Activational and organizational effects of testosterone on the number of mating partners and reproductive success in males of a social rodent.

The timing of exposure to the steroid hormone, testosterone, produces activational and organizational effects in vertebrates. These activational and organizational effects are hypothesized to relate with the number of female mating partners and reproductive success in males. We tested this hypothesis by examining 151 wild degu (Octodon degus) males across a 10-year study. We quantified the association between adult serum testosterone levels (i.e., an indirect index of adult activational effects) and anogenital distance (AGD) length (i.e., a direct index of fetal organizational effects), and their interaction on the number of female mating partners and reproductive success. We found no evidence of an association between adult male serum testosterone levels and the number of female mating partners, or between adult male serum testosterone levels and reproductive success. However, male AGD was positively associated with reproductive success, but not so with the number of female mating partners. Additionally, the positive association between male AGD and male reproductive success was mediated by the number of mates. Our findings do not support major roles of activational or organizational effects of testosterone on the number of female mating partners and its consequences on male reproductive success. Instead, our results suggest that compared with individual male attributes, the female social environment plays a more important role in driving male reproductive success.

Social environment and anogenital distance length phenotype interact to explain testosterone levels in a communally rearing rodent: Part 2: The female side.

Testosterone is known as a "male" hormone; however, females also synthetize testosterone, which influences female sexual and aggressive behavior. In female vertebrates, as in males, testosterone levels can vary seasonally. However, female testosterone levels may also be related with female anogenital distance (AGD) length phenotype (a proxy of prenatal androgen exposure), and the social group environment. We used data from a long-term rodent study (2009-2019) in a natural population of degus (Octodon degus) to examine the potential associations between female serum testosterone levels, season, female AGD phenotype, and social group composition. We quantified female serum testosterone levels during the mating and offspring rearing seasons, and we determined the number of females and males in social groups, as well the composition of groups, in terms of the AGD of the female and male group mates. Our results indicate that female testosterone levels vary with season, being highest during the offspring rearing season. Additionally, female testosterone levels were associated with the number of male group-members and the AGD of male group-members but were not associated with female social environment and focal female AGD phenotype. Together, our results suggest that female testosterone levels are sensitive to intersexual interactions. Our results also reveal that female and male testosterone levels do not differ between the sexes, a finding previously reported only in rock hyraxes. We discuss how the complex social system of degus could be driving this physiological similarity between the sexes.

Social environment and anogenital distance length phenotype interact to explain testosterone levels in a communally rearing rodent: Part 1: The male side.

In vertebrates, male testosterone levels vary across the year being generally higher during the mating season relative to the offspring rearing season. However, male testosterone levels may also be associated with male anogenital distance (AGD) length (a proxy of prenatal androgen exposition), and influenced by the social group environment. In social species, it has been proposed that high levels of testosterone could be incompatible with the development of an amicable social environment. Thus, in these species, it is predicted that males have relatively low levels of testosterone. Our goal was to examine the potential association between male serum testosterone levels, season, male AGD length, and the social environment in the rodent Octodon degus under natural conditions. We quantified male serum testosterone levels during the mating and offspring rearing seasons, and we determined the number of females and males in each social group, as well as the composition of groups, in terms of the AGD length of the female and male group mates, from 2009 to 2019. Our results revealed that male testosterone levels covary with season, being highest during the offspring rearing season. Additionally, male testosterone levels vary with male AGD length, and female and male social group environments. More importantly, male degus exhibit low levels of testosterone that are indistinguishable from female levels during offspring rearing season. Similar to other highly social mammals, where males and females live together year-round, male amicable behavior could be the best male mating strategy, thus leading to a reduction in circulating testosterone levels.

Socially unstable conditions experienced during development prime female Octodon degus to shape the phenotype of their own offspring.

Because residents and immigrants from group living species may experience fitness costs associated with permanent changes in group membership, we examined the hypothesis that females experiencing socially unstable or socially stable conditions during development compensate these costs by shaping the phenotype of their own offspring differently. Groups of adult females experiencing either socially stable or unstable conditions in the early social environment were assigned to either socially stable or unstable conditions in the social environment as adults. We quantified affiliative and agonistic interactions among the females during pregnancy and lactation of the focal female, maternal and allomaternal care, hypothalamic-anterior pituitary-adrenal axis (HPA) acute stress response, and early offspring growth. Social instability during breeding enhanced agonistic interactions among adult females, and offspring that experienced socially unstable conditions exhibited enhanced offspring care, regardless of adult environments. Neither social behavior, offspring care, acute stress physiology, nor early growth was influenced by early or adult social stability conditions. These findings imply that socially unstable conditions prime developing females to shape the phenotype of their offspring to prevent negative effects of socially unstable environments.

