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

2019 ◽  
Vol 374 (1770) ◽  
pp. 20180117 ◽  
Author(s):  
Ben Dantzer ◽  
Constance Dubuc ◽  
Ines Braga Goncalves ◽  
Dominic L. Cram ◽  
Nigel C. Bennett ◽  
...  

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’.

2018 ◽  
Author(s):  
Ben Dantzer ◽  
Constance Dubuc ◽  
Ines Braga Goncalves ◽  
Dominic L. Cram ◽  
Nigel C. Bennett ◽  
...  

AbstractThe 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.


2019 ◽  
Vol 374 (1770) ◽  
pp. 20180110 ◽  
Author(s):  
Willem E. Frankenhuis ◽  
Daniel Nettle ◽  
Sasha R. X. Dall

There is enduring debate over the question of which early-life effects are adaptive and which ones are not. Mathematical modelling shows that early-life effects can be adaptive in environments that have particular statistical properties, such as reliable cues to current conditions and high autocorrelation of environmental states. However, few empirical studies have measured these properties, leading to an impasse. Progress, therefore, depends on research that quantifies cue reliability and autocorrelation of environmental parameters in real environments. These statistics may be different for social and non-social aspects of the environment. In this paper, we summarize evolutionary models of early-life effects. Then, we discuss empirical data on environmental statistics from a range of disciplines. We highlight cases where data on environmental statistics have been used to test competing explanations of early-life effects. We conclude by providing guidelines for new data collection and reflections on future directions. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine'.


2019 ◽  
Vol 374 (1770) ◽  
pp. 20190039 ◽  
Author(s):  
Bram Kuijper ◽  
Mark A. Hanson ◽  
Emma I. K. Vitikainen ◽  
Harry H. Marshall ◽  
Susan E. Ozanne ◽  
...  

Variation in early-life conditions can trigger developmental switches that lead to predictable individual differences in adult behaviour and physiology. Despite evidence for such early-life effects being widespread both in humans and throughout the animal kingdom, the evolutionary causes and consequences of this developmental plasticity remain unclear. The current issue aims to bring together studies of early-life effects from the fields of both evolutionary ecology and biomedicine to synthesise and advance current knowledge of how information is used during development, the mechanisms involved, and how early-life effects evolved. We hope this will stimulate further research into early-life effects, improving our understanding of why individuals differ and how this might influence their susceptibility to disease.This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.


2019 ◽  
Vol 374 (1770) ◽  
pp. 20180113 ◽  
Author(s):  
Étienne Danchin ◽  
Arnaud Pocheville ◽  
Philippe Huneman

Recent discoveries show that early in life effects often have long-lasting influences, sometimes even spanning several generations. Such intergenerational effects of early life events appear not easily reconcilable with strict genetic inheritance. However, an integrative evolutionary medicine of early life effects needs a sound view of inheritance in development and evolution. Here, we show how to articulate the gene-centred and non-gene-centred visions of inheritance. We first recall the coexistence of two gene concepts in scientific discussions, a statistical one (focused on patterns of parent–offspring resemblance, and implicitly including non-DNA-sequence-based resemblance), and a molecular one (based on the DNA sequence). We then show how all the different mechanisms of inheritance recently discovered can be integrated into an inclusive theory of evolution where different mechanisms would enable adaptation to changing environments at different timescales. One surprising consequence of this integrative vision of inheritance is that early in life effects start much earlier than fertilization.This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.


