Social divergence: molecular pathways underlying castes and longevity in a facultatively eusocial small carpenter bee

Abstract

Unravelling the evolutionary origins of eusocial life is a longstanding endeavour in the field of evolutionary-developmental biology. Descended from solitary ancestors, eusocial insects such as honeybees have evolved ontogenetic division of labour in which short-lived workers perform age-associated tasks, while a long-lived queen produces brood. It is hypothesized that (i) eusocial caste systems evolved through the co-option of deeply conserved genes and (ii) longevity may be tied to oxidative damage mitigation capacity. To date, however, these hypotheses have been examined primarily among only obligately eusocial corbiculate bees. We present brain transcriptomic data from a Japanese small carpenter bee, Ceratina japonica (Apidae: Xylocopinae), which demonstrates both solitary and eusocial nesting in sympatry and lives 2 or more years in the wild. Our dataset captures gene expression patterns underlying first- and second-year solitary females, queens and workers, providing an unprecedented opportunity to explore the molecular mechanisms underlying caste-antecedent phenotypes in a long-lived and facultatively eusocial bee. We find that C. japonica 's queens and workers are underpinned by divergent gene regulatory pathways, involving many differentially expressed genes well-conserved among other primitively eusocial bee lineages. We also find support for oxidative damage reduction as a proximate mechanism of longevity in C. japonica .

Co-expression Gene Networks and Machine-learning Algorithms Unveil a Core Genetic Toolkit for Reproductive Division of Labour in Rudimentary Insect Societies

“…The toolkits include specific genes that are shared across species and differentially expressed between social phenotypes; for example, genes related to core metabolic and reproductive processes (e.g., the egg-yolk protein Vitellogenin ( Amsalem et al 2014 ; Morandin et al 2019 )), possible “master” regulatory genes (e.g., zinc finger transcription factor family [ Rehan et al 2018 ]), and genes related to neural and sensory processing (e.g., neuroparsin-A-like [ Qiu et al 2018 ]). Signs of a toolkit for sociality are also evident at the functional level, with numerous studies uncovering shared gene pathways ( Berens et al 2015 ), networks ( Patalano et al 2015 ; Morandin et al 2016 ), and molecular and cellular processes at the mRNA level between queen and worker social phenotypes ( Wyatt et al 2020 ; Shell and Rehan 2022 ). Genes upregulated in reproductives may relate to epigenetic modifications ( Shell and Rehan 2019 ) or conserved functions such as transcription or biosynthetic processes associated with basic functions ( Taylor et al 2021 ).…”