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Molecular Basis of Eusocial Complexity: The Case of Worker Reproductivity in Bees
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK.
Örebro University, School of Medical Sciences. Örebro University Hospital. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK.ORCID iD: 0000-0001-6416-052x
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK.
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK.
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2024 (English)In: Genome Biology and Evolution, E-ISSN 1759-6653, Vol. 16, no 12, article id evae269Article in journal (Refereed) Published
Abstract [en]

In eusocial insects, the molecular basis of worker reproductivity, including how it changes with eusocial complexity, remains relatively poorly understood. To address this, we used mRNA-seq to isolate genes differentially expressed between ovary-active and ovary-inactive workers in the intermediately eusocial bumblebee Bombus terrestris. By comparisons with data from the advanced eusocial honeybee Apis mellifera, which shows reduced worker reproductivity, we characterized gene expression differences associated with change in worker reproductivity as a function of eusocial complexity. By comparisons with genes associated with queen-worker caste development in B. terrestris larvae, we tested the behavioral-morphological caste homology hypothesis, which proposes co-option of genes influencing reproductive division of labor in adults in morphological caste evolution. We conducted comparisons having isolated genes expressed in B. terrestris worker-laid eggs to remove the potential confound caused by gene expression in eggs. Gene expression differences between the B. terrestris worker phenotypes were mainly in fat body and ovary, not brain. Many genes (86%) more highly expressed in ovary of ovary-active workers were also expressed in worker-laid eggs, confirming egg-expressed genes were potentially confounding. Comparisons across B. terrestris and A. mellifera, and with B. terrestris larvae, returned significant percentage overlaps in differentially expressed genes and/or enriched Gene Ontology terms, suggesting conserved gene functions underpin worker reproductivity as it declines with increasing eusocial complexity and providing support for the behavioral-morphological caste homology hypothesis. Therefore, within bees, both a degree of conserved gene use and gene co-option appear to underlie the molecular basis of worker reproductivity and morphological caste evolution.

Place, publisher, year, edition, pages
Oxford University Press, 2024. Vol. 16, no 12, article id evae269
Keywords [en]
Apis, Bombus, gene expression, mRNA-seq, evolution of eusociality, worker reproduction
National Category
Genetics and Genomics
Identifiers
URN: urn:nbn:se:oru:diva-118509DOI: 10.1093/gbe/evae269ISI: 001383405300001PubMedID: 39663835Scopus ID: 2-s2.0-85214012757OAI: oai:DiVA.org:oru-118509DiVA, id: diva2:1928225
Note

This work was supported by the UK’s Biotechnology and Biological Sciences Research Council (BBSRC grant reference number BB/M001482/1) and Natural Environment Research Council (NERC research grant reference numbers NE/L006758/1, NE/R000875/1). Laboratory work (library preparation and sequencing) was supported and performed by the NERC Biomolecular Analysis Facility (NBAF) at the University of Edinburgh (Edinburgh Genomics). Edinburgh Genomics is partly supported through core grants from BBSRC (BB/T017864/1) and NERC (UKSBS PR18037).

Available from: 2025-01-16 Created: 2025-01-16 Last updated: 2025-02-07Bibliographically approved

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