Costs of reproduction are present but latent in eusocial bumblebee queens

Collins, David H., Prince, David C., Donelan, Jenny L., Chapman, Tracey and Bourke, Andrew F. G. ORCID: (2023) Costs of reproduction are present but latent in eusocial bumblebee queens. BMC Biology, 21. ISSN 1741-7007

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Background: The standard evolutionary theory of ageing proposes that ageing occurs because of a trade-off between reproduction and longevity. Eusocial insect queens exhibit positive fecundity-longevity associations and so have been suggested to be counter-examples through not expressing costs of reproduction and through remodelling conserved genetic and endocrine networks regulating ageing and reproduction. If so, eusocial evolution from solitary ancestors with negative fecundity-longevity associations must have involved a stage at which costs of reproduction were suppressed and fecundity and longevity became positively associated. Using the bumblebee (Bombus terrestris), we experimentally tested whether queens in annual eusocial insects at an intermediate level of eusocial complexity experience costs of reproduction, and, using mRNA-seq, the extent to which they exhibit a remodelling of relevant genetic and endocrine networks. Specifically, we tested whether costs of reproduction are present but latent, or whether a remodelling of relevant genetic and endocrine networks has already occurred allowing queens to reproduce without costs. Results: We experimentally increased queens’ costs of reproduction by removing their eggs, which caused queens to increase their egg-laying rate. Treatment queens had significantly reduced longevity relative to control queens whose egg-laying rate was not increased. Reduced longevity in treatment queens was not caused by increased worker-to-queen aggression or by increased overall activity in queens. In addition, treatment and control queens differed in age-related gene expression based on mRNA-seq in both their overall expression profiles and the expression of ageing-related genes. Remarkably, these differences appeared to occur principally with respect to relative age, not chronological age. Conclusions: This study represents the first simultaneously phenotypic and transcriptomic experimental test for a longevity cost of reproduction in eusocial insect queens. The results support the occurrence of costs of reproduction in annual eusocial insects of intermediate social complexity and suggest that reproductive costs are present but latent in queens of such species, i.e. that these queens exhibit condition-dependent positive fecundity-longevity associations. They also raise the possibility that a partial remodelling of genetic and endocrine networks underpinning ageing may have occurred in intermediately eusocial species such that, in unmanipulated conditions, age-related gene expression depends more on chronological than relative age.

Item Type: Article
Additional Information: Funding Information: This work was funded by the UK’s Natural Environment Research Council (NERC research grant reference number NE/R000875/1). Edinburgh Genomics is partly supported through core grants from BBSRC (BB/T017864/1) and NERC (UKSBS PR18037).
Uncontrolled Keywords: age-related gene expression,bombus terrestris,costs of reproduction,eusociality,evolutionary theory of ageing,mrna-seq,biotechnology,structural biology,ecology, evolution, behavior and systematics,physiology,biochemistry, genetics and molecular biology(all),agricultural and biological sciences(all),plant science,developmental biology,cell biology ,/dk/atira/pure/subjectarea/asjc/1300/1305
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 01 Aug 2023 12:32
Last Modified: 08 Aug 2023 08:30
DOI: 10.1186/s12915-023-01648-5


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