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

2019 ◽  
Vol 374 (1770) ◽  
pp. 20180114 ◽  
Author(s):  
Emma I. K. Vitikainen ◽  
Faye J. Thompson ◽  
Harry H. Marshall ◽  
Michael A. Cant

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’.

Author(s):  
Carsten Schradin ◽  
Rainer H. Straub

“Nothing in Biology makes sense, except in the light of evolution.” This famous citation of Theodosius Dobzhansky also underlies the integrative field of evolutionary medicine, which faces the challenge to combine (patho-)physiological mechanisms with evolutionary function. Here we introduce a concept from the study of animal behavior, which are the four questions of Tinbergen that consider: 1. the ontogeny of an individual describing its development, 2. its physiological machinery, which 3. has fitness consequences influencing 4. the evolutionary history (phylogeny) of future generations. It is shown how this concept can be applied to infectious disease and to chronic inflammatory systemic diseases. Evolutionary medicine takes lifetime reproductive success into account. The hypothesis to be tested is that mechanisms underlying a disease in old age might have higher fitness benefits in the pre-reproductive and/or reproductive life history stage, leading to an overall increased lifetime fitness.


2019 ◽  
Vol 28 (5) ◽  
pp. 1127-1137 ◽  
Author(s):  
Justin R. Eastwood ◽  
Michelle L. Hall ◽  
Niki Teunissen ◽  
Sjouke A. Kingma ◽  
Nataly Hidalgo Aranzamendi ◽  
...  

2019 ◽  
Vol 32 (3) ◽  
pp. 243-251 ◽  
Author(s):  
Jeffrey A. Harvey ◽  
Lucas de Haan ◽  
Oriol Verdeny-Vilalta ◽  
Bertanne Visser ◽  
Rieta Gols

Abstract Closely related species in nature usually exhibit very similar phylogenetically conserved traits, such as reproduction, behavior and development. Here, we compared fecundity schedules, lifetime reproductive success and offspring sex ratios in three congeneric facultative hyperparasitoid wasps that exhibit several overlapping traits and which co-occur in the same small-scale habitats. Gelis agilis, G. proximus and G. hortensis are abundant in meadows and forest edge habitats in the Netherlands. Gelis agilis is asexual (all female), whereas the other two species reproduce sexually. Here they developed on cocoons of the primary parasitoid Cotesia glomerata. When provided with unlimited hosts, lifetime reproductive success was three times higher in G. proximus than in G. agilis with G. hortensis producing intermediate numbers of offspring. All three species depleted their teneral reserves during their lives. Females of G. proximus and G. hortensis lived significantly longer than females of G. agilis. Offspring sex ratios in young G. proximus mothers were female-biased and marginally male-biased in G. hortensis. As mothers aged, however, the ratio of male:female progeny produced rapidly increased until no daughters emerged later in life. Our results reveal significant differences in reproductive traits among the three species despite them co-occurring in the same microhabitats, being very closely related and morphologically similar. The increase in the production of male progeny by Gelis mothers over time suggests a depletion in sperm number or viability with age. This is especially interesting, given that Gelis species are among the least fecund parasitoids thus far studied. It is likely that in the field most Gelis mothers are probably only able to parasitize a few hosts and to maintain the production of female offspring.


FACETS ◽  
2017 ◽  
Vol 2 (1) ◽  
pp. 34-52 ◽  
Author(s):  
Ashley Guncay ◽  
Thiropa Balasubramaniam ◽  
Katie Plagens ◽  
Joel Weadge ◽  
Tristan A.F. Long

In some species where males make no direct contribution to a female’s lifetime reproductive success, females choose mates based on the indirect benefits manifested in their offspring. One trait that may be subject to this sexual selection is immunocompetence (the ability to mount an immune response following exposure to pathogens); however, the results of previous work on its link to male attractiveness have been ambiguous. Herein we examine the life history consequences of mating with males with a history of failure or success in reproductive competitions in Drosophila melanogaster. By examining egg-to-adult survival, body weights, and bacterial loads of offspring reared in either the absence or presence of a bacterial pathogen, we were able to examine whether sire reproductive success was associated with their offsprings’ ability to respond to an immunological challenge and other life history traits. Our results are partially consistent with the predictions of the “immunocompetence handicap hypothesis”: competitively successful males (“studs”) sire male offspring that are better able to handle an immunological challenge than those sired by competitively unsuccessful males (“duds”). However, our assay also revealed the opposite pattern in female offspring, suggestive of the complicating presence of alleles with sexually antagonistic effects on the expression of this important life history trait.


