Abstract

Monogamy is associated with sibling-directed altruism in multiple animal taxa, including insects, birds and mammals. Inclusive-fitness theory readily explains this pattern by identifying high relatedness as a promoter of altruism. In keeping with this prediction, monogamy should promote the evolution of voluntary sterility in insect societies if sterile workers make for better helpers. However, a recent mathematical population-genetics analysis failed to identify a consistent effect of monogamy on voluntary worker sterility. Here, we revisit that analysis. First, we relax genetic assumptions, considering not only alleles of extreme effect—encoding either no sterility or complete sterility—but also alleles with intermediate effects on worker sterility. Second, we broaden the stability analysis—which focused on the invasibility of populations where either all workers are fully sterile or all workers are fully reproductive—to identify where intermediate pure or mixed evolutionarily stable states may occur. Third, we consider a broader range of demographically explicit ecological scenarios relevant to altruistic worker non-reproduction and to the evolution of eusociality more generally. We find that, in the absence of genetic constraints, monogamy always promotes altruistic worker sterility and may inhibit spiteful worker sterility. Our extended analysis demonstrates that an exact population-genetics approach strongly supports the prediction of inclusive-fitness theory that monogamy promotes sib-directed altruism in social insects.

Highlights

  • Altruism among animals is epitomized by the workers of eusocial insect societies, who sacrifice their personal reproductive success to promote their siblings’ welfare [1]

  • We find that a more-comprehensive investigation of Olejarz et al.’s [19] exact population-genetics approach strongly supports the view that monogamy promotes altruistic worker sterility in insect societies and corroborates inclusive-fitness theory more generally

  • By relaxing the strong genetic constraints imposed by the analysis of Olejarz et al [19], monogamy always promotes the invasion of non-spiteful worker sterility relative to promiscuity

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Summary

Introduction

Altruism among animals is epitomized by the workers of eusocial insect societies, who sacrifice their personal reproductive success to promote their siblings’ welfare [1]. Worker sterility may represent a trade-off between personal reproduction and sibling welfare, to how the evolution of eusociality involves individuals forgoing dispersal in order to join an unmated worker caste [8,9,10] As both empirical [13] and theoretical [12,17,18] studies have demonstrated that high relatedness promotes the evolution of a sterile worker caste, a standard account of inclusive-fitness theory might predict that—as with other forms of sibling altruism—monogamy should promote voluntary worker sterility. We find that a more-comprehensive investigation of Olejarz et al.’s [19] exact population-genetics approach strongly supports the view that monogamy promotes altruistic worker sterility in insect societies and corroborates inclusive-fitness theory more generally

Model and results
Unconstrained allelic effects: monogamy promotes worker sterility
Recessive worker-sterility alleles only
Dominant worker-sterility alleles only
Any worker-sterility alleles
Beyond invasion: monogamy promotes worker sterility
Alternative ecological scenarios: monogamy promotes worker sterility
Discussion
Spiteful worker sterility and policing
Explicit population-genetics analysis
Numerical experiments
Evolutionarily stable strategy analysis
Demographically explicit ecological scenarios
Stable level of sterility
Stochastic individual-based model
Reproductive offspring if the mutant allele is dominant
Reproductive offspring if the mutant allele is recessive
Condition for invasion of a dominant mutant sterility allele
Condition for invasion of a recessive mutant sterility allele
Relatedness calculations
Findings
Class reproductive values
Full Text
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