Genetic toolkit for sociality predicts castes across the spectrum of social complexity in wasps

Abstract

Major evolutionary transitions describe how biological complexity arises; e.g. in evolution of complex multicellular bodies, and superorganismal insect societies. Such transitions involve the evolution of division of labour, e.g. as queen and worker castes in insect societies. Castes across different evolutionary lineages are thought to be regulated by a conserved genetic toolkit. However, this hypothesis has not been tested thoroughly across the complexity spectrum of the major transition. Here we reveal, using machine learning analyses of brain transcription, evidence of a shared genetic toolkit across the spectrum of social complexity in Vespid wasps. Whilst molecular processes underpinning the simpler societies (which likely represent the origins of social living) are conserved throughout the major transition, additional processes appear to come into play in more complex societies. Such fundamental shifts in regulatory processes with complexity may typify other major evolutionary transitions, such as the evolution of multicellularity.

Dynamic neurogenomic responses to social interactions and dominance outcomes in female paper wasps

“…We observed multiple genes that show increases in expression over time in losers in the brain. The most upregulated gene in terms of log2 fold change in losers is a myosin heavy chain gene, which are upregulated in social wasp worker brains compared to queens [54]. We also observed a pattern of upregulation of arrestin in late losers but down regulation in winners and control nonsocial wasps.…”

“…Many of the genes with the largest decreases in losers at the later time show this up-then-down pattern, including vitellogenin, apolipophorin III, esterase E4 and apideacin. Both vitellogenin and esterase E4 are consistently downregulated in workers compared to queens across Polistine wasps [54]. Comparisons between worker and gyne P. metricus found lower levels of apolipophorin III in worker-compared to gyne-destined larvae [55].…”

“…Previous studies of caste differential expression in P. canadensis found that arrestin was upregulated in workers relative to queens [56], and it is found upregulated among foragers in ants as well [59]. FPPS encodes farnesyl pyrophosphate synthase which is involved in JH production [60,61] and is upregulated in queens in Polistine wasps [54]. We also observed increases in inositol monophosphatase (imp), which is involved in the inositol phosphate signaling pathway [62] and has been linked to task differentiation in ants and bees [63,64].…”

“…Vitellogenin (vg) is classically recognized for its role as an egg-yolk protein, which has a conserved role in oogenesis across insects [91]. In paper wasps, levels of vg in the head or brain have been associated with social status, being highest in single and dominant foundresses and lowest in subordinate foundresses and workers [38,54,56,89]. Our data suggest that vg levels quickly respond to social interaction, rising substantially in both losers and winners relative to nonsocial controls at the early time point (Fig 6B).…”

“…Nonsocial control wasps show relatively lower levels of vg compared to socially interacting wasps, though it is hard to contextualize the vg levels observed in control wasps compared to those reported in other studies. Previous studies have examined patterns of gene expression in wasps in relation to life history state or broader social contexts (e.g., foundresses versus worker) and not in response to specific social experiences [38,54,56,89]. Additionally, the wasps in this study had been kept in the lab without nests prior to the trials, following other studies of staged aggression contests [35,36,44], which likely influences baseline levels of gene expression.…”