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.

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.

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.