Sociality Sculpts Similar Patterns of Molecular Evolution in Two Independently Evolved Lineages of Eusocial Bees
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Genome Informatics Facility Publications Genome Informatics Facility 2-26-2021 Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees Wyatt A. Shell York University Michael A. Steffen University of New Hampshire, Durham Hannah K. Pare University of New Hampshire, Durham Arun S. Seetharam Iowa State University, [email protected] Andrew J. Severin Iowa State University, [email protected] See next page for additional authors Follow this and additional works at: https://lib.dr.iastate.edu/genomeinformatics_pubs Part of the Behavior and Ethology Commons, Bioinformatics Commons, Evolution Commons, and the Genomics Commons Recommended Citation Shell, Wyatt A.; Steffen, Michael A.; Pare, Hannah K.; Seetharam, Arun S.; Severin, Andrew J.; Toth, Amy L.; and Rehan, Sandra M., "Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees" (2021). Genome Informatics Facility Publications. 7. https://lib.dr.iastate.edu/genomeinformatics_pubs/7 This Article is brought to you for free and open access by the Genome Informatics Facility at Iowa State University Digital Repository. It has been accepted for inclusion in Genome Informatics Facility Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees Abstract While it is well known that the genome can affect social behavior, recent models posit that social lifestyles can, in turn, influence genome evolution. Here, we perform the most phylogenetically comprehensive comparative analysis of 16 bee genomes to date: incorporating two published and four new carpenter bee genomes (Apidae: Xylocopinae) for a first-ever genomic comparison with a monophyletic clade containing solitary through advanced eusocial taxa. We find that eusocial lineages have undergone more gene family expansions, feature more signatures of positive selection, and have higher counts of taxonomically restricted genes than solitary and weakly social lineages. Transcriptomic data reveal that caste-affiliated genes ear deeply-conserved; gene regulatory and functional elements are more closely tied to social phenotype than phylogenetic lineage; and regulatory complexity increases steadily with social complexity. Overall, our study provides robust empirical evidence that social evolution can act as a major and surprisingly consistent driver of macroevolutionary genomic change. Disciplines Behavior and Ethology | Bioinformatics | Evolution | Genomics Comments This article is published as Shell, Wyatt A., Michael A. Steffen, Hannah K. Pare, Arun S. Seetharam, Andrew J. Severin, Amy L. Toth, and Sandra M. Rehan. "Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees." Communications Biology 4 (2021). DOI: 10.1038/ s42003-021-01770-6. Posted with permission. Creative Commons License This work is licensed under a Creative Commons Attribution 4.0 License. Authors Wyatt A. Shell, Michael A. Steffen, Hannah K. Pare, Arun S. Seetharam, Andrew J. Severin, Amy L. Toth, and Sandra M. Rehan This article is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/ genomeinformatics_pubs/7 ARTICLE https://doi.org/10.1038/s42003-021-01770-6 OPEN Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees Wyatt A. Shell 1,2, Michael A. Steffen2, Hannah K. Pare2, Arun S. Seetharam 3, Andrew J. Severin 3, ✉ Amy L. Toth 4 & Sandra M. Rehan1 While it is well known that the genome can affect social behavior, recent models posit that social lifestyles can, in turn, influence genome evolution. Here, we perform the most phy- logenetically comprehensive comparative analysis of 16 bee genomes to date: incorporating fi 1234567890():,; two published and four new carpenter bee genomes (Apidae: Xylocopinae) for a rst-ever genomic comparison with a monophyletic clade containing solitary through advanced eusocial taxa. We find that eusocial lineages have undergone more gene family expansions, feature more signatures of positive selection, and have higher counts of taxonomically restricted genes than solitary and weakly social lineages. Transcriptomic data reveal that caste-affiliated genes are deeply-conserved; gene regulatory and functional elements are more closely tied to social phenotype than phylogenetic lineage; and regulatory complexity increases steadily with social complexity. Overall, our study provides robust empirical evi- dence that social evolution can act as a major and surprisingly consistent driver of macro- evolutionary genomic change. 1 Department of Biology, York University, Toronto, ON, Canada. 