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

Abstract

2The phenotype of parents can have long-lasting effects on the development of offspring 2 3 as well as on their behaviour, physiology, and morphology as adults. In some cases, 2 4 these changes may increase offspring fitness but, in others, they can elevate parental 2 5 fitness at a cost to the fitness of their offspring. We show that in Kalahari meerkats 2 6 (Suricata suricatta), the circulating glucocorticoid (GC) hormones of pregnant females 2 7 affect the growth and cooperative behaviour of their offspring. We performed a 3-year 2 8 experiment in wild meerkats to test the hypothesis that GC-mediated maternal effects 2 9 reduce the potential for offspring to reproduce directly and therefore cause them to 3 0 exhibit more cooperative behaviour. Daughters (but not sons) born to mothers treated 3 1 with cortisol during pregnancy were smaller early in life and exhibited significantly more 3 2 of two types of cooperative behaviour (pup rearing and feeding) once they were adults 3 3 compared to offspring from control mothers. They also had lower measures of GCs as 3 4 they aged, which could explain the observed increases in cooperative behaviour. 3 5 Because early growth is a crucial determinant of fitness in female meerkats, our results 3 6 indicate that GC-mediated maternal effects may reduce the fitness of offspring, but may 3 7 elevate parental fitness as a consequence of increasing the cooperative behaviour of 3 8 their daughters. 3 9 4 0

Maternal glucocorticoids have minimal effects on HPA axis activity and behavior of juvenile wild North American red squirrels

“…Research on the impacts of elevated postnatal GCs or increased postnatal exposure to stressors is less common. Some studies show that postnatal treatment of mothers with GCs can downregulate the activity of the HPA axis in offspring (Grace and Anderson, 2018;Grace et al, 2020), although we note that the effects of early-life exposure to GCs or stressful experiences on HPA axis-reactivity depend upon the species and that these effects can be sex-specific (Dantzer et al, 2019;Grace and Anderson, 2018;Grace et al, 2020;Marasco et al, 2012;Spencer et al, 2009). Although we did find that offspring from Journal of Experimental Biology • Accepted manuscript mothers treated with GCs during pregnancy did not have a more reactive HPA axis, there was a trend for offspring from mothers treated with GCs during lactation to have reduced HPA axis reactivity as measured using AUC (p = 0.11, Table 3A), and plasma cortisol concentrations 30 min after the ACTH injection (p = 0.055, Table S4).…”

Prenatal environmental conditions underlie alternative reproductive tactics that drive the formation of a mixed-kin cooperative society

“…Studies of two other avian species, western bluebirds (Sialia mexicana) and great tits (Parus major), found an effect of maternal androgen deposition on offspring dispersal in response to ecological conditions 18,19 . Viviparous lizards (Lacerta vivipara) show a similar effect 46 , and maternal hormones have also been shown to increase helping behavior in subordinate female meerkats (Suricata suricatta) 22 . Alternatively, conditions experienced by parents may affect their behavior towards their offspring after birth, such that dispersal is driven purely by behavioral interactions prior to offspring becoming self-sufficient 47,48 .…”

“…Male superb starlings are more likely to become alloparents and help more than females 38 , and alloparents buffer the detrimental effects of harsh environmental conditions on reproductive success in this species 41 . Thus, prenatal parental effects promoting alloparental behavior following harsher prenatal conditions might serve to selfishly increase the parents' short-term future reproductive success and indirectly limit dispersal of male offspring 22 . Although males born following benign prenatal conditions could, conversely, be more likely to disperse so as to reduce kin competition, this seems less probable because kin competition has actually been shown to decrease under benign environmental conditions in other cooperatively breeding species 50,51 .…”

“…Parental effects may be particularly important in cooperatively breeding species 21 , where parents can limit offspring dispersal by influencing helping behavior or promote dispersal to reduce kin competition 19,22,23 . Although dispersal in most social species tends to be sex-biased 24 , in many cooperative breeders, individuals of one sex can adopt either of two alternative reproductive tactics: natal dispersal or philopatry 8,15 .…”

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

“…Data accessibility. All data are available in the Dryad Digital Repository: https://doi.org/10.5061/dryad.260t0rm [74]. All code for statistical analyses is available from the first author.…”