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Causes, consequences and evolution of inbreeding tolerance and avoidance in a cooperative mammal

Subject Area Evolutionary Cell and Developmental Biology (Zoology)
Sensory and Behavioural Biology
Evolution, Anthropology
Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Term from 2014 to 2019
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 263742823
 
Final Report Year 2020

Final Report Abstract

This project set out to explore the causes and consequences of inbreeding using rich, multigenerational data from a long-term study of a cooperatively breeding mammal, the banded mongoose (Mungos mungo). The main aims were to produce a large multigenerational pedigree and to use this to quantify the magnitude of inbreeding depression for multiple traits, to investigate inbreeding avoidance mechanisms, and to explore the interplay between inbreeding and cooperative behaviour. In order to address the first objective, we built upon an existing microsatellite dataset to generate a final dataset comprising a total of 1,940 individuals genotyped at up to 43 microsatellite loci and then used a combination of genetic parentage assignment approaches to construct a tengeneration deep pedigree comprising 1,725 maternal links and 1,625 paternal links. This dataset uncovered appreciable variance in inbreeding, with around 7% of individuals being strongly inbred, 13% of individuals being moderately inbred and 47% of the population being weakly inbred. To address the second objective, we investigated inbreeding depression for multiple life-history traits using pedigree-based inbreeding coefficients (fped) and standardized multilocus heterozygosity (sMLH). Within an information theoretic framework, we evaluated support for either fped or sMLH as inbreeding terms and used sequential regression to determine whether the residuals of sMLH on fped explained fitness variation above and beyond fped. We found no evidence of inbreeding depression for survival, either before or after nutritional independence. By contrast, inbreeding was negatively associated with two quality-related traits, yearling body mass and annual male reproductive success. The latter was best explained by both fped and residual sMLH, suggesting that genetic markers are capable of capturing variation in realized inbreeding above and beyond the pedigree expectation. To address the third objective, we used piecewise structural equation modeling to shed light on the cues that breeding females use to avoid inbreeding via extra-group mating. We found that, although females are able to adaptively adjust their extra-group breeding levels according to within-group inbreeding risk, they do not appear to alter their breeding patterns directly in response to their relatedness to within-group male breeders. Instead, they are more likely to breed with extra-group males when individual and societal factors indicate a high risk of inbreeding within their group. The limited reliability of these proxies of inbreeding risk may therefore help to explain why inbreeding still occurs frequently in this species. Finally, we exploited the unique “escorting” system of this species to investigate the interplay between inbreeding and altruistic behaviour. Specifically, we tested the hypothesis that that high levels of early-life care provided to young may create a relatively benign environment which offsets inbreeding depression, allowing inbred societies to evolve. We found that care provided by escorts mitigates the impact of inbreeding depression on pup survival and thus allows more pups to reach adulthood. However, as adults, inbred individuals provide less care, reducing the amount of help available to the next generation. This suggests that inbred societies may be rare in nature because the protective care that enables elevated levels of inbreeding is itself reduced by inbreeding depression. Taken together, the results of this project shed new light on the evolutionary ecology of inbreeding in wild populations.

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