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Cuticular and Dufour’s Gland Chemistry Reflect Reproductive and Social State in the Facultatively Eusocial Sweat Bee Megalopta genalis (Hymenoptera: Halictidae)

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Abstract

Queen pheromones evolved independently in multiple eusocial insect lineages, in which they mediate reproductive conflict by inhibiting worker ovarian development. Although fundamentally important for reproductive division of labor – the hallmark of eusociality – their evolutionary origins are enigmatic. Here, we analyze cuticular and Dufour’s gland chemistries across alternative social and reproductive phenotypes in Megalopta genalis bees (tribe Augochlorini, family Halictidae) that facultatively express simple eusociality. Reproductive bees have distinct overall glandular and cuticular chemical phenotypes compared with non-reproductive workers. On the cuticle, a likely site of signal transmission, reproductives are enriched for certain alkenes, most linear alkanes, and are heavily enriched for all methyl-branched alkanes. Chemicals belonging to these compound classes are known to function as fertility signals in other eusocial insect taxa. Some macrocyclic lactones, compounds that serve as queen pheromones in the other eusocial halictid tribe (Halictini), are also enriched among reproductives relative to workers. The intra-population facultative eusociality of M. genalis permits direct comparisons between individuals expressing alternative reproductive phenotypes – females that reproduce alone (solitary reproductives) and social queens – to highlight traits in the latter that may be important mediators of eusociality. Compared with solitary reproductives, the cuticular chemistries of queens are more strongly differentiated from those of workers, and furthermore are especially enriched for methyl-branched alkanes. Determining the pheromonal function(s) and information content of the candidate signaling compounds we identify will help illuminate the early evolutionary history of queen pheromones, chemical signals central to the organization of insect eusocial behavior.

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Data Availability

The chemical data generated for this study, and the R scripts used for heatmap generation, are available on Cornell University’s eCommons repository (https://doi.org/10.7298/9qym-kw90).

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Acknowledgements

We thank Stefan Schulz for assistance with interpretation of lactone spectra, Robert Raguso for helpful comments on early drafts of the manuscript, and Jocelyn Millar for guidance with derivatization procedures and methylalkane chemical standards. Yasuharu Yoshimi graciously contributed macrocyclic lactone chemical standards. We also thank Gabriel Trujillo, Isis Lopez, and Esther Velasquez for field assistance, and Barro Colorado Island staff for logistical support in Panamá.

Funding

C. Kingwell was supported by fellowships from the Smithsonian Tropical Research Institute, the Natural Sciences and Engineering Research Council of Canada (NSERC), and Cornell University.

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Authors and Affiliations

  1. Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, USA

    Callum Kingwell & Katalin Böröczky

  2. Smithsonian Tropical Research Institute, Panama City, Panama

    Callum Kingwell & William Wcislo

  3. Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany

    Iris Steitz & Manfred Ayasse

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  1. Callum Kingwell
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Contributions

C. Kingwell, M. Ayasse, and W. Wcislo conceptualized the study. C. Kingwell collected field data, conducted statistical analyses, and wrote the first draft of the manuscript. C. Kingwell, K. Böröczky, M. Ayasse, and I. Steitz determined the identities of chemical compounds. All authors contributed to the writing of the final manuscript.

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Correspondence to Callum Kingwell.

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Kingwell, C., Böröczky, K., Steitz, I. et al. Cuticular and Dufour’s Gland Chemistry Reflect Reproductive and Social State in the Facultatively Eusocial Sweat Bee Megalopta genalis (Hymenoptera: Halictidae). J Chem Ecol 47, 420–432 (2021). https://doi.org/10.1007/s10886-021-01262-1

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