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

Abstract

Life's most dramatic innovations, from the emergence of self-replicating molecules to highly-integrated societies, often involve increases in biological complexity. Some groups traverse different levels of complexity, providing a framework to identify key factors shaping these evolutionary transitions. Halictid bees span the transition from individual to group reproduction, with repeated gains and losses of eusociality. We generated chromosome-length genome assemblies for 17 species and searched for genes that both experienced positive selection when eusociality arose and relaxed selection when eusociality was secondarily lost. Loci exhibiting these complementary evolutionary signatures are predicted to carry costs outweighed by their importance for traits in eusocial lineages. Strikingly, these loci included two proteins that bind and transport juvenile hormone (JH) -a key regulator of insect development and reproduction. Though changes in JH abundance are frequently associated with polymorphisms, the mechanisms coupling JH to novel phenotypes are not well understood. Our results suggest novel links between JH and eusociality arose in halictids by altering transport and availability of JH in a tissue-specific manner, including in the brain. Through genomic comparisons of species encompassing both the emergence and breakdown of eusociality, we provide insights into the mechanisms targeted by selection to shape a key evolutionary transition.

Tropical and montaneA.ceranashow distinct dance-distance calibration curves

“…Both species evolved in the tropics and later extended their distribution range to temperate climate zones, but this happened on different continents, from Africa to Europe in A. mellifera and from South-East Asia to Northern Asia in A. cerana (Dogantzis et al 2021; Ji et al, 2020; Smith, 2020). Thus, larger foraging ranges and shallower slopes of the dance-distance calibration curves in temperate populations of A. cerana and A. mellifera represent parallel adaptations that might have evolved in response to similar selection pressures and is based on similar genomic mechanisms (Gallant et al, 2014; Ji et al, 2020; Jones et al, 2023; Pfenning et al, 2014). In the future, our extensive knowledge of honey bee behavior and the growing availability of genome information and molecular tools for all Apis species should increase the attractiveness of this group for comparative evolutionary studies on behavioral variation and the underlying molecular and neural mechanisms (Alves et al, 2023; Bastin et al, 2018; Jourjine and Hoekstra, 2021; Kohl et al, 2020; Seeley 1985).…”

Emergent Collective Behavior Evolves More Rapidly Than Individual Behavior Among Ant Species

“…If true, we would expect that relatively small phenotypic changes in the traits of lower-level units (e.g., isolated cells or individuals), together with small changes in traits regulating social interactions, could readily generate relatively large phenotypic changes in the higher-level emergent phenotype, potentially underlying major transitions in biological organization. Available comparative genomic studies seeking to identify genetic changes underlying the evolution of multicellularity ( 45–47 ) and eusociality ( 48–50 ) emphasize such relatively small genetic changes, consistent with emergent evolution. Further study across a wide range of emergent traits and systems will be necessary to elucidate to what degree emergent evolution has contributed to generating the phenotypic diversity of life.…”

Host species and geography impact bee-associated RNA virus communities with evidence for isolation by distance in viral populations

“…At the time of analysis, L. versatum did not have a reference genome, and reads from these samples were aligned to the L. leucozonium reference genome. Except for A. melifera , reference genomes for all bee species were generated by the labs of Sarah Kocher and Erez Lieberman Aiden [ 35–37 ]. RNA reads that aligned to the reference were discarded, and the unaligned reads were used as input for assembly with rnavirusSPADES [ 38 ].…”