•Glucocorticoid (GC) dynamics during pregnancy are mostly known from model species.•These findings may not be generally applicable to mammals.•We review GCs during pregnancy in a variety of orders to ...assess generality.•In most species, maternal GCs increase during late pregnancy.•Increase in fetal GC exposure in late pregnancy is essential for development.
Pregnancy is one of the defining characteristics of placental mammals. Key in the growth and development of the fetus during pregnancy are the dynamics of glucocorticoids (GCs) and their binding protein,corticosteroid-binding globulin (CBG), which determines how much of the GCs are free and biologically active. Out of more than 5000 species of placental mammals in 19 different orders, our understanding of the dynamics of maternal GCs and CBG during pregnancy is largely limited to the detailed study of 3 groups – sheep, laboratory rodents, and humans. The assumption is often made that what we see in these few species applies to the rest. To examine this generality, we compared patterns of maternal GCs over pregnancy from all placental mammals where data is available: in the blood of 13 species from 5 different orders and in metabolites in excreta in an additional 20 species from 9 orders. We found that maternal free GCs increase by late pregnancy in most taxa. This increase is achieved by either an increase in total GC secretion or a decrease in CBG. A major exception is found in the even-toed ungulates (sheep, cows, etc.) where maternal GCs and CBG remain stable, but where the fetal adrenals mature in late pregnancy and produce the majority of their own GCs. We conclude that patterns of change in maternal GCs and CBG during pregnancy are species-specific but are alternative means to the same end: increased fetal exposure to GCs in late pregnancy, which is essential for development.
Chronic stress has long been hypothesized to play a role in driving population cycles. Christian (1950) hypothesized that high population density results in chronic stress and mass “die-offs” in ...small mammal populations. Updated variations of this hypothesis propose that chronic stress at high population density may reduce fitness, reproduction, or program aspects of phenotype, driving population declines. We tested the effect of density on the stress axis in meadow voles (
Microtus pennsylvanicus
) by manipulating population density in field enclosures over three years. Using fecal corticosterone metabolites as a non-invasive measure of glucocorticoid (GC) concentrations, we found that density alone was not associated with GC differences. However, we found that the seasonal relationship of GC levels differed by density treatment, with high-density populations having elevated GC levels early in the breeding season and decreasing towards late summer. We additionally tested hippocampal glucocorticoid receptor and mineralocorticoid receptor gene expression in juvenile voles born at different densities, with the hypothesis that high density may reduce receptor expression, altering negative feedback of the stress axis. We found that females had marginally higher glucocorticoid receptor expression at high density, no effect in males, and no detectable effect of density on mineralocorticoid receptor expression in either sex. Hence, we found no evidence that high density directly impairs negative feedback in the hippocampus, but rather female offspring may be better equipped for negative feedback. We compare our findings with prior studies to attempt to disentangle the complicated relationship between density, seasonality, sex, reproduction and the stress axis.
Nearly 100 years ago, Charles Elton described lemming and vole population cycles as ecological models for understanding population regulation in nature. Yet, the mechanisms driving these cycles are ...still not fully understood. These rodent populations can continue to cycle in the absence of predation and with food supplementation, and represent a major unsolved problem in population ecology.
It has been hypothesized that the social environment at high population density can drive selection for a low‐reproduction phenotype, resulting in population self‐regulation as an intrinsic mechanism driving the cycles. However, a physiological mechanism for this self‐regulation has not been demonstrated. We manipulated population density in wild meadow voles Microtus pennsylvanicus using large‐scale field enclosures over 3 years and examined reproductive performance and physiology.
Within the field enclosures, we assessed the proportion of breeding animals, mass at sexual maturation, and faecal androgen and oestrogen metabolites. We then collected brain tissue from juvenile voles born at high or low density, quantified mRNA expression of gonadotropin‐releasing hormone (GnRH) and oestrogen receptor alpha (ERα) and measured DNA methylation at six CpG sites in a region that was highly conserved with the mouse GnRH promoter.