Intra-specific variation in social organization of Strepsirrhines.

Strepsirrhines, that is, lemurs, galagos, and lorises, are considered basal primates, making them important to understand the evolution of primate sociality. Apart from some lemurs, they are nocturnal and solitary living, though the view of their sociality nature has changed with field studies being completed. We conducted a review of the primary literature about the social organization (group composition) of strepsirrhines, with the aim to determine whether intra-specific variation in social organization (IVSO) occurs and to determine how many species are pair-living, group-living, or solitary living. We found data in 83 peer-reviewed studies for 43 of the 132 strepsirrhine species and compared our results using two databases on social systems of mammals published in 2011 and 2013. While it is often assumed that primates show relatively fixed social organizations, we found that 60.5% of species for which data exist have IVSO. We found only 7% of the species to be truly solitary living (with 34.9% additional species to be sometimes solitary living), which is in contrast to the other databases, which had reported 60.9% and 37.7% of species to be solitary. We further explored group compositions by designating "functional groups" (e.g., foraging, breeding, and infant care groups). While functional groups might explain IVSO within a single species, this was not consistent over species with IVSO, such that IVSO was poorly explained by functional groups. Our study supports the view that most strepsirrhines are social (58.1% of species with another 34.9% of species sometimes living in pairs or groups) and show complex and often variable social organizations; reinforcing the assumption that the ancestor of all primates was social and not solitary.

The modulating role of group stability on fitness effects of group size is different in females and males of a communally rearing rodent.

Group size may influence fitness benefits and costs that emerge from cooperative and competitive interactions in social species. However, evidence from plural breeding mammals indicates that group size is insufficient to explain variation in direct fitness, implying other attributes of social groups were overlooked. We studied the natural population of a social rodent during 5 years to test the hypothesis that social stability - in terms of group composition - modulates the effects of increasing number of breeding females (a proxy of communal rearing) and males on the number of offspring weaned (sired) and on the number of offspring weaned (sired) surviving to breeding age (two proxies of direct fitness). We quantified the effects of social stability (measured as changes in female or male group members between mating and the onset of lactation) on these fitness measures. We used live trapping, telemetry and DNA markers to determine social and fitness measures. Social stability in degus was variable in terms of the number of changes in group composition across groups. Low stability was mostly due to mortality and emigration of group members. Results supported a modulating role of social stability on the relationship between group size and the number of offspring weaned (sired). Stability in female and male group composition were both modulators of fitness to females and males. The modulatory role of stability was sex specific, where high social stability was often fitness beneficial to the females. Instead, low social stability was fitness enhancing to the males.

Maternal stress and plural breeding with communal care affect development of the endocrine stress response in a wild rodent.

Maternal stress can significantly affect offspring fitness. In laboratory rodents, chronically stressed mothers provide poor maternal care, resulting in pups with hyperactive stress responses. These hyperactive stress responses are characterized by high glucocorticoid levels in response to stressors plus poor negative feedback, which can ultimately lead to decreased fitness. In degus (Octodon degus) and other plural breeding rodents that exhibit communal care, however, maternal care from multiple females may buffer the negative impact on pups born to less parental mothers. We used wild, free-living degus to test this hypothesis. After parturition, we manipulated maternal stress by implanting cortisol pellets in 0%, 50-75%, or 100% of adult females within each social group. We then sampled pups for baseline and stress-induced cortisol, negative feedback efficacy, and adrenal sensitivity. From groups where all mothers were implanted with cortisol, pups had lower baseline cortisol levels and male pups additionally had weaker negative feedback compared to 0% or 50-75% implanted groups. Contrary to expectations, stress-induced cortisol did not differ between treatment groups. These data suggest that maternal stress impacts some aspects of the pup stress response, potentially through decreased maternal care, but that presence of unstressed mothers may mitigate some of these effects. Therefore, one benefit of plural breeding with communal care may be to buffer post-natal stress.

Seasonal variation in the degu (Octodon degus) endocrine stress response.

