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

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

Data for "No task specialisation among Damaraland mole-rat helpers"

Behavioural data of captive Damaraland mole-rats followed longitudinally across development. Data takes the form of all occurrence scan sampling conducted at 4-minute sampling intervals (within an overall observation period of 12 hours); each row represents a single observation at one of the sampling intervals