At high density, there was a lower proportion of reproductive animals. Juvenile voles born at high densities had reduced expression of GnRH in the hypothalamus, accompanied by marginally lower faecal sex hormone metabolites. Female juvenile voles born at high density also had higher methylation levels at two CpG sites while males did not, aligning with prior observations that females (but not males) from high‐density environments retain reduced reproduction long term.
Our results support a physiological basis for population self‐regulation in vole cycles, as altering population density alone induced reproductive downregulation at the hypothalamic level. Our results demonstrate that altering the early‐life social environment can fundamentally impact reproductive function in the brain. This, in turn, can drive population demography changes in wild animals.
In this study the authors manipulated vole population density to test mechanisms of intrinsic regulation (self‐regulation). The authors found that voles at high density have lower gonadotropin‐releasing hormone (GnRH) expression in the hypothalamus, and females additionally had higher cytosine methylation in the GnRH promoter region. This implies direct, density‐dependent suppression of reproduction.
Wild mammal populations exhibit a variety of dynamics, ranging from fairly stable with little change in population size over time to high‐amplitude cyclic or erratic fluctuations. A persistent ...question in population ecology is why populations fluctuate as they do. Answering this seemingly simple question has proven to be challenging. Broadly, density‐dependent feedback mechanisms should allow populations to grow at low density and slow or halt growth at high density. However, experimental tests of what demographic processes result in density‐dependent feedback and on what timescale have proven elusive. Here, we used replicated density perturbation experiments and capture‐mark‐recapture analyses to test density‐dependent population growth in populations of meadow voles (Microtus pennsylvanicus) during the summer breeding season by manipulating founding population density and observing the pattern of survival, reproduction, and population growth. High population density had no consistent effect on survival rates but generally negatively influenced recruitment and population growth rates. However, these density‐dependent effects varied within the breeding season and across years. Our study provides evidence that density‐dependent feedback mechanisms operate at finer time scales than previously believed and that process, additively with delayed year effects, is key to understanding multiyear population demography.
Vertebrates have high species‐level variation in circulating hormone concentrations, and the functional significance of this variation is largely unknown. We tested the hypothesis that interspecific ...differences in hormone concentrations are partially driven by plant consumption, based on the prediction that herbivores should have higher basal hormone levels to ‘outcompete’ plant endocrine disruptors. We compared levels of glucocorticoids (GCs), the hormones with the most available data, across 166 species. Using phylogenetically informed comparisons, we found that herbivores had higher GC levels than carnivores. Furthermore, we found that the previously described negative relationship between GC levels and body mass only held in herbivores, not carnivores, and that the effect of diet was greatest at extreme body sizes. These findings demonstrate the far‐reaching effects of diet on animal physiology, and provide evidence that herbivory influences circulating hormone concentrations. We urge future direct testing of the relationship between phytochemical load and GC levels.
We tested the hypothesis that interspecific differences in vertebrate hormone concentrations are partially driven by plant consumption, based on the prediction that herbivores should have higher basal hormone levels to ‘outcompete’ plant endocrine disruptors. Using phylogenetically informed comparisons, we found that herbivores had higher glucocorticoid levels than carnivorous. We urge future direct testing on the relationship between phytochemical load and GC levels.
In some cooperatively breeding groups, individuals have distinct behavioral characteristics that are often stable and predictable across time. However, in others, as in the eusocial naked mole-rat, ...evidence for behavioral phenotypes is ambiguous. Here, we study whether the naked mole-rat can be divided into discrete phenotypes and if circulating hormone concentrations underpin these differences. Naked mole-rat colonies consist of a single breeding female and large numbers of non-reproductive subordinates that in some cases can exceed several hundred in a colony. The subordinates can potentially be divided into soldiers, who defend the colony; workers, who maintain it; and dispersers, who want to leave it. We established six colonies de novo, tracked them over three years, and assessed the behavior and hormone concentrations of the subordinates. We found that soldiers tended to be from earlier litters and were higher ranked compared to workers, whereas dispersers were distributed throughout litters and rankings. There was no difference in estradiol, testosterone, or dehydroepiandrosterone (DHEA) concentrations among phenotypes. Progesterone concentrations were higher in soldiers, but this difference appeared to be driven by a few individuals. Principal component analysis demonstrated that soldiers separated into a discrete category relative to workers/dispersers, with the highest ranked loadings being age, body mass, and testosterone concentrations. However, the higher testosterone in soldiers was correlated with large body size instead of strictly behavioral phenotype. Workers and dispersers have more overlap with each other and no hormonal differences. Thus the behavioral variation in subordinate naked mole-rats is likely not driven by circulating steroid hormone concentrations, but rather it may stem from alternative neural and/or neuroendocrine mechanisms.
