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.

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.

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.

Parental care in male degus (Octodon degus) is flexible and contingent upon female care.

Parents in many animal species provide care to their offspring as a mechanism to enhance their own fitness. In mammals, this behavior is expressed mostly by the females, but also by males of some species. Proximally, rates of paternal offspring care have been linked to organizational and activational effects of testosterone. Specifically, intrauterine position of male fetuses is associated with differential exposure to testosterone, leading to development of males with different levels of masculinization (assessed through differences in the length of the anogenital distance (AGD). The relative roles played by organizational and activational effects of testosterone on male parental care remain unclear. In this study, we aimed to determine if male sex-biased uterine environment and testosterone levels across the breeding period explain variation in paternal care in the social rodent, Octodon degus. Neither quantity (time with the offspring) nor quality (frequency of grooming and retrieving) of paternal care was affected by male sex-biased uterine environment, nor did paternal care significantly differ across the different stages of male reproduction. In contrast, paternal care was associated with maternal care. Quantity of male care decreased with increasing quantity of maternal care, and quality of male care increased with increasing quality of maternal care. While serum testosterone did not differ between males with different sex-biased uterine environment, male testosterone tended to increase during mating and decrease when pregnant females or offspring were present.

Stress, sleep, and sex: A review of endocrinological research in Octodon degus.

The Common Degu (Octodon degus) is a small rodent endemic to central Chile. It has become an important model for comparative vertebrate endocrinology because of several uncommon life-history features - it is diurnal, shows a high degree of sociality, practices plural breeding with multiple females sharing natal burrows, practices communal parental care, and can easily be studied in the laboratory and the field. Many studies have exploited these features to make contributions to comparative endocrinology. This review summarizes contributions in four major areas. First are studies on degu stress responses, focusing on seasonal changes in glucocorticoid (GC) release, impacts of parental care on offspring GC responses, and fitness consequences of individual variations of GC responses. These studies have helped confirm the ecological relevance of stress responses. Second are studies exploring diurnal circadian rhythms of melatonin and sex steroids. These studies have formed important work translating circadian biology from nocturnal laboratory rodents to diurnal humans. Third are studies that exploit the open nature of degu natural habitat, combined with laboratory studies, to explore the impact of testosterone on agonistic behavior. Studies have focused primarily on male:male, female:female, male:female, and parental behaviors. Fourth, are contributions to the study of female masculinization from male siblings in the uterus. These studies have focused on both the behavioral consequences of masculinization and the impact of those behaviors on fitness. Taken together, the studies reviewed here have formed a strong foundation for further studies in the degu so that future studies can address how endocrinological components underlie new mechanistic connections to the ecological effects on behavior and fitness.

Masculinized females produce heavier offspring in a group living rodent.

Alternative morphotypes have been reported less frequently in females than in males. An exception to this rule is the gradient of phenotypical masculinization reported in some female mammals, in which feminized and masculinized females represent two opposite ends along this gradient. These phenotypical differences originate during prenatal development as the consequence of maternal effects. Feminized and masculinized females differ in several traits, including morphological, physiological, behavioural and reproductive traits. Differences previously reported in reproductive traits between feminized and masculinized females come mostly from mechanistic studies performed in the laboratory, and not necessarily on social species. As a result, it is unclear to what extent these reported differences between female alternative morphotypes materialize in wild, natural populations. We quantified the effect of female alternative morphotype on female reproductive traits in a natural population of Octodon degus, a highly social rodent. We assessed female alternative morphotype through a continuous gradient of anogenital distance. Thus, feminized females were close to the short end of anogenital distance, while masculinized females were close to the long end of this gradient. We also tested the hypothesis that the social environment interacts with female morphotype to influence female reproductive traits. In female degus, only body weight affected litter size, where heavier females weaned more offspring. Masculinized females delivered male-biased litters and weaned heavier offspring. Lastly, masculinized females gave birth later in the breeding season compared to feminized females. Contrary to previous claims, our findings do not support that masculinized females are less fertile than feminized females. Moreover, masculinized females produced heavier, potentially higher quality offspring compared with feminized females.

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.

Social structure in a family group of Guanaco (Lama guanicoe, Ungulate): is female hierarchy based on 'prior attributes' or 'social dynamics'?

Social life involves costs and benefits mostly associated with how individuals interact with each other. The formation of hierarchies inside social groups has evolved as a common strategy to avoid high costs stemming from social interactions. Hierarchical relationships seem to be associated with different features such as body size, body condition and/or age, which determine dominance ability ('prior attributes' hypothesis). In contrast, the 'social dynamic' hypothesis suggests that an initial social context is a determinant in the formation of the hierarchy, more so than specific individual attributes. Hierarchical rank places individuals in higher positions, which presumably increases resource accessibility to their benefit, including opportunities for reproduction. We evaluate the maintenance of hierarchy in a family group of guanacos (Lama guanicoe) and evaluate the possible mechanisms involved in the stability of these interactions and their consequences. We estimate the linearity of social hierarchy and their dynamics. We find evidence of the formation of a highly linear hierarchy among females with males positioned at the bottom of the hierarchy. This hierarchy is not affected by physical characteristics or age, suggesting that it is established only through intra-group interactions. Rank is not related with calves' weight gain either; however, subordinated females, with lower rank, exhibit higher rates of allosuckling. We found no evidence of hierarchical structure in calves suggesting that hierarchical relationship in guanacos could be established during the formation of the family group. Hence, our results suggest that hierarchical dynamics could be related more to social dynamics than to prior attributes. We finally discuss the importance of hierarchies established by dominance and their role in minimizing social costs of interactions.