Luis A. Ebensperger

A review of the evolutionary causes of rodent group-living

I analyze and summarize the empirical evidence supporting alternative hypotheses posed to explain the evolution of rodent group-living. Eight hypotheses are considered: two rely on net fitness benefits to individuals, five rely on ecological and life-history constraints, and one uses elements of both. I expose the logic behind each hypothesis, identify its key predictions, examine how the available evidence on rodent socioecology supports or rejects its predictions, and identify some priorities for future research. I show that empirical support for most hypotheses is meager due to a lack of relevant studies. Also, empirical support for a particular hypothesis, when it exists, comes from studies of the same species used to formulate the original hypothesis. Two exceptions are the hypothesis that individual rodents live in groups to reduce their predation risk and the hypothesis that group-living was adopted by individuals to reduce their cost of thermoregulation. Finally, most hypotheses have been examined without regard to competing hypotheses and often in a restricted taxonomic context. This is clearly an unfortunate situation given that most competing hypotheses are not mutually exclusive. I suggest that in the future comparative approaches should be used. These studies should examine simultaneously the relevance of different benefits and constraints hypothesized to explain the evolution of rodent sociality.

Communal burrowing in the hystricognath rodent, Octodon degus: a benefit of sociality?

Abstract We examined the hypothesis that a main benefit of group-living in the semifossorial rodent, Octodon degus (Rodentia: Octodontidae), is to decrease individual cost of burrow construction. We contrasted the digging behavior of groups of three same-sex, adult-sized individuals with that of solitary degus. The behavior of singles and trios was recorded inside a large terrarium partially filled with natural soil and under controlled conditions of food, light, and temperature. The observation that degus in groups do not decrease their burrowing time or frequency of digging compared with solitary diggers does not support the hypothesis that communal burrowing is a primary cause of degu sociality. On the other hand, the observation that degus in groups removed significantly more soil per capita than solitary digging degus, and that grouped individuals coordinated their digging – group members burrowed mostly in the same sites and formed digging chains –, suggests that social burrowing may potentially reduce the cost of burrow construction in the long term. We suggest that such long-term benefits will be a consequence rather than a cause of degu group-living.

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.

An experimental examination of the consequences of communal versus solitary breeding on maternal condition and the early postnatal growth and survival of degu, Octodon degus, pups

Individuals of numerous rodent species engage in group living, in which they share an area of activity, a nest (or den), and interact more frequently with group members than with individuals from other such groups. Members of social groups may engage in communal breeding when they rear their young together in a common nest. We conducted an experimental study under laboratory conditions to explore the costs and benefits linked to early postnatal investment in offspring by female degus. In particular, we examined the quality and quantity of offspring produced by females rearing their litters in the presence of a second lactating (related or unrelated) female (‘communally breeding’) with offspring produced by lactating females in the presence of a nonbreeding (related or unrelated) female (‘singularly breeding’), and the offspring of solitary females. The physical condition of mothers (mass lost through lactation) was also examined. We studied 70 female degus and their litters, and 13 additional nonbreeding females, under constant conditions of adult density, nest availability, restricted food availability and breeding experience of subjects. The number of pups, the mass of pups, and the physical condition of mothers breeding communally did not differ from those of singularly and solitarily breeding females. Similar results were obtained when kinship of breeding females was considered. When reproductive performance of individuals within communally breeding groups was examined, we found that costs and benefits were not shared equally. Weanlings of litters born in the presence of a previous litter were smaller and less numerous than weanlings of litters born when no other young were present. Taken together, our results show that female degus derive no apparent reproductive benefits from early postnatal rearing of their offspring. Moreover, a proportion of females seem to pay a net cost.

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.

Do female degus communally nest and nurse their pups

Abstract. We examined the nesting and nursing behavior of females of the caviomorph rodent Octodon degus. We recorded the behavior of two, three-female groups of lactating degus kept in captivity and compared it with that of singly housed lactating females. Grouped females spontaneously nested communally. Five of six lactating females had non-offspring pups hanging from their teats, which suggests that some non-offspring nursing took place. Non-mothers increased their maternal behavior after the delivery of their own pups. Although time allocated to parental care by each communally nesting dam did not differ from that of solitary lactating females, young of communal litters spent less time alone and enjoyed more time cared for by a lactating female than young of single dams.

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.

Digestive and Metabolic Flexibility Allows Female Degus to Cope with Lactation Costs

Lactation is the most energetically demanding period in the life cycle of female mammals, and its effects on digestive flexibility and the size of internal organs have been extensively studied in laboratory mice and rats since the early 1900s. However, there have been only two studies on this topic for wild rodent species. Here, we analyzed digestive flexibility—that is, changes in gut content, activity of digestive enzymes, and gut morphology—during lactation in the caviomorph rodent Octodon degus. In addition, we evaluated changes in the size of other internal organs and analyzed their relationship with the resting metabolic rate. We found that gut content, the dry masses of digestive chambers, the dry mass of liver, and resting metabolic rate were greater in lactating than in nonbreeding control females. In contrast, fat stores were higher in control subjects. Maltase and aminopeptidase‐N specific activity did not change with lactation, and both enzymes had greater activity values in the middle portion of the small intestine. Thus, our data indicate that the previously reported increase in food assimilation that occurs during lactation in O. degus is related to a mass increase in several central organs, leading, in turn, to higher energetic costs. Fat stores may help to mitigate these costs, but, as expected for small animals, to a limited extent. Our study reveals a complex interplay among energy acquisition, storage, and expenditure processes that ultimately determine an organism’s fitness.

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.