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

Elife. 2021 Mar 30:10:e68287. doi: 10.7554/eLife.68287.

Abstract

Dorsoventral pattering relies on Toll and BMP signalling in all insects studied so far, with variations in the relative contributions of both pathways. Drosophila and the beetle Tribolium share extensive dependence on Toll, while representatives of more distantly related lineages like the wasp Nasonia and bug Oncopeltus rely more strongly on BMP signalling. Here, we show that in the cricket Gryllus bimaculatus, an evolutionarily distant outgroup, Toll has, like in Drosophila, 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 Drosophila. Our data suggest two surprising hypotheses: (1) that Toll's patterning function in Gryllus and Drosophila is the result of convergent evolution or (2) a Drosophila-like system arose early in insect evolution and was extensively altered in multiple independent lineages.

Keywords: BMP signalling; Sog/Chordin; SoxN; Toll signalling; evolutionary biology; morphogen; pipe.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Evolution
  • Body Patterning / genetics*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics
  • Embryo, Nonmammalian
  • Embryonic Development
  • Evolution, Molecular
  • Gene Regulatory Networks*
  • Gryllidae / embryology*
  • Gryllidae / genetics
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Toll-Like Receptors / genetics*
  • Toll-Like Receptors / metabolism

Substances

  • Drosophila Proteins
  • Insect Proteins
  • Toll-Like Receptors

Associated data

  • SRA/PRJNA492804
  • figshare/10.6084/m9.figshare.14211062