2 Department of Biological Sciences, University of New Hampshire, Durham, NH 03924, USA. 3 Office of Biotechnology, Iowa State University, Ames, IA 50011, USA. 4 Department of Entomology, Iowa State University, Ames, IA 50011, USA. ✉ email: [email protected] COMMUNICATIONS BIOLOGY | (2021) 4:253 | https://doi.org/10.1038/s42003-021-01770-6 | www.nature.com/commsbio 1 ARTICLE COMMUNICATIONS BIOLOGY | https://doi.org/10.1038/s42003-021-01770-6 ociogenomics has provided important advances in our important foundational inferences into the factors contributing to understanding of the molecular basis of social life1. Studies the evolutionary emergence and elaboration of insect S 21,22 have repeatedly shown that the evolution of animal sociality sociality . Empirical insights from these works, however, are is strongly influenced and accompanied by a variety of genomic effectively limited to one particularly derived bee lineage. Moving changes2–5. An emerging theme in sociobiology is the observation forward, as genomic resources continue to be developed, the field that, in addition to genes affecting social behavior, social life itself of sociogenomics will benefit enormously by expanding into bee may drive new patterns and processes in genome evolution6. For systems representative of other social lineages and phenotypes. example, it has been proposed that changes in demography, levels This project is a step along that route, incorporating genome data of selection, and the novel demands of social life can drive rapid from six carpenter bee species (Apidae: Xylocopinae), collectively sequence evolution, changes in genome organization, and other representative of an independent origin of sociality, and a first- forms of genomic change. To date, however, there remains a ever monophyletic dataset incorporating solitary (i.e. ancestral) paucity of genomic information for multiple closely-related spe- through advanced eusocial (i.e. derived) taxa11,17,23. This unique cies that vary in levels of sociality, leaving these ideas without dataset also affords us an opportunity to begin empirically dis- robust empirical support. cerning the degree to which the evolution of eusocial traits may Eusocial organisms demonstrate the most complex form of have been driven by environmental constraints (i.e. adaptive social organization in nature: a single reproductive queen is change) versus shared ancestry (i.e. phylogenetic inertia24,25)—a supported by hundreds or thousands of sterile offspring, all largely open question within the field of social evolution. Though cooperatively working together to rear additional generations of often handled separately, the effects of adaptive change and brood7,8. Eusociality has evolved only rarely but has emerged phylogenetic inertia are not mutually exclusive24; and compara- more often among bees than in any other group (as many as four tive assessment of the molecular impact of each on the evolution times9–11). As is demonstrated by the obligate social nesting of of social traits would greatly inform further theoretical and advanced eusocial bees, the emergence of social life marks a pivot empirical approaches. point from individual to group living, making it one of the most Owing to their global distribution and rich social diversity, car- consequential evolutionary transitions in the history of biological penter bees have long been the focus of illuminating phylogenetic complexity on Earth12. The progression from solitary to eusocial and behavioral ecological research (e.g.17,23,26–28). To date, pub- life among the socially diverse bees thus presents unique oppor- lished genomic and transcriptomic resources for the Xylocopinae tunities to address how the transition to sociality—and a new have been limited but highly informative resources for comparative level of biological organization (i.e. superorganismal)—may studies of early social evolution29–35. Here we present four newly influence genome evolution. sequenced xylocopine genomes and transcriptomes and combine It is generally thought that the evolutionary change from these with published genomic and transcriptomic data from 12 ancestral solitary life to group living in bees could not have additional bee species to address three main questions. (1) Do occurred in a single, abrupt evolutionary step. Rather, evidence genomes of independently evolved social bee lineages (Apinae and indicates that bees have collectively reverted to solitary life at least Xylocopinae) undergo parallel molecular changes during various nine times following an emergence of group living9–11. Addi- stages of social evolution? As articulated by the social ladder fra- tionally,