Hormones and cooperative behaviours in the Damaraland mole-rat (Fukomys damarensis)

Large individual differences in cooperative contributions are common within animal societies such as cooperative breeders, where helpers care for offspring which are not their own. Understanding this variation has been a major focus in behavioural ecology and while evidence has shown that individuals are capable to adaptively adjust their cooperative behaviours, the physiological mechanisms underlying such adjustments remain poorly understood. Steroid hormones are prominent candidates to regulate cooperative behaviours due to their ability to integrate internal physiological state and environmental stimuli to produce an adaptive behavioural response. In this thesis, I investigate the effects of two steroid hormones, Cortisol (CORT) and Testosterone (T), in the regulation of cooperative behaviours in the Damaraland mole-rat (Fukomys damarensis). Because these hormones are susceptible to both modulate and be modulated by cooperative contributions, I experimentally tested both sides of this relationship. I show that, despite the absence of correlation between CORT and T and cooperative contributions, experimental increases of cooperative contributions elevate CORT levels, but not T (Chapter 3). Additionally, experimental increases of CORT levels in female helpers raised their cooperative contributions by more than one half demonstrating the regulatory effect of CORT on cooperative behaviours (Chapter 4). As breeding opportunities are likely to affect cooperative contributions and because T is a likely candidate to mediate a trade-off between future reproduction and current cooperation, I tested the effects of experimental increases of T levels in female helpers. I show that such elevations have no measurable effect of aggression, dispersal tendencies (both important to attain a breeding position) or cooperative contributions (Chapter 5). Taken together, the results of this thesis demonstrate that CORT can both respond to and regulate cooperative behaviours and suggest that this hormone may play a major role in the adaptive regulation of cooperative behaviour.Cambridge International Scholarship from the Cambridge Trus

Differences in cooperative behavior among Damaraland mole rats are consequences of an age-related polyethism.

In many cooperative breeders, the contributions of helpers to cooperative activities change with age, resulting in age-related polyethisms. In contrast, some studies of social mole rats (including naked mole rats, Heterocephalus glaber, and Damaraland mole rats, Fukomys damarensis) suggest that individual differences in cooperative behavior are the result of divergent developmental pathways, leading to discrete and permanent functional categories of helpers that resemble the caste systems found in eusocial insects. Here we show that, in Damaraland mole rats, individual contributions to cooperative behavior increase with age and are higher in fast-growing individuals. Individual contributions to different cooperative tasks are intercorrelated and repeatability of cooperative behavior is similar to that found in other cooperatively breeding vertebrates. Our data provide no evidence that nonreproductive individuals show divergent developmental pathways or specialize in particular tasks. Instead of representing a caste system, variation in the behavior of nonreproductive individuals in Damaraland mole rats closely resembles that found in other cooperatively breeding mammals and appears to be a consequence of age-related polyethism.This study was funded by an European Research Council grant to THCB (294494).This is the author accepted manuscript. The final version is available from the National Academy of Sciences via http://dx.doi.org/10.1073/pnas.160788511

Allo-parental care in Damaraland mole-rats is female biased and age dependent, though independent of testosterone levels

Abstract In Damaraland mole-rats (Fukomys damarensis), non-breeding subordinates contribute to the care of offspring born to the breeding pair in their group by carrying and retrieving young to the nest. In social mole-rats and some cooperative breeders, dominant females show unusually high testosterone levels and it has been suggested that high testosterone levels may increase reproductive and aggressive behavior and reduce investment in allo-parental and parental care, generating age and state-dependent variation in behavior. Here we show that, in Damaraland mole-rats, allo-parental care in males and females is unaffected by experimental increases in testosterone levels. Pup carrying decreases with age of the non-breeding helper while the change in social status from non-breeder to breeder has contrasting effects in the two sexes. Female breeders were more likely than female non-breeders to carry pups but male breeders were less likely to carry pups than male non-breeders, increasing the sex bias in parental care compared to allo-parental care. Our results indicate that testosterone is unlikely to be an important regulator of allo-parental care in mole-rats.Peer reviewe

Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity.

In some mammals and many social insects, highly cooperative societies are characterized by reproductive division of labor, in which breeders and nonbreeders become behaviorally and morphologically distinct. While differences in behavior and growth between breeders and nonbreeders have been extensively described, little is known of their molecular underpinnings. Here, we investigate the consequences of breeding for skeletal morphology and gene regulation in highly cooperative Damaraland mole-rats. By experimentally assigning breeding 'queen' status versus nonbreeder status to age-matched littermates, we confirm that queens experience vertebral growth that likely confers advantages to fecundity. However, they also upregulate bone resorption pathways and show reductions in femoral mass, which predicts increased vulnerability to fracture. Together, our results show that, as in eusocial insects, reproductive division of labor in mole-rats leads to gene regulatory rewiring and extensive morphological plasticity. However, in mole-rats, concentrated reproduction is also accompanied by costs to bone strength

