Striking parallels between dorsoventral patterning in <i>Drosophila</i> and <i>Gryllus</i> 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. <i>Drosophila</i> and the beetle <i>Tribolium</i> share extensive dependence on Toll, while representatives of more distantly related lineages like the wasp <i>Nasonia</i> and bug <i>Oncopeltus</i> rely more strongly on BMP signalling. Here, we show that in the cricket <i>Gryllus bimaculatus</i>, an evolutionarily distant outgroup, Toll has, like in <i>Drosophila</i>, 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 to <i>Drosophila</i>. Our data suggest two surprising hypotheses: (1) that Toll's patterning function in <i>Gryllus</i> and <i>Drosophila</i> is the result of convergent evolution or (2) a <i>Drosophila-like</i> system arose early in insect evolution and was extensively altered in multiple independent lineages.