Convergent and complementary selection shaped gains and losses of eusociality in sweat bees

Beryl M. Jones, Benjamin E.R. Rubin, Olga Dudchenko, Callum J. Kingwell, Ian M. Traniello, Z. Yan Wang, Karen M. Kapheim, Eli S. Wyman, Per A. Adastra, Weijie Liu, Lance R. Parsons, S. Ra Elle Jackson, Katharine Goodwin, Shawn M. Davidson, Matthew J. McBride, Andrew E. Webb, Kennedy S. Omufwoko, Nikki Van Dorp, Mauricio Fernández Otárola, Melanie PhamArina D. Omer, David Weisz, Joshua Schraiber, Fernando Villanea, William T. Wcislo, Robert J. Paxton, Brendan G. Hunt, Erez Lieberman Aiden, Sarah D. Kocher

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Sweat bees have repeatedly gained and lost eusociality, a transition from individual to group reproduction. Here we generate chromosome-length genome assemblies for 17 species and identify genomic signatures of evolutionary trade-offs associated with transitions between social and solitary living. Both young genes and regulatory regions show enrichment for these molecular patterns. We also identify loci that show evidence of complementary signals of positive and relaxed selection linked specifically to the convergent gains and losses of eusociality in sweat bees. This includes two pleiotropic proteins that bind and transport juvenile hormone (JH)—a key regulator of insect development and reproduction. We find that one of these proteins is primarily expressed in subperineurial glial cells that form the insect blood–brain barrier and that brain levels of JH vary by sociality. Our findings are consistent with a role of JH in modulating social behaviour and suggest that eusocial evolution was facilitated by alteration of the proteins that bind and transport JH, revealing how an ancestral developmental hormone may have been co-opted during one of life’s major transitions. More broadly, our results highlight how evolutionary trade-offs have structured the molecular basis of eusociality in these bees and demonstrate how both directional selection and release from constraint can shape trait evolution.

Original languageEnglish (US)
Pages (from-to)557-569
Number of pages13
JournalNature Ecology and Evolution
Volume7
Issue number4
DOIs
StatePublished - Apr 2023

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Ecology

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