with a scenario in which competition drives natal dispersal in juveniles in social degus. In particular, competition would be the consequence of high degu abundance in relation to the abundance of burrow systems available at the time of offspring emergence.

Direct fitness of group living mammals varies with breeding strategy, climate and fitness estimates

1. Understanding how variation in fitness relates to variation in group living remains critical to determine whether this major aspect of social behaviour is currently adaptive. 2. Available evidence in social mammals aimed to examine this issue remains controversial. Studies show positive (i.e. potentially adaptive), neutral or even negative fitness effects of group living. 3. Attempts to explain this variation rely on intrinsic and extrinsic factors to social groups. Thus, relatively more positive fitness effects are predicted in singularly breeding as opposed to plural breeding species. Fitness effects of sociality in turn may depend on ecological conditions (i.e. extrinsic factors) that influence associated benefits and costs. 4. We used meta-analytic tools to review how breeding strategy or ecological conditions influence the effect size associated with direct fitness-sociality relationships reported in the mammalian literature. Additionally, we determined how taxonomic affiliation of species studied, different fitness and sociality measures used, and major climatic conditions of study sites explained any variation in direct fitness effect size. 5. We found group living had modest, yet positive effects on direct fitness. This generally adaptive scenario was contingent not only upon breeding strategy and climate of study sites, but also on fitness measures examined. Thus, positive and significant effects characterized singular as opposed to plural breeding strategies. 6. We found more positive fitness effects on studies conducted in tropical as opposed to temperate or arid climates. More positive and significant effects were noted on studies that relied on group fecundity, male fecundity and offspring survival as measures of fitness. 7. To conclude, direct fitness consequences of mammalian group living are driven by interspecific differences in breeding strategy and climate conditions. Other factors not examined in this study, namely individual variation in direct and indirect fitness benefits and potential interactions between social and ecological conditions, may be important and require further studies.

On the dynamics of rodent social groups

A prevailing view is that animal social groups are largely determined by natal philopatry. However, other processes can influence the dynamics of social groups, including emigration of individuals that join pre-existing groups. Given that fitness consequences of living in a group may vary depending on how groups changes, the extent to which alternative mechanisms drive social dynamics is an important theme to the evolution of sociality. We considered the available literature on social rodents to examine (i) whether the available evidence supports single versus multiple mechanisms, (ii) how strongly evidence supports a major importance of natal philopatry, and (iii) whether mechanisms of group formation are linked to the reproductive strategy across species. While natal philopatry is considered the major process behind group dynamics in 26% of species examined, studies on 74% of species indicate two or more mechanisms take place simultaneously. Natal philopatry is considered a primary mechanism in communal (56%) and singular breeders (70%), but less so in solitary breeders (18%). Thus, the tenet that natal philopatry is the main process driving group dynamics in rodents may be premature, and studies aimed at examining the importance of alternative mechanisms are justified.

Fecal cortisol levels predict breeding but not survival of females in the short-lived rodent, Octodon degus

The cort-adaptation hypothesis indicates that an association between glucocorticoid (cort) levels and fitness may vary with the extent to which reproduction or breeding effort is a major determinant of cort levels. Support for a context dependent association between cort and fitness comes mostly from relatively long-lived, bird species. We tested the hypothesis that there are gender and context (life-history) specific cort-fitness relationships in degus, a short-lived and generally semelparous social rodent. In particular, we used demographical records on a natural population to estimate adult survival through seasons and years and linked that to records of baseline cort (based on fecal cortisol metabolites). We found no evidence for a direct relationship between baseline cort and adult survival across seasons, and this lack of association was recorded irrespective of sex and life history stage. Yet, cort levels during early lactation predicted the probability that females produce a second litter during the same breeding season, supporting a connection between baseline cort levels and breeding effort. Overall, the differential effects of cort on survival and breeding supported that the extent of cort-fitness relationships depends on the fitness component examined.

Burrow limitations and group living in the communally rearing rodent, Octodon degus

Abstract Group living is thought to evolve whenever individuals attain a net fitness advantage due to reduced predation risk or enhanced foraging efficiency, but also when individuals are forced to remain in groups, which often occurs during high-density conditions due to limitations of critical resources for independent breeding. The influence of ecological limitations on sociality has been studied little in species in which reproduction is more evenly shared among group members. Previous studies in the caviomorph rodent Octodon degus (a New World hystricognath) revealed no evidence that group living confers an advantage and suggest that burrow limitations influence formation of social groups. Our objective was to examine the relevance of ecological limitations on sociality in these rodents. Our 4-year study revealed no association between degu density and use of burrow systems. The frequency with which burrow systems were used by degus was not related to the quality of these structures; only in 1 of the 4 years did the frequency of burrow use decrease with decreasing abundance of food. Neither the number of females per group nor total group size (related measures of degu sociality) changed with yearly density of degus. Although the number of males within social groups was lower in 2008, this variation was not related clearly to varying density. The percentage of females in social groups that bred was close to 99% and did not change across years of varying density. Our results suggest that sociality in degus is not the consequence of burrow limitations during breeding. Whether habitat limitations contribute to variation in vertebrate social systems is discussed.