•Naked mole-rat subordinates are classified into workers, dispersers and soldiers.•Soldiers tend to be born in earlier litters and rank higher in dominance.•Soldiers have higher levels of circulating progesterone.•Workers and dispersers have overlapping biological correlates.•Behavioral phenotypes are not driven by circulating hormones.
•A fecal glucocorticoid metabolite assay was validated in wild colobus monkeys.•Morning samples have higher levels than afternoon samples.•Pregnant females have higher baseline levels than lactating ...or cycling females.•In the two days around parturition, maternal glucocorticoids temporarily increase.
Analysis of glucocorticoid profiles serves as a valuable, multi-faceted tool for insight into the behavior and physiology of wild populations. Recently, the measurement of fecal glucocorticoid metabolites (FCMs) has exploded in popularity due to its compatibility with noninvasive techniques and remote environments A critical first step is to perform a biological validation to ensure that the assay accurately reflect changes in FCM levels. We use an enzyme immunoassay (EIA) to perform a biological validation on samples collected from two males and six females in a wild population of Colobus vellerosus in response to three naturally occurring potential stressors. We also describe the FCM response pattern in the week following parturition in three females and examine the influence of sex, reproductive state, and time of day on the concentrations of baseline samples collected daily from 13 adult individuals over a period of four months. We validated the assay: FCM levels increase in response to natural stressors with a two-day lag. In the two days surrounding parturition, FMC levels increased. Baseline concentrations were affected by collection time and female reproductive state, with lactating females having lower concentrations than pregnant or cycling females. Thus, we successfully carried out the first validation and characterization of FCMs in a wild African colobine. This will serve as an essential foundation for future studies of C. vellerosus and similar wild primates whose objective is to investigate the role glucocorticoids play in responses to social and ecological challenges.
Synopsis
For cooperative species, there can be great value in the synchronization of physiological states to coordinate group behavioral states. This is evident in naked mole-rats (Heterocephalus ...glaber), which have the most extreme form of cooperative breeding in mammals. Colonies have a single reproductive female, “the queen,” and 1–3 breeding males. These breeders are supported by adult “subordinates,” which are all socially suppressed into a pre-pubertal state. Subordinates cooperate in colony maintenance, defense, and alloparental care. Prior work has reported that there may be social sharing of hormones among individuals in the colony because when the queen is pregnant, subordinates of both sexes develop enlarged nipples and female subordinates can develop vaginal perforation. We sought to document the hormonal changes and mechanisms behind these observations. We found that subordinate estradiol levels were elevated during the queen’s pregnancy and were correlated with queen levels. To determine if this occurs by direct hormone-sharing, where group members uptake the hormones of conspecifics through excreta or the skin, we then tested whether treating a single subordinate in the colony with estradiol would induce the same effect in other colony members. It did not, which indicates that the influence on group estradiol levels may be specific to cues from the queen. These queen cues may be behavioral in nature, as we found that queens were less aggressive during pregnancy, which prior work has suggested may relax reproductive suppression of subordinates. Yet, levels of queen aggression alone were not associated, or were weakly associated, with their colony’s estradiol levels, though our sample size examining this particular relationship was low. This is suggestive that additional queen cues of reproductive status, beyond just aggression, may be relevant in influencing the subordinate hormonal change, or that the relationship between aggression and colony estradiol levels is more subtle and would need to be elucidated with a larger sample size. These results have implications for how cooperative breeders coordinate reproduction and alloparental care, and how social cues can influence individual and group physiology.
