Evolutionary Determinants of Nonseasonal Breeding in Wild Chacma Baboons.

AbstractAnimal reproductive phenology varies from strongly seasonal to nonseasonal, sometimes among closely related or sympatric species. While the extent of reproductive seasonality is often attributed to environmental seasonality, this fails to explain many cases of nonseasonal breeding in seasonal environments. We investigated the evolutionary determinants of nonseasonal breeding in a wild primate, the chacma baboon (Papio ursinus), living in a seasonal environment with high climatic unpredictability. We tested three hypotheses proposing that nonseasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favoring birth asynchrony, and (3) individual, rank-dependent variations in optimal reproductive timing. We found strong support for an effect of reproductive asynchrony modulated by rank: (i) birth synchrony is costly to subordinate females, lengthening their interbirth intervals; (ii) females alter their reproductive timings (fertility periods and conceptions) in relation to previous conceptions in the group; and (iii) the reported effect of birth synchrony on interbirth intervals weakens the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in group-living organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

A comprehensive profile of reproductive hormones in eusocial Damaraland mole-rats (Fukomys damarensis).

In species where sociality and group cohesion are primarily determined by the maintenance of a reproductive division of labour and cooperative behaviours, the eusocial Damaraland mole-rat (Fukomys damarensis) presents a model which provides behavioural and endocrine distinctions between sex (males and females) and reproductive class (breeders and non-breeders). Although previous studies have demonstrated the endocrine aspects of reproductive suppression and behaviour in Damaraland mole-rats, they have focused on one hormone separately and on different conspecifics and samples across time. Unfortunately, this could introduce extrinsic biases when using these studies to compile complete hormonal profiles for comparisons. This study, therefore, set out to obtain a profile of the reproductive hormones from breeding and non-breeding male and female Damaraland mole-rats at a single point in time, from which circulating plasma prolactin and urinary progesterone, testosterone, and cortisol were measured. As expected, plasma prolactin and urinary cortisol did not differ between the breeders and non-breeders. However, breeders (both male and female) possessed increased urinary testosterone and progesterone concentrations compared to their non-breeding counterparts. These results, in conjunction with the variation in the expression of the respective hormonal receptors within the brains of breeders and non-breeders suggest that elevated testosterone and progesterone in breeders establish a neural dominance phenotype, which ultimately aids in controlling breeding activities. This study has emphasised the need for holistic, comprehensive profiling of reproductive endocrine systems.

Reproductive Suppression Caused by Spermatogenic Arrest: Transcriptomic Evidence from a Non-Social Animal.

Reproductive suppression is an adaptive strategy in animal reproduction. The mechanism of reproductive suppression has been studied in social animals, providing an essential basis for understanding the maintenance and development of population stability. However, little is known about it in solitary animals. The plateau zokor is a dominant, subterranean, solitary rodent in the Qinghai-Tibet Plateau. However, the mechanism of reproductive suppression in this animal is unknown. We perform morphological, hormonal, and transcriptomic assays on the testes of male plateau zokors in breeders, in non-breeders, and in the non-breeding season. We found that the testes of non-breeders are smaller in weight and have lower serum testosterone levels than those of breeders, and the mRNA expression levels of the anti-Müllerian hormone (AMH) and its transcription factors are significantly higher in non-breeder testes. Genes related to spermatogenesis are significantly downregulated in both meiotic and post-meiotic stages in non-breeders. Genes related to the meiotic cell cycle, spermatogenesis, flagellated sperm motility, fertilization, and sperm capacitation are significantly downregulated in non-breeders. Our data suggest that high levels of AMH may lead to low levels of testosterone, resulting in delayed testicular development, and physiological reproductive suppression in plateau zokor. This study enriches our understanding of reproductive suppression in solitary mammals and provides a basis for the optimization of managing this species.

The endocrine control of reproductive suppression in an aseasonally breeding social subterranean rodent, the Mahali mole-rat (Cryptomys hottentotus mahali).

