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

Abstract

Axis specification is a fundamental developmental process. Despite this, the mechanisms by which it is controlled across insect taxa are strikingly different. An excellent example of this is terminal patterning, which in Diptera such as Drosophila melanogaster occurs via the localized activation of the receptor tyrosine kinase Torso. In Hymenoptera, however, the same process appears to be achieved via localized mRNA. How these mechanisms evolved and what they evolved from remains largely unexplored. Here, we show that torso-like, known for its role in Drosophila terminal patterning, is instead required for the integrity of the vitelline membrane in the hymenopteran wasp Nasonia vitripennis. We find that other genes known to be involved in Drosophila terminal patterning, such as torso and Ptth, also do not function in Nasonia embryonic development. These findings extended to orthologues of Drosophila vitelline membrane proteins known to play a role in localizing Torso-like in Drosophila; in Nasonia these are instead required for dorso–ventral patterning, gastrulation and potentially terminal patterning. Our data underscore the importance of the vitelline membrane in insect development, and implies phenotypes caused by knockdown of torso-like must be interpreted in light of its function in the vitelline membrane. In addition, our data imply that the signalling components of the Drosophila terminal patterning systems were co-opted from roles in regulating moulting, and co-option into terminal patterning involved the evolution of a novel interaction with the vitelline membrane protein Torso-like.

Expression and Function of Toll Pathway Components in the Early Development of the Wasp Nasonia vitripennis

“…The absence of pipe expression in the follicle cells in the honeybee indicates that the loss likely happened early in hymenopteran evolution [ 81 ]. Interestingly, a recent investigation of vitelline membrane proteins in N. vitrpennis [ 95 ] found that their knockdown leads to phenotypes at the cuticular level quite similar to those where the DV axis is disrupted ([ 43 , 96 ], J.A.L., personal observations). This indicates that vitelline membrane components still play a role in establishing DV polarity, but the mechanism and potentially the effect may be different.…”

smiFISH and embryo segmentation for single-cell multi-gene RNA quantification in arthropods

“…Tribolium were dechorionated and fixed as described for Drosophila , but for increased devitellinization efficiency, embryos were passed through a 19G needle in ice-cold 100% methanol. Fixed Nasonia embryos were kindly provided by Shannon Taylor from Peter Dearden’s lab 36 . Parhyale embryos were manually collected from females anaesthetized with 0.01% clove oil in sea water.…”

smiFISH and embryo segmentation for single-cell multi-gene RNA quantification in arthropods

“…Tribolium were dechorionated and fixed as described for Drosophila, but for increased devitellinization efficiency, embryos were passed through a 19G needle in ice-cold 100% methanol. Fixed Nasonia embryos were kindly provided by Shannon Taylor from Peter Dearden's lab 35 . Parhyale embryos were manually collected from females anaesthetized with 0.01% clove oil in sea water.…”