Cecilia León

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.

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.

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.

Nest and Space use in a Highland Population of the Southern Mountain Cavy (Microcavia australis)

Abstract We examined the spatial and social structure of a high-altitude population of the scarcely known southern mountain cavy (Microcavia australis) in Argentina. We used radiotelemetry techniques to monitor nest use at night and daily home ranges and examine whether southern mountain cavies form nesting associations that are socially cohesive groups. We further timed our observations to breeding time of our study population (September–November) to assess opportunities for communal breeding. The nighttime telemetry of 24 radiotagged cavies revealed 7 nesting associations (i.e., communal nesting). These included 1–4 breeding females and 1 or 2 breeding males. Nesting associations were stable in terms of identity of individual members and in the location of putative nest sites. Most associations used a single nest site, but some shared 2 or 3. We noted that all nest sites were located under dominant shrubs, but use of nest sites was unrelated to variation in shrub cover. Nest sites with more burrow entrances were more frequently used by radiocollared cavies. During the day, home ranges of cavies overlapped more with ranges of nest mates than with those of non–nest mates, implying that nesting groups were socially cohesive units. This study confirmed that southern mountain cavies are communally nesting, and, because communal nesting occurs during breeding time, our findings support the idea that cavies engage in communal care of young.

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.

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.

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.

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.

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

Maternal stress and care significantly affect offsprings 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.

Highly masculinized and younger males attain higher reproductive success in a social rodent

Alternative morphotypes have been reported in males of different taxa. In some mammals, highly masculinized and slightly masculinized males represent 2 opposite ends along a gradient of phenotypic variation in males. This phenotypical gradient originates during prenatal development. Laboratory studies have documented how highly and slightly masculinized males differ in several traits, including their reproductive success. However, the extent to which these reported differences materialize in natural populations remains unknown. We quantified the impact of male morphotype on male reproductive success in a natural population of Octodon degus, a highly social rodent. We assessed male morphotype through a continuous gradient of anogenital distance. We also tested the hypothesis that the social environment interacts with male morphotype to influence male reproductive success. We found that individual attributes, including masculinization level and age, impacted male reproductive success. Highly masculinized and younger males had greater reproductive success. Additionally, male body weight had a small magnitude but positive effect on male reproductive success. Male reproductive success was not affected by social attributes such as group composition. Thus, the number of males and females within a group did not affect male reproductive success, nor did the average male anogenital distance within a group. Our results support the hypothesis that the prenatal environment can result in long-term effects on individual life history and cause intrasexual phenotypical variation in natural populations. Our findings suggest that male phenotypical masculinization could be an adaptive trait, regardless of the social environment.