Cooperative behaviour, sociality and reproductive suppression in African mole-rats have been extensively studied. Nevertheless, endocrine correlates of some species of social mole-rats have been neglected, and these species may hold the key to understanding the behavioural and physiological complexity that allows the maintenance of social groups in African mole-rats. In this study, we investigated endocrine correlates implicated in the suppression of reproduction and cooperative behaviours, namely glucocorticoids (a stress-related indicator) through faecal glucocorticoid metabolites (fGCMs), plasma testosterone (an indicator of aggression) and plasma prolactin in the Mahali mole-rat (Cryptomys hottentotus mahali) across reproductive classes (breeding females and males, non-breeding females and males) and season (wet and dry). Breeders possessed higher levels of testosterone than non-breeders. In reproductively suppressed non-breeding females, fGCMs were significantly higher than in breeders. Furthermore, an adrenocorticotropic hormone stimulation test (ACTH challenge test) on both male and female non-breeders revealed that female non-breeders show a more significant response to the ACTH challenge than males. At the same time, plasma prolactin levels were equally elevated to similar levels in breeding and non-breeding females. Chronically high levels of prolactin and fGCM are reported to cause reproductive suppression and promote cooperative behaviours in non-breeding animals. Furthermore, there was a negative relationship between plasma prolactin and progesterone in non-breeding females. However, during the wet season, a relaxation of suppression occurs through reduced prolactin which corresponds with elevated levels of plasma progesterone in non-breeding females. Therefore, prolactin is hypothesised to be the primary hormone controlling reproductive suppression and cooperative behaviours in non-breeding females. This study provides new endocrine findings for the maintenance of social suppression in the genus Cryptomys.

The elusive role of prolactin in the sociality of the naked mole-rat.

Despite decades of research into the evolutionary drivers of sociality, we know relatively little about the underlying proximate mechanisms. Here we investigate the potential role of prolactin in the highly social naked mole-rat. Naked mole-rats live in large social groups but, only a small number of individuals reproduce. The remaining non-breeders are reproductively suppressed and contribute to burrow maintenance, foraging, and allo-parental care. Prolactin has well-documented links with reproductive timing and parental behaviour, and the discovery that non-breeding naked mole-rats have unusually high prolactin levels has led to the suggestion that prolactin may help maintain naked mole-rat sociality. To test this idea, we investigated whether urinary prolactin was correlated with cooperative behaviour and aggression. We then administered the prolactin-suppressing drug Cabergoline to eight female non-breeders for eight weeks and assessed the physiology and behaviour of the animals relative to controls. Contrary to the mammalian norm, and supporting previous findings for plasma, we found non-breeders had elevated urinary prolactin concentrations that were similar to breeding females. Further, prolactin levels were higher in heavier, socially dominant non-breeders. Urinary prolactin concentrations did not explain variation in working behaviour or patterns of aggression. Furthermore, females receiving Cabergoline did not show any behavioural or hormonal (progesterone) differences, and urinary prolactin did not appear to be suppressed in individuals receiving Cabergoline. While the results add to the relatively limited literature experimentally manipulating prolactin to investigate its role in reproduction and behaviour, they fail to explain why prolactin levels are high in non-breeding naked mole-rats, or how female non-breeding phenotypes are maintained.

A retrospective view of early research on dominance, stress and reproduction in cooperatively breeding carnivores.

Social carnivores have been central in studies of cooperative breeding, and research using noninvasive methods to examine behavioral and endocrine mechanisms of reproductive suppression started in the 1980s with dwarf mongooses in Serengeti National Park. Here, I synthesize the methods, findings and limitations of a research program that examined relationships between social dominance, age, mass, aggression, mating, gonadal steroids, glucocorticoids and reproduction in female and male dwarf mongooses, African wild dogs and wolves. Infanticide is a reliable backstop for reproductive suppression in females, and reproduction is energetically costly in these species. These conditions favor hypothalamic - pituitary - gonadal (HPG) adaptations that reduce the fertility of subordinate females to avoid the cost of producing doomed offspring. Infanticide also favors close synchronization of reproduction when subordinate females do become pregnant. In males, infanticide is a less reliable backstop and reproduction is less costly, so direct effects of subordination on fertility are less pronounced. Age is a strong predictor of social dominance in these species, but the evolutionary reason for this is not clear. In dwarf mongooses and wild dogs, alpha females were never deposed by younger packmates, but alpha males were: this difference is also not understood. Patterns of reproduction supported models predicting that alphas are less likely to share reproduction when the fitness costs of reproduction are high, when the fitness expected for dispersers is low, and with young subordinates to whom they are more closely related. Correlations between dominance and adrenal glucocorticoid concentrations varied between species and sexes, but did not support the hypothesis that chronic stress causes reproductive suppression.