Many wild animals show seasonal variation in circulating levels of stress hormones. Seasonal changes in the stress response may help animals better cope with the different challenges faced during each life history stage. We determined the seasonal stress profile of wild, free-living degus in Chile. Female degus were sampled during non-breeding (January), mating/early gestation (July), late gestation (August), and lactation (1st litter-September, 2nd litter-January). Male degus were sampled during the first three time-points. We measured baseline cortisol (CORT), stress-induced CORT, and negative feedback efficacy using a dexamethasone suppression test. While we found that neither males nor females showed seasonal variation in baseline CORT or negative feedback levels, we did find significant seasonal variation in stress-induced CORT levels of both sexes. Male stress-induced CORT was lowest during mating while female stress-induced CORT was highest during late gestation and lactation. Overall, females had higher stress-induced CORT compared to males. Our data suggest that stress-induced levels of CORT are highest during periods with increased chance of stressor exposure or times of positive energy balance. Consequently, CORT responses to stress appear to be regulated according to different life history needs.

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.

Habitat type influences endocrine stress response in the degu (Octodon degus).

While many studies have examined whether the stress response differs between habitats, few studies have examined this within a single population. This study tested whether habitat differences, both within-populations and between-populations, relate to differences in the endocrine stress response in wild, free-living degus (Octodon degus). Baseline cortisol (CORT), stress-induced CORT, and negative feedback efficacy were measured in male and female degus from two sites and three habitats within one site during the mating/early gestation period. Higher quality cover and lower ectoparasite loads were associated with lower baseline CORT concentrations. In contrast, higher stress-induced CORT but stronger negative feedback efficacy were associated with areas containing higher quality forage. Stress-induced CORT and body mass were positively correlated in female but not male degus across all habitats. Female degus had significantly higher stress-induced CORT levels compared to males. Baseline CORT was not correlated with temperature at time of capture and only weakly correlated with rainfall. Results suggest that degus in habitats with good cover quality, low ectoparasite loads, and increased food availability have decreased endocrine stress responses.

Social consequences of rapid environmental change.

While direct influences of the environment on population growth and resilience are well studied, indirect routes linking environmental changes to population consequences are less explored. We suggest that social behavior is key for understanding how anthropogenic environmental changes affect the resilience of animal populations. Social structures of animal groups are evolved and emergent phenotypes that often have demographic consequences for group members. Importantly, environmental drivers may directly influence the consequences of social structure or indirectly influence them through modifications to social interactions, group composition, or group size. We have developed a framework to study these demographic consequences. Estimating the strength of direct and indirect pathways will give us tools to understand, and potentially manage, the effect of human-induced rapid environmental changes.

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.

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.

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.

Limited and fitness-neutral effects of resource heterogeneity on sociality in a communally rearing rodent.

Contrasting scenarios have been proposed to explain how resource heterogeneity influences group living or sociality. First, sociality may result from individuals in larger groups attaining net fitness benefits by monopolizing access to resources ("resource-defense" hypothesis). Second, sociality may be the fitness-neutral outcome of multiple individuals using a territory with sufficient resources to sustain a group of conspecifics ("resource-dispersion" hypothesis). While previous studies have tended to support the resource-dispersion hypothesis, these analyses have typically examined only 1 or a few predictions, making it difficult to distinguish between the 2 alternatives. We conducted a 4-year field study of Octodon degus to quantify the effects of spatial heterogeneity in food and refuge distributions on group size and 2 components of reproductive success (per capita number of offspring, offspring survival) in this plural breeding and communal rearing rodent. We found only a small effect of heterogeneity of food resources on group size; the effect food resource distribution on group territory size varied across years. Group size did not vary with spatial variation in group territory size and quality. Importantly, there was no covariation between group size and quality of an individual's territory (i.e., a measure of individual access to resources), or between this measure of territory quality and reproductive success, implying no resource-based benefits to social degus. Overall, our results were more consistent with fitness-neutral relationships among spatial heterogeneity of resources, sociality, and territory size. The resource-dispersion hypothesis, however, did not provide a complete explanation for degu socioecology. Se han propuesto distintas hipótesis para explicar cómo la heterogeneidad de los recursos afecta la vida en grupos, o sociabilidad. Esta puede surgir en situaciones donde individuos en grupos grandes se benefician al monopolizar el acceso a recursos (hipótesis de defensa de recursos). Por otra parte, la vida en grupos también puede ser el resultado neutro (en términos de adecuación) de individuos que comparten un territorio con recursos suficientes (hipótesis de dispersión de recursos). Aunque algunos estudios previos han validado la hipótesis de dispersión de recursos, estos solo han evaluado un número limitado de las predicciones de esta hipótesis, lo que ha dificultado distinguir entre esta y otras hipótesis alternativas. Durante un estudio de 4 años cuantificamos los efectos de la heterogeneidad espacial de alimento y distribución de refugios sobre el tamaño de grupo y dos componentes del éxito reproductivo (número per cápita de crías, supervivencia de las crías) en Octodon degus. Se registraron efectos relativamente pequeños de la heterogeneidad espacial del alimento sobre el tamaño de grupo, y variables entre años sobre el tamaño del territorio de cada grupo. El tamaño de grupo no fue afectado por la variación espacial en el tamaño y calidad del territorio de los grupos. No se registró co-variación entre el tamaño de los grupos y la calidad del territorio de cada individuo (una medida individual del acceso a recursos), o entre la calidad del territorio individual y el éxito reproductivo, lo que sugiere ausencia de beneficios derivados del uso social de recursos en degus. En general, los resultados fueron más consistentes con un escenario de efectos neutros de la heterogeneidad espacial de recursos sobre la sociabilidad. Sin embargo, la hipótesis de dispersión de recursos no explicó el conjunto de efectos (o su ausencia) asociados a la socioecología del degu.