Kin recognition for incest avoidance in Damaraland mole-rats, Fukomys damarensis

Across taxa, breeding among close relatives is usually avoided because it incurs fitness costs to offspring. Incest is often averted through the dispersal of either sex from the natal area to breed. In some philopatric species, association among relatives extends in to adulthood, and an ability to discriminate kin may be required for individuals to reduce inbreeding risk. Here, we aim to determine the mechanism of kin recognition for incest avoidance in the Damaraland mole-rat Fukomys damarensis, a cooperative breeder characterized by extreme reproductive skew. Pairs of opposite-sex adults were formed in the laboratory and, within pairs, genetic relatedness and degree of familiarity were manipulated through cross-fostering experiments. We found that unfamiliar pairs were more likely to engage in sexual behaviours and bred more successfully than familiar pairs, regardless of their genetic similarity. Females paired with unfamiliar males were also more likely to exhibit reproductive activation, characterized by increased levels of oestradiol and progesterone. This study shows that in Damaraland mole-rats, inbreeding avoidance can be achieved through a discrimination mechanism that relies on association during rearing, and that ovulation is induced by mating. This study advances our understanding of incest avoidance in species with constrained dispersal

No task specialization among helpers in Damaraland mole-rats

The specialization of individuals in specific behavioural tasks is often attributed either to irreversible differences in development, which generate functionally divergent cooperative phenotypes, or to agerelated changes in the relative frequency with which individuals perform different cooperative activities; both of which are common in many insect caste systems. However, contrasts in cooperative behaviour can take other forms and, to date, few studies of cooperative behaviour in vertebrates have explored the effects of age, adult phenotype and early development on individual differences in cooperative behaviour in sufficient detail to discriminate between these alternatives. Here, we used multinomial models to quantify the extent of behavioural specialization within nonreproductive Damaraland mole-rats, Fukomys damarensis, at different ages. We showed that, although there were large differences between individuals in their contribution to cooperative activities, there was no evidence of individual specialization in cooperative activities that resembled the differences found in insect societies with distinct castes where individual contributions to different activities are negatively related to each other. Instead, individual differences in helping behaviour appeared to be the result of age-related changes in the extent to which individuals committed to all forms of helping. A similar pattern is observed in cooperatively breeding meerkats, Suricata suricatta, and there is no unequivocal evidence of caste differentiation in any cooperative vertebrate. The multinomial models we employed offer a powerful heuristic tool to explore task specialization and developmental divergence across social taxa and provide an analytical approach that may be useful in exploring the distribution of different forms of helping behaviour in other cooperative species.The Kalahari Mole-rat Project is supported by a European Research Council Grant awarded to TCB (#294494); J.T. is funded by a Natural Environment Research Council Doctoral Training Programme (NERC reference number 1505720).http://www.elsevier.com/locate/anbehavam2019Mammal Research InstituteZoology and Entomolog

Oxidative costs of cooperation in cooperatively breeding Damaraland mole-rats

Within cooperatively breeding societies, individuals adjust cooperative contributions to maximize indirect fitness and minimize direct fitness costs. Yet, little is known about the physiological costs of cooperation, which may be detrimental to direct fitness. Oxidative stress, the imbalance between reactive oxygen species (by-products of energy production) and antioxidant protection, may represent such a cost when cooperative behaviours are energetically demanding. Oxidative stress can lead to the accumulation of cellular damage, compromising survival and reproduction, thus mediating the trade-off between these competing life-history traits. Here, we experimentally increased energetically demanding cooperative contributions in captive Damaraland mole-rats (Fukomys damarensis). We quantified oxidative stress-related effects of increased cooperation on somatic and germline tissues, and the trade-off between them. Increased cooperative contributions induced oxidative stress in females and males, without increasing somatic damage. Males accumulated oxidative damage in their germline despite an increase in antioxidant defences. Finally, oxidative damage accumulation became biased towards the germline, while antioxidant protection remained biased towards the soma, suggesting that males favour the maintenance of somatic tissues (i.e. survival over reproduction). Our results show that heightened cooperative contributions can ultimately affect direct fitness through oxidative stress costs, which may represent a key selective pressure for the evolution of cooperation.A Postgraduate Research Support bursary awarded by the University of Pretoria; Department of Science and Technology/ National Research Foundation SARChI chair in Behavioural Ecology and Physiology; the Swiss National Science Foundation and animal husbandry and facilities at the Kalahari Research Centre were funded by European Research Council Advanced Grants.http://royalsocietypublishing.org/journal/rspbhj2021Mammal Research InstituteZoology and Entomolog

Benefits of cooperation in captive Damaraland mole-rats

Although the social mole-rats are commonly classified as eusocial breeders on the grounds that groups include a single breeding female (the “queen”) and a number of nonbreeding individuals (“helpers”) of both sexes, alloparental care is not highly developed in these species and there is no direct evidence that the presence or number of nonbreeders is associated with reductions in the workload of the “queen.” An alternative interpretation of mole-rat groups is that the social mole-rats are cooperative foragers rather than cooperative or eusocial breeders. Here, in captive colonies of Damaraland mole-rats (Fukomys damarensis), we provide the first evidence that increases in the number of nonbreeding subordinates in mole-rat groups are associated with reductions in the workload of “queens” and with increases in their fecundity.The European Research Council and the Human Frontier Science Program.https://academic.oup.com/beheco2021-03-12hj2020Mammal Research InstituteZoology and Entomolog