The past, present and future of reproductive skew theory and experiments

Peter Nonacs, Reinmar Hager

    Research output: Contribution to journalArticlepeer-review

    Abstract

    A major evolutionary question is how reproductive sharing arises in cooperatively breeding species despite the inherent reproductive conflicts in social groups. Reproductive skew theory offers one potential solution: each group member gains or is allotted inclusive fitness equal to or exceeding their expectation from reproducing on their own. Unfortunately, a multitude of skew models with conflicting predictions has led to confusion in both testing and evaluating skew theory. The confusion arises partly because one set of models (the 'transactional' type) answer the ultimate evolutionary question of what ranges of reproductive skew can yield fitness-enhancing solutions for all group members. The second set of models ('compromise') give an evolutionarily proximate, game-theoretic evolutionarily stable state (ESS) solution that determines reproductive shares based on relative competitive abilities. However, several predictions arising from compromise models require a linear payoff to increased competition and do not hold with non-linear payoffs. Given that for most species it may be very difficult or impossible to determine the true relationship between effort devoted to competition and reproductive share gained, compromise models are much less predictive than previously appreciated. Almost all skew models make one quantitative prediction (e.g. realized skew must fall within ranges predicted by transactional models), and two qualitative predictions (e.g. variation in relatedness or competitive ability across groups affects skew). A thorough review of the data finds that these three predictions are relatively rarely supported. As a general rule, therefore, the evolution of cooperative breeding appears not to be dependent on the ability of group members to monitor relatedness or competitive ability in order to adjust their behaviour dynamically to gain reproductive share. Although reproductive skew theory fails to predict within-group dynamics consistently, it does better at predicting quantitative differences in skew across populations or species. This suggests that kin selection can play a significant role in the evolution of sociality. To advance our understanding of reproductive skew will require focusing on a broader array of factors, such as the frequency of mistaken identity, delayed fitness payoffs, and selection pressures arising from across-group competition. We furthermore suggest a novel approach to investigate the sharing of reproduction that focuses on the underlying genetics of skew. A quantitative genetics approach allows the partitioning of variance in reproductive share itself or that of traits closely associated with skew into genetic and non-genetic sources. Thus, we can determine the heritability of reproductive share and infer whether it actually is the focus of natural selection. We view the 'animal model' as the most promising empirical method where the genetics of reproductive share can be directly analyzed in wild populations. In the quest to assess whether skew theory can provide a framework for understanding the evolution of sociality, quantitative genetics will be a central tool in future research. © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society.
    Original languageEnglish
    Pages (from-to)271-298
    Number of pages27
    JournalBiological Reviews
    Volume86
    Issue number2
    DOIs
    Publication statusPublished - May 2011

    Keywords

    • Animal model
    • Cooperative breeding
    • Game theory
    • Indirect genetic effects
    • Kin selection
    • Maternal effects
    • Quantitative genetics
    • Reproductive skew
    • Sociality

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