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Live long and prosper: durable benefits of early-life care in banded mongooses.

ABSTRACT: Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses ( Mungos mungo) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called 'escorts' form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se, over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

SUBMITTER: Vitikainen EIK

PROVIDER: S-EPMC6460079 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Live long and prosper: durable benefits of early-life care in banded mongooses.

Vitikainen Emma I K EIK Thompson Faye J FJ Marshall Harry H HH Cant Michael A MA

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20190401 1770

Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in coopera ...[more]

PMID: 30966878

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Project description:Intergroup conflict is widespread in nature and is proposed to have strong impacts on the evolution of social behavior. The conflict-cohesion hypothesis predicts that exposure to intergroup conflict should lead to increased social cohesion to improve group success or resilience in future conflicts. There is evidence to support this prediction from studies of affiliative responses to outgroup threats in some animal societies. However, most of these studies have focused on behavioral changes over short time periods (minutes and hours after exposure to an outgroup), and hence very little is known about the dynamics and durability of responses to intergroup conflict over the longer term. We investigated this question by simulating intergroup encounters in wild banded mongooses (Mungos mungo) and measuring social behavior before, during, and after these encounters over a 5-day period. We also ran control trials with non-threatening stimuli. Banded mongooses reacted immediately to intrusion stimuli by vocalizing, grouping together, and advancing on the stimulus. In the first 5 min after simulated intrusions, we saw an elevation in grooming levels, but in the hour after exposure grooming rates declined sharply, contrary to our expectation. In the two subsequent days, grooming rates remained at this depressed rate. In control trials, the initial increase in grooming was not seen, but grooming declined compared to the longer-term time periods. Grooming changed across time, but not in the same pattern as during intrusions, suggesting that intrusions had an impact above and beyond that of the experimental setup. The dynamics of grooming responses were short lived and more complex than we initially expected. We suggest this unexpected result may be linked to the frequency of aggressive intergroup encounters in this system. As control and experimental trials were run at different times of year, future work would be needed to confirm that these relative patterns are replicable. Our results indicate short-lived impacts of outgroup threat on measures of social cohesion in this species, but cannot confirm longer-term changes.

Project description:BACKGROUND:Glucocorticoids mediate responses to perceived stressors, thereby restoring homeostasis. However, prolonged glucocorticoid elevation may cause homeostatic overload. Using extensive field investigations of banded mongoose (Mungos mungo) groups in northern Botswana, we assessed the influence of reproduction, predation risk, and food limitation on apparent homeostatic overload (n=13 groups, 1542 samples from 268 animals). We experimentally manipulated reproduction and regulated food supply in captive mongooses, and compared their glucocorticoid responses to those obtained from free-living groups. RESULTS:At the population level, variation in glucocorticoid levels in free-living mongooses was explained by food limitation: fecal organic matter, recent rainfall, and access to concentrated anthropogenic food resources. Soil macrofauna density and reproductive events explained less and predation risk very little variation in glucocorticoid levels. Reproduction and its associated challenges alone (under regulated feeding conditions) increased glucocorticoid levels 19-fold in a captive group. Among free-living groups, glucocorticoid elevation was seasonal (occurring in late dry season or early wet season when natural food resources were less available), but the timing of peak glucocorticoid production was moderated by access to anthropogenic resources (groups with fewer anthropogenic food sources had peaks earlier in dry seasons). Peak months represented 12- and 16-fold increases in glucocorticoids relative to nadir months with some animals exhibiting 100-fold increases. Relative to the captive group nadir, some free-living groups exhibited 60-fold increases in peak glucocorticoid levels with some animals exhibiting up to 800-fold increases. Most of these animals exhibited 1- to 10-fold increases relative to the captive animal peak. CONCLUSIONS:Banded mongooses exhibit seasonal chronic glucocorticoid elevation, associated primarily with food limitation and secondarily with reproduction. Magnitude and duration of this elevation suggests that this may be maladaptive for some animals, with possible fitness consequences. In late dry season, this population may face a convergence of stressors (food limitation, agonistic encounters at concentrated food resources, evictions, estrus, mate competition, parturition, and predation pressure on pups), which may induce homeostatic overload.

Dataset Information

Live long and prosper: durable benefits of early-life care in banded mongooses.

Publications

Live long and prosper: durable benefits of early-life care in banded mongooses.

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