2019 ◽  
Vol 374 (1770) ◽  
pp. 20180111 ◽  
Author(s):  
Bram Kuijper ◽  
Rufus A. Johnstone

Numerous studies have shown that social adversity in early life can have long-lasting consequences for social behaviour in adulthood, consequences that may in turn be propagated to future generations. Given these intergenerational effects, it is puzzling why natural selection might favour such sensitivity to an individual’s early social environment. To address this question, we model the evolution of social sensitivity in the development of helping behaviours, showing that natural selection indeed favours individuals whose tendency to help others is dependent on early-life social experience. In organisms with non-overlapping generations, we find that natural selection can favour positive social feedbacks, in which individuals who received more help in early life are also more likely to help others in adulthood, while individuals who received no early-life help develop low tendencies to help others later in life. This positive social sensitivity is favoured because of an intergenerational relatedness feedback: patches with many helpers tend to be more productive, leading to higher relatedness within the local group, which in turn favours higher levels of help in the next generation. In organisms with overlapping generations, this positive feedback is less likely to occur, and those who received more help may instead be less likely to help others (negative social feedback). We conclude that early-life social influences can lead to strong between-individual differences in helping behaviour, which can take different forms dependent on the life history in question. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.


2014 ◽  
Vol 29 (2) ◽  
pp. 268-276 ◽  
Author(s):  
Timothy S. Mitchell ◽  
Jessica A. Maciel ◽  
Fredric J. Janzen

2021 ◽  
Vol 18 (1) ◽  
Author(s):  
Lucia Mentesana ◽  
Martin N. Andersson ◽  
Stefania Casagrande ◽  
Wolfgang Goymann ◽  
Caroline Isaksson ◽  
...  

Abstract Background In egg-laying animals, mothers can influence the developmental environment and thus the phenotype of their offspring by secreting various substances into the egg yolk. In birds, recent studies have demonstrated that different yolk substances can interactively affect offspring phenotype, but the implications of such effects for offspring fitness and phenotype in natural populations have remained unclear. We measured natural variation in the content of 31 yolk components known to shape offspring phenotypes including steroid hormones, antioxidants and fatty acids in eggs of free-living great tits (Parus major) during two breeding seasons. We tested for relationships between yolk component groupings and offspring fitness and phenotypes. Results Variation in hatchling and fledgling numbers was primarily explained by yolk fatty acids (including saturated, mono- and polyunsaturated fatty acids) - but not by androgen hormones and carotenoids, components previously considered to be major determinants of offspring phenotype. Fatty acids were also better predictors of variation in nestling oxidative status and size than androgens and carotenoids. Conclusions Our results suggest that fatty acids are important yolk substances that contribute to shaping offspring fitness and phenotype in free-living populations. Since polyunsaturated fatty acids cannot be produced de novo by the mother, but have to be obtained from the diet, these findings highlight potential mechanisms (e.g., weather, habitat quality, foraging ability) through which environmental variation may shape maternal effects and consequences for offspring. Our study represents an important first step towards unraveling interactive effects of multiple yolk substances on offspring fitness and phenotypes in free-living populations. It provides the basis for future experiments that will establish the pathways by which yolk components, singly and/or interactively, mediate maternal effects in natural populations.


2017 ◽  
Vol 284 (1863) ◽  
pp. 20171248 ◽  
Author(s):  
Ben Dantzer ◽  
Ines Braga Goncalves ◽  
Helen C. Spence-Jones ◽  
Nigel C. Bennett ◽  
Michael Heistermann ◽  
...  

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.


2018 ◽  
Vol 285 (1885) ◽  
pp. 20181164 ◽  
Author(s):  
Philip A. Downing ◽  
Ashleigh S. Griffin ◽  
Charlie K. Cornwallis

The evolution of helping behaviour in species that breed cooperatively in family groups is typically attributed to kin selection alone. However, in many species, helpers go on to inherit breeding positions in their natal groups, but the extent to which this contributes to selection for helping is unclear as the future reproductive success of helpers is often unknown. To quantify the role of future reproduction in the evolution of helping, we compared the helping effort of female and male retained offspring across cooperative birds. The kin selected benefits of helping are equivalent between female and male helpers—they are equally related to the younger siblings they help raise—but the future reproductive benefits of helping differ because of sex differences in the likelihood of breeding in the natal group. We found that the sex which is more likely to breed in its natal group invests more in helping, suggesting that in addition to kin selection, helping in family groups is shaped by future reproduction.


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