Evolution of the Torso activation cassette, a pathway required for terminal patterning and moulting

Abstract

Embryonic terminal patterning and moulting are critical developmental processes in insects. In Drosophila and Tribolium both of these processes are regulated by the Torso‐activation cassette (TAC). The TAC consists of a common receptor, Torso, ligands Trunk and prothoracicotropic hormone (PTTH), and the spatially restricted protein Torso‐like, with combinations of these elements acting mechanistically to activate the receptor in different developmental contexts. In order to trace the evolutionary history of the TAC we determined the presence or absence of TAC components in the genomes of arthropods. Our analyses reveal that Torso, Trunk and PTTH are evolutionarily labile components of the TAC with multiple individual or combined losses occurring in the arthropod lineages leading to and within the insects. These losses are often correlated, with both ligands and receptor missing from the genome of the same species. We determine that the PTTH gene evolved in the common ancestor of Hemiptera and Holometabola, and is missing from the genomes of a number of species with experimentally demonstrated PTTH activity, implying another molecule may be involved in ecdysis in these species. In contrast, the torso‐like gene is a common component of pancrustacean genomes.

The torso-like gene functions to maintain the structure of the vitelline membrane in Nasonia vitripennis, implying its co-option into Drosophila axis formation

“…A nasonia tsl sequence was identified and its phylogenetic position assessed with respect to pan-arthropod Tsl proteins in (Skelly et al, 2018). We refer to this gene (NCBI LOC100118858) as Nv-tsl .…”

“…2). To investigate whether this function is coupled to the canonical terminal patterning system, we investigated the function of orthologues of the remaining TAC genes, PTTH and its receptor torso (previously identified by Skelly et al, 2018). Based on these data, we name LOC103315910 as Nv-PTTH and LOC103316970 as Nv-torso.…”

“…The ancestral role of tsl is unclear. The gene is present throughout the Pancrustacea and is present in genomes lacking other TAC genes (Skelly et al 2018). This implies it likely has an ancestral role independent from terminal patterning as carried out in Drosophila and from the other TAC genes.…”

“…Our data support the hypothesis that the TAC genes were co-opted from other roles into terminal patterning (Duncan et al, 2013). Trunk/PTTH and Torso seem to have been co-opted from a more ancient role in moulting control (Duncan et al, 2013; Skelly et al, 2018). Our data from Nasonia , [a hymenopteran insect, the sister group to the rest of the holometabola (Krauss et al, 2004; Savard et al, 2006; Zdobnov and Bork, 2007)], implies an ancestral role of tsl could have been to ensure VM integrity (Fig.…”

“…Tsl protein and RNA are expressed at the termini of the oocyte (Schoppmeier and Schroder 2005; Baumer et al 2012), and (like Drosophila ) no localized expression of tor or trk has been reported. In hymenoptera (bees, wasps, ants and others), trk is missing from multiple sequenced genomes implying its loss early in hymenopteran evolution (Skelly et al, 2018). PTTH is missing from a more limited subset often correlating with loss of tor .…”