2018 ◽  
Vol 115 (8) ◽  
pp. 1860-1864 ◽  
Author(s):  
Changcao Wang ◽  
Xin Lu

How can altruism evolve or be maintained in a selfish world? Hamilton’s rule shows that the former process will occur when rb > c—the benefits to the recipients of an altruistic act b, weighted by the relatedness between the social partners r, exceed the costs to the altruists c—drives altruistic genotypes spreading against nonaltruistic ones. From this rule, we infer that altruistic genotypes will persist in a population by forming a stable heritable polymorphism with nonaltruistic genotypes if rb = c makes inclusive fitness of the two morphs equal. We test this prediction using the data of 12 years of study on a cooperatively breeding bird, the Tibetan ground tit Pseudopodoces humilis, where helping is performed by males only and kin-directed. Individual variation in ever acting as a helper was heritable (h2 = 0.47), and the resultant altruism polymorphism remained stable as indicated by low-level annual fluctuation of the percentage of helpers among all adult males (24–28%). Helpers’ indirect fitness gains from increased lifetime reproductive success of related breeders statistically fully compensated for their lifetime direct fitness losses, suggesting that rb = c holds. While our work provides a fundamental support for Hamilton’s idea, it highlights the equivalent inclusive fitness returns to altruists and nonaltruists mediated by rb = c as a theoretically and realistically important mechanism to maintain social polymorphism.


2020 ◽  
Vol 117 (40) ◽  
pp. 24909-24919 ◽  
Author(s):  
Chelsea J. Weibel ◽  
Jenny Tung ◽  
Susan C. Alberts ◽  
Elizabeth A. Archie

In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.


2020 ◽  
Vol 167 (10) ◽  
Author(s):  
Matthew J. Powers ◽  
Ryan J. Weaver ◽  
Kyle B. Heine ◽  
Geoffrey E. Hill

2007 ◽  
Vol 274 (1618) ◽  
pp. 1603-1609 ◽  
Author(s):  
Andrew J Young ◽  
Goran Spong ◽  
Tim Clutton-Brock

In cooperatively breeding species, subordinates typically suffer strong constraints on within-group reproduction. While numerous studies have highlighted the additional fitness benefits that subordinates might accrue through helping, few have considered the possibility that subordinates may also seek extra-group matings to improve their chances of actually breeding. Here, we show that subordinate males in cooperative meerkat, Suricata suricatta , societies conduct frequent extraterritorial forays, during periods of peak female fertility, which give rise to matings with females in other groups. Genetic analyses reveal that extra-group paternity (EGP) accrued while prospecting contributes substantially to the reproductive success of subordinates: yielding the majority of their offspring (approx. 70%); significantly reducing their age at first reproduction and allowing them to breed without dispersing. We estimate that prospecting subordinates sire 20–25% of all young in the population. While recent studies on cooperative birds indicate that dominant males accrue the majority of EGP, our findings reveal that EGP can also arise from alternative reproductive tactics employed exclusively by subordinates. It is important, therefore, that future attempts to estimate the fitness of subordinate males in animal societies quantify the distribution of extra-group as well as within-group paternity, because a substantial proportion of the reproductive success of subordinates may otherwise go undetected.


2021 ◽  
Vol 288 (1957) ◽  
pp. 20210579
Author(s):  
Sahas Barve ◽  
Christina Riehl ◽  
Eric L. Walters ◽  
Joseph Haydock ◽  
Hannah L. Dugdale ◽  
...  

Cooperative breeding strategies lead to short-term direct fitness losses when individuals forfeit or share reproduction. The direct fitness benefits of cooperative strategies are often delayed and difficult to quantify, requiring data on lifetime reproduction. Here, we use a longitudinal dataset to examine the lifetime reproductive success of cooperative polygamy in acorn woodpeckers ( Melanerpes formicivorus ), which nest as lone pairs or share reproduction with same-sex cobreeders. We found that males and females produced fewer young per successful nesting attempt when sharing reproduction. However, males nesting in duos and trios had longer reproductive lifespans, more lifetime nesting attempts and higher lifetime reproductive success than those breeding alone. For females, cobreeding in duos increased reproductive lifespan so the lifetime reproductive success of females nesting in duos was comparable to those nesting alone and higher than those nesting in trios. These results suggest that for male duos and trios, reproductive success alone may provide sufficient fitness benefits to explain the presence of cooperative polygamy, and the benefits of cobreeding as a duo in females are higher than previously assumed. Lifetime individual fitness data are crucial to reveal the full costs and benefits of cooperative polygamy.


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