The development of individual differences in cooperative behaviour: maternal glucocorticoid hormones alter helping behaviour of offspring in wild meerkats.

The phenotype of parents can have long-lasting effects on the development of offspring as well as on their behaviour, physiology and morphology as adults. In some cases, these changes may increase offspring fitness but, in others, they can elevate parental fitness at a cost to the fitness of their offspring. We show that in Kalahari meerkats ( Suricata suricatta), the circulating glucocorticoid (GC) hormones of pregnant females affect the growth and cooperative behaviour of their offspring. We performed a 3-year experiment in wild meerkats to test the hypothesis that GC-mediated maternal effects reduce the potential for offspring to reproduce directly and therefore cause them to exhibit more cooperative behaviour. Daughters (but not sons) born to mothers treated with cortisol during pregnancy grew more slowly early in life and exhibited significantly more of two types of cooperative behaviour (pup rearing and feeding) once they were adults compared to offspring from control mothers. They also had lower measures of GCs as they aged, which could explain the observed increases in cooperative behaviour. Because early life growth is a crucial determinant of fitness in female meerkats, our results indicate that GC-mediated maternal effects may reduce the fitness of offspring, but may elevate parental fitness as a consequence of increasing the cooperative behaviour of their daughters. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

The influence of stress hormones and aggression on cooperative behaviour in subordinate meerkats.

In cooperative breeders, aggression from dominant breeders directed at subordinates may raise subordinate stress hormone (glucocorticoid) concentrations. This may benefit dominants by suppressing subordinate reproduction but it is uncertain whether aggression from dominants can elevate subordinate cooperative behaviour, or how resulting changes in subordinate glucocorticoid concentrations affect their cooperative behaviour. We show here that the effects of manipulating glucocorticoid concentrations in wild meerkats (Suricata suricatta) on cooperative behaviour varied between cooperative activities as well as between the sexes. Subordinates of both sexes treated with a glucocorticoid receptor antagonist (mifepristone) exhibited significantly more pup protection behaviour (babysitting) compared to those treated with glucocorticoids (cortisol) or controls. Females treated with mifepristone had a higher probability of exhibiting pup food provisioning (pup-feeding) compared to those treated with cortisol. In males, there were no treatment effects on the probability of pup-feeding, but those treated with cortisol gave a higher proportion of the food they found to pups than those treated with mifepristone. Using 19 years of behavioural data, we also show that dominant females did not increase the frequency with which they directed aggression at subordinates at times when the need for assistance was highest. Our results suggest that it is unlikely that dominant females manipulate the cooperative behaviour of subordinates through the effects of aggression on their glucocorticoid levels and that the function of aggression directed at subordinates is probably to reduce the probability they will breed.

Beyond aggression: Androgen-receptor blockade modulates social interaction in wild meerkats.

In male vertebrates, androgens are inextricably linked to reproduction, social dominance, and aggression, often at the cost of paternal investment or prosociality. Testosterone is invoked to explain rank-related reproductive differences, but its role within a status class, particularly among subordinates, is underappreciated. Recent evidence, especially for monogamous and cooperatively breeding species, suggests broader androgenic mediation of adult social interaction. We explored the actions of androgens in subordinate, male members of a cooperatively breeding species, the meerkat (Suricata suricatta). Although male meerkats show no rank-related testosterone differences, subordinate helpers rarely reproduce. We blocked androgen receptors, in the field, by treating subordinate males with the antiandrogen, flutamide. We monitored androgen concentrations (via baseline serum and time-sequential fecal sampling) and recorded behavior within their groups (via focal observation). Relative to controls, flutamide-treated animals initiated less and received more high-intensity aggression (biting, threatening, feeding competition), engaged in more prosocial behavior (social sniffing, grooming, huddling), and less frequently initiated play or assumed a 'dominant' role during play, revealing significant androgenic effects across a broad range of social behavior. By contrast, guarding or vigilance and measures of olfactory and vocal communication in subordinate males appeared unaffected by flutamide treatment. Thus, androgens in male meerkat helpers are aligned with the traditional trade-off between promoting reproductive and aggressive behavior at a cost to affiliation. Our findings, based on rare endocrine manipulation in wild mammals, show a more pervasive role for androgens in adult social behavior than is often recognized, with possible relevance for understanding tradeoffs in cooperative systems.

Embryo oxygenation in pipefish brood pouches: novel insights.