Postnatal Development of the Degu (Octodon degus) Endocrine Stress Response Is Affected by Maternal Care.

Maternal stress and care significantly affect offspring's future behavior and physiology. Studies in laboratory rats have shown that maternal stress decreases maternal care and that low rates of certain maternal behaviors cause offspring to develop hyperreactive stress responses. Plurally breeding rodents that practice communal care, such as degus (Octodon degus), may be able to buffer some of these effects since offspring receive care from multiple females. Directly after parturition, 0% (Control group), 50% (Mixed group), or 100% (CORT group) per cage of pair-housed female degus were implanted with 21-day release cortisol pellets. The amount of maternal care provided by females was determined from video recordings during the next 3 weeks. Females with cortisol implants did not alter rates of maternal care. However, females recently introduced to captivity had low rates of pup contact and pup retrievals compared to females of captive origin. When pups reached 4 weeks of age, we determined their baseline and stress-induced cortisol levels, in addition to assessing their negative feedback efficacy and adrenal sensitivity. Pups from mothers recently introduced to captivity had weak negative feedback. Within captive pups, those from CORT mothers weighed less compared to pups from either Control or Mixed mothers. Captive CORT pups also had weak adrenal sensitivity compared to captive Control pups. These findings demonstrate that maternal care and glucocorticoid elevation impact certain components of the degu pup stress response, but that plural breeding with communal care may buffer some of these effects.

Immunocompetence of breeding females is sensitive to cortisol levels but not to communal rearing in the degu (Octodon degus).

One hypothesis largely examined in social insects is that cooperation in the context of breeding benefits individuals through decreasing the burden of immunocompetence and provide passive immunity through social contact. Similarly, communal rearing in social mammals may benefit adult female members of social groups by reducing the cost of immunocompetence, and through the transfer of immunological compounds during allonursing. Yet, these benefits may come at a cost to breeders in terms of a need to increase investment in individual immunocompetence. We examined how these potential immunocompetence costs and benefits relate to reproductive success and survival in a natural population of the communally rearing rodent, Octodon degus. We related immunocompetence (based on ratios of white blood cell counts, total and specific immunoglobulins of G isotype titers) and fecal glucocorticoid metabolite (FGC) levels of adults immunized with hemocyanin from the mollusk Concholepas concholepas to measures of sociality (group size) and communal rearing (number of breeding females). Offspring immunocompetence was quantified based on circulating levels of the same immune parameters. Neither female nor offspring immunocompetence was influenced by communal rearing or sociality. These findings did not support that communal rearing and sociality enhance the ability of females to respond to immunological challenges during lactation, or contribute to enhance offspring condition (based on immunocompetence) or early survival (i.e., to 3months of age). Instead, levels of humoral and cellular components of immunocompetence were associated with variation in glucorcorticoid levels of females. We hypothesize that this covariation is driven by physiological (life-history) adjustments needed to sustain breeding.

Taxon matters: promoting integrative studies of social behavior: NESCent Working Group on Integrative Models of Vertebrate Sociality: Evolution, Mechanisms, and Emergent Properties.

The neural and molecular mechanisms underlying social behavior - including their functional significance and evolution - can only be fully understood using data obtained under multiple social, environmental, and physiological conditions. Understanding the complexity of social behavior requires integration across levels of analysis in both laboratory and field settings. However, there is currently a disconnect between the systems studied in the laboratory versus the field. We argue that recent conceptual and technical advances provide exciting new opportunities to close this gap by making non-model organisms accessible to modern approaches in both laboratory and nature.

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.

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.