Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network

Abstract

Dorsoventral pattering relies on Toll and BMP signalling in all insects studied so far, with variations in the relative contributions of both pathways.Drosophilaand the beetleTriboliumshare extensive dependence on Toll, while representatives of more distantly related lineages like the waspNasoniaand bugOncopeltusrely more strongly on BMP signalling. Here, we show that in the cricketGryllus bimaculatus, an evolutionarily distant outgroup, Toll has, like inDrosophila, a direct patterning role for the ventral half of the embryo. In addition, Toll polarises BMP signalling, although this does not involve the conserved BMP inhibitor Sog/Chordin. Finally, Toll activation relies on ovarian patterning mechanisms with striking similarity toDrosophila. Our data suggest two surprising hypotheses: (1) that Toll's patterning function inGryllusandDrosophilais the result of convergent evolution or (2) aDrosophila-likesystem arose early in insect evolution and was extensively altered in multiple independent lineages.