The pipefish brood pouch presents a unique mode of parental care that enables males to protect, osmoregulate, nourish and oxygenate the developing young. Using a very fine O2 probe, we assessed the extent to which males of the broad-nosed pipefish (Syngnathus typhle) oxygenate the developing embryos and are able to maintain pouch fluid O2 levels when brooding in normoxia (100% O2 saturation) and hypoxia (40% O2 saturation) for 24 days. In both treatments, pouch fluid O2 saturation levels were lower compared with the surrounding water and decreased throughout the brooding period, reflecting greater offspring demand for O2 during development and/or decreasing paternal ability to provide O2 to the embryos. Male condition (hepatosomatic index) was negatively affected by hypoxia. Larger males had higher pouch fluid O2 saturation levels compared with smaller males, and levels were higher in the bottom section of the pouch compared with other sections. Embryo size was positively correlated with O2 availability, irrespective of their position in the pouch. Two important conclusions can be drawn from our findings. First, our results highlight a potential limitation to brooding within the pouch and dismiss the notion of closed brood pouches as well-oxygenated structures promoting the evolution of larger eggs in syngnathids. Second, we provide direct evidence that paternal care improves with male size in this species. This finding offers an explanation for the documented strong female preference for larger partners because, in terms of oxygenation, the brood pouch can restrict embryo growth.

Mean fecal glucocorticoid metabolites are associated with vigilance, whereas immediate cortisol levels better reflect acute anti-predator responses in meerkats.

Adrenal hormones likely affect anti-predator behavior in animals. With experimental field studies, we first investigated associations between mean fecal glucocorticoid metabolite (fGC) excretion and vigilance and with behavioral responses to alarm call playbacks in free-ranging meerkats (Suricata suricatta). We then tested how vigilance and behavioral responses to alarm call playbacks were affected in individuals administered exogenous cortisol. We found a positive association between mean fGC concentrations and vigilance behavior, but no relationship with the intensity of behavioral responses to alarm calls. However, in response to alarm call playbacks, individuals administered cortisol took slightly longer to resume foraging than control individuals treated with saline solution. Vigilance behavior, which occurs in the presence and absence of dangerous stimuli, serves to detect and avoid potential dangers, whereas responses to alarm calls serve to avoid immediate predation. Our data show that mean fGC excretion in meerkats was associated with vigilance, as a re-occurring anti-predator behavior over long time periods, and experimentally induced elevations of plasma cortisol affected the response to immediate threats. Together, our results indicate an association between the two types of anti-predator behavior and glucocorticoids, but that the underlying mechanisms may differ. Our study emphasizes the need to consider appropriate measures of adrenal activity specific to different contexts when assessing links between stress physiology and different anti-predator behaviors.

Reproductive compensation in broad-nosed pipefish females.

The differential allocation hypothesis assumes that animals should weigh costs and benefits of investing into reproduction with a current mate against the expected quality of future mates, and predicts that they should invest more into reproduction when pairing with a high-quality mate. In the broad-nosed pipefish (Syngnathus typhle), males care for the embryos in a brood pouch and females compete for access to male mating partners. Both sexes prefer mating with large partners. In the present study, we show that the same female provides both large and small mating partners with eggs of similar size, weight and lipid content when mated to two males in succession. Importantly, however, eggs provided to small males (less preferred) had higher egg protein content (11% more) than those provided to large males (preferred). Thus, contrary to the differential allocation hypothesis, eggs did not contain more resources when females mated with a larger male. Instead, the pattern observed in our results is consistent with a compensatory reproductive strategy.

Brooding fathers, not siblings, take up nutrients from embryos.

It is well known that many animals with placenta-like structures provide their embryos with nutrients and oxygen. However, we demonstrate here that nutrients can pass the other way, from embryos to the parent. The study was done on a pipefish, Syngnathus typhle, in which males brood fertilized eggs in a brood pouch for several weeks. Earlier research has found a reduction of embryo numbers during the brooding period, but the fate of the nutrients from these 'reduced' embryos has been unknown. In this study, we considered whether (i) the brooding male absorbs the nutrients, (ii) siblings absorb them, or (iii) a combination of both. Males were mated to two sets of females, one of which had radioactively labelled eggs (using (14)C-labelled amino acids), such that approximately half the eggs in the brood pouch were labelled. This allowed us to trace nutrient uptake from these embryos. We detected that (14)C-labelled amino acids were transferred to the male brood pouch, liver and muscle tissue. However, we did not detect any significant (14)C-labelled amino-acid absorption by the non-labelled half-siblings in the brood pouch. Thus, we show, to our knowledge, for the first time, that males absorb nutrients derived from embryos through their paternal brood pouch.