Molecular mechanisms of self-regulation in multiannual rodent populations: Experimental test of an updated hypothesis.

IN FOCUS: Edwards, P. D., Frenette-Ling, C., Palme, R., & Boonstra, R. (2021). Social density suppresses GnRH expression and reduces reproductivity in voles: A mechanism for population self-regulation. Journal of Animal Ecology, 90, 784-795. Intrinsic population processes are important in the regulation of populations of small rodents, including those which display multiannual cycles. By measuring reproductive parameters, faecal androgen metabolites, and gene expression and DNA methylation in the CNS of juvenile voles, this paper demonstrates that suppression of reproduction occurs in female voles at high density compared to low density in enclosures, and that this maternal, epigenetic effect is also apparent in their offspring. This suggsests that direct density dependence influences reproduction and, hence, immediate rate of population growth, while gene expression mediated by DNA methylation blocking transcription, may have a delayed density-dependent effect in juveniles. Both direct and delayed density dependence are necessary to generate multiannual population cycles. Edwards et al. (2021) break new ground in demonstrating the molecular and physiological basis of variation in population dynamics of small mammals ranging from multiannual cycles to stability that have fascinated researchers for nearly a century.

A mechanism for population self-regulation: Social density suppresses GnRH expression and reduces reproductivity in voles.

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.

Evolutionary Pathways to Communal and Cooperative Breeding in Carnivores.

In animal societies, individuals can cooperate in a variety of tasks, including rearing young. Such cooperation is observed in complex social systems, including communal and cooperative breeding. In mammals, both these social systems are characterized by delayed dispersal and alloparenting, whereas only cooperative breeding involves reproductive suppression. While the evolution of communal breeding has been linked to direct fitness benefits of alloparenting, the direct fitness cost of reproductive suppression has led to the hypothesis that the evolution of cooperative breeding is driven by indirect fitness benefits accrued through raising the offspring of related individuals. To decipher between the evolutionary scenarios leading to communal and cooperative breeding in carnivores, we investigated the coevolution among delayed dispersal, reproductive suppression, and alloparenting. We reconstructed ancestral states and transition rates between these traits. We found that cooperative breeding and communal breeding evolved along separate pathways, with delayed dispersal as the first step for both. The three traits coevolved, enhancing and stabilizing one another, which resulted in cooperative social systems as opposed to intermediate configurations being stable. These findings promote the key role of coevolution among traits to stabilize cooperative social systems and highlight the specificities of evolutionary patterns of sociality in carnivores.

Effect of colony disruption and social isolation on naked mole-rat endocrine correlates.

The social environment of animals can have profound implications on their behaviour and physiology. Naked mole-rats (Heterocephalus glaber) are highly social with complex dominance hierarchies that influence both stress- and reproduction-related hormones. Homeostasis may be affected by aggressive interactions, colony instability and social isolation. Furthermore, naked mole-rat colonies are characterised by a marked reproductive skew; a single female and few males are reproductively active while other colony members are reproductively suppressed. Thus, there are distinct differences in related hormone concentrations between reproductively active and non-active animals; however, this changes when non-reproductive individuals are removed from the colony. We investigated the effects of social isolation and colony disruption on plasma cortisol and progesterone concentrations in non-breeding naked mole-rats. During colony disruption, we found a significant increase in cortisol concentrations in females removed from the colony for social isolation (experimental) as well as in females that remained in the colony (control). Cortisol concentrations were reduced in both groups after experimental animals were paired up. No changes in cortisol concentrations were observed in control or experimental males after removal from the colony or pairing. This suggests that the females, but not the males, found colony disruption and social isolation stressful. Upon removal from the colony, both control and experimental females showed a small increase in progesterone, which returned to basal levels again in the control animals. Experimental females showed a dramatic spike in progesterone when they were paired with males, indicating reproductive activation. The sex difference in the stress responses may be due to the stronger reproductive suppression imposed on females, or the increased likelihood of dispersal for males. It is clear that the social environment reflects on the endocrine correlates of animals living in a colony, and that the colony structure may affect the sensitivity of the animals to changes in their environment.