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Genomic footprint of evolution of eusociality in bees: floral food use and CYPome “blooms”

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Abstract

Comparative analyses of genomes of ten bee species representing different degrees of social complexity have demonstrated that independent transitions to eusociality are often accompanied by or lead to expansions or contractions of gene families (albeit different families across independent lineages). Because collective gathering, processing, and storage of plant products is a hallmark of bee social complexity, we examined the genomic inventory of cytochrome P450 genes (the CYPome) in these ten genomes, to search for footprints of eusociality in phytochemical detoxification pathways and, using a Bayesian implementation of the McDonald–Kreitman test, evidence of adaptive evolution within P450 lineages associated with food processing in eusocial florivorous Bombus and Apis species versus eusocial carnivorous Polistes species.We found no patterns linking CYPome size to level of social complexity within the ten bee genomes at the gene family level; however, a pattern emerged at the subfamily level, with the CYP6AS subfamily most diverse in perennial eusocial resin-collecting bees. In Apis mellifera, several CYP6AS enzymes are known to metabolize flavonols, ubiquitous constituents of nectar and honey, pollen and beebread, and resins and propolis. CYP6AS subfamily size varies from 7 in the solitary Habropoda laboriosa and the facultatively eusocial Lasioglossum albipes to 17 in the perennial eusocial Melipona quadrifasciatus; the degree of sociality across the ten species is correlated with CYP6AS inventory size (Spearman’s rho = 0.704, p < 0.023). Remarkably, there is perfect overlap between CYP6AS genes upregulated by the flavonol quercetin in A. mellifera and CYP6AS genes with signs of adaptive evolution in either Apis or Bombus. Our finding of positive selection on CYP6AS genes in Apis and Bombus, but not Polistes supports the hypothesis that CYP6AS subfamily expansion was involved in facilitating the shift from carnivory to florivory in bees. That some CYP6AS enzymes metabolize flavonoids suggests that subfamily expansion results from increased evolutionary exposure to these phytochemicals, through concentration of nectar into honey, pollen into beebread, and plant resins into propolis. Accompanying the evolutionary progression from solitary to perennial eusocial behavior in bees is a transition from short-term storage of ephemeral low-quality resources to concentrating and stockpiling those resources for colony use, with a concomitant need for phytochemical detoxification.

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Abbreviations

P450:

Cytochrome P450

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Acknowledgements

We thank Amy Toth, Laura Beani, and André Rodrigues for providing access to the Polistes samples for sequencing. This work was supported by USDA AFRI072116 to MRB, the Natural Science and Engineering Research Council of Canada (AZ), and the National Institute of Food and Agriculture, US Department of Agriculture Hatch Project under OHO01277.

Availability of data and material

Manually annotated nucleotide and amino acid sequences for bee P450 genes are available in the supplemental information (Supplemental File S1). The raw data for the honey bee and bumble bee population genomics dataset are found on NCBI’s short read archive (accession SRP029219 and PRNJA347806, respectively). Accessions to the Polistes population genomic dataset will be available upon acceptance of  Dogantzis et al. (in review).

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Author notes

  1. Brock A. Harpur

    Present address: Donnelly Centre, University of Toronto, 160 College St, Toronto, ON, M5S 3E2, Canada

Authors and Affiliations

  1. Department of Entomology, The Ohio State University, Ohio Agricultural Research and Development Center, 118 Thorne Hall, 1680 Madison Avenue, Wooster, OH, 44691, USA

    Reed M. Johnson

  2. Department of Biology, York University, 4700 Keele Street, Toronto, M3J 1P3, ON, Canada

    Brock A. Harpur, Kathleen A. Dogantzis & Amro Zayed

  3. Department of Entomology, 320 Morrill Hall, University of Illinois at Urbana-Champaign, 505 S. Goodwin, Urbana, IL, 61801-3795, USA

    May R. Berenbaum

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Contributions

RMJ annotated all of the CYP genes in the ten bee genomes and in the wasp genomes; BH, KD, and AZ carried out the population genomic analysis of CYP6AS genes in Apis, Bombus, and Polistes, and MRB conceived of the project, devised the hypothesis, and provided the ecological context for the genomic work. All authors contributed to writing the manuscript.

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Correspondence to May R. Berenbaum.

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Johnson, R.M., Harpur, B.A., Dogantzis, K.A. et al. Genomic footprint of evolution of eusociality in bees: floral food use and CYPome “blooms”. Insect. Soc. 65, 445–454 (2018). https://doi.org/10.1007/s00040-018-0631-x

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