Hemimetabolous insects elucidate the origin of sexual development via alternative splicing

Elife. 2019 Sep 3:8:e47490. doi: 10.7554/eLife.47490.

Abstract

Insects are the only known animals in which sexual differentiation is controlled by sex-specific splicing. The doublesex transcription factor produces distinct male and female isoforms, which are both essential for sex-specific development. dsx splicing depends on transformer, which is also alternatively spliced such that functional Tra is only present in females. This pathway has evolved from an ancestral mechanism where dsx was independent of tra and expressed and required only in males. To reconstruct this transition, