Abstract

Eusocial insects provide special opportunities to elucidate the evolution of ageing as queens have apparently evaded costs of reproduction and reversed the fecundity–longevity trade-off generally observed in non-social organisms. But how reproduction affects longevity in eusocial insects has rarely been tested experimentally. In this study, we took advantage of the reproductive plasticity of workers to test the causal role of reproduction in determining longevity in eusocial insects. Using the eusocial bumblebee Bombus terrestris, we found that, in whole colonies, in which workers could freely ‘choose’ whether to become reproductive, workers' level of ovarian activation was significantly positively associated with longevity and ovary-active workers significantly outlived ovary-inactive workers. By contrast, when reproductivity was experimentally induced in randomly selected workers, thereby decoupling it from other traits, workers' level of ovarian activation was significantly negatively associated with longevity and ovary-active workers were significantly less long-lived than ovary-inactive workers. These findings show that workers experience costs of reproduction and suggest that intrinsically high-quality individuals can overcome these costs. They also raise the possibility that eusocial insect queens exhibit condition-dependent longevity and hence call into question whether eusociality entails a truly reversed fecundity–longevity trade-off involving a fundamental remodelling of conserved genetic and endocrine networks underpinning ageing.

Highlights

  • The evolution of ageing, costs of reproduction and life history represent central, interlinked topics in evolutionary ecology [1,2,3]

  • Our findings show that reproductive workers in B. terrestris experience costs of reproduction as in non-social organisms and that they do not exhibit a genuine reversal of the negative fecundity–longevity trade-off

  • We conclude that B. terrestris workers experience costs of reproduction and we hypothesize that intrinsic quality differences between individuals account for the apparently reversed fecundity–longevity trade-off among workers in whole colonies

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Summary

Introduction

The evolution of ageing, costs of reproduction and life history represent central, interlinked topics in evolutionary ecology [1,2,3]. In Experiment 1, we tested for the existence and directionality of the association of worker longevity and reproduction (ovarian activation) in queenright (with a queen) or queenless whole colonies in which workers could freely ‘choose’ whether to become reproductive or not ( termed ‘whole colonies’) This confirmed that, in B. terrestris as in other species, individuals that become reproductive in whole colonies live longer than non-reproductive ones. In Experiment 2, levels of ovarian activation and relative rates of non-agonistic worker behaviours were analysed with linear models (LMs) or linear mixed model (LMMs) with group membership as a random factor conditional on the presence of dependent observations. Full details of statistical model fitting and testing of model assumptions are provided in the electronic supplementary 4 material, tables S1 – S6

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