Convergent Loss of Prothoracicotropic Hormone, A Canonical Regulator of Development, in Social Bee Evolution

Abstract

The evolution of insect sociality has repeatedly involved changes in developmental events and their timing. Here, we propose the hypothesis that loss of a canonical regulator of moulting and metamorphosis, prothoracicotropic hormone (PTTH), and its receptor, Torso, is associated with the evolution of sociality in bees. Specifically, we posit that the increasing importance of social influences on early developmental timing in social bees has led to their decreased reliance on PTTH, which connects developmental timing with abiotic cues in solitary insects. At present, the evidence to support this hypothesis includes the absence of genes encoding PTTH and Torso from all fully-sequenced social bee genomes and its presence in all available genomes of solitary bees. Based on the bee phylogeny, the most parsimonious reconstruction of evolutionary events is that this hormone and its receptor have been lost multiple times, across independently social bee lineages. These gene losses shed light on possible molecular and cellular mechanisms that are associated with the evolution of social behavior in bees. We outline the available evidence for our hypothesis, and then contextualize it in light of what is known about developmental cues in social and solitary bees, and the multiple precedences of major developmental changes in social insects.

The complete genome of Tetragonisca angustula (Apidae: Meliponini), the most commonly reared stingless bee in Brazil

“…Therefore, the nding that OR orthogroups have been rapidly contracting in T. angustula is intriguing and raises important questions concerning its evolution. One could claim that eusociality may have played a role in the observed OR contraction, as previously shown regarding immunity [119] and regulatory orthologs [120]. However, our analyses actually revealed a rather opposite trend, i.e., a rapid expansion within Meliponini that was drastically reversed in T. angustula.…”

Convergent evolution associated with the loss of developmental diapause may promote extended lifespan in bees

“…In Hymenoptera, the loss of PTTH and torso appears linked to the evolution of sociality in bees, as all examined social bee genomes lack these genes (Costa et al 2022) (Figure 1). Our findings suggest that not only sociality, but also the loss of developmental diapause, predicts PTTH and torso loss, with the latter being a stronger predictor.…”

“…PTTH and torso loss have been previously associated with social behavior in bees. In a previous screening of 22 bee genomes, all 15 of the included social species were missing both PTTH and torso (Costa et al 2022). We aimed to discern whether the diapause stage or sociality exerted a stronger influence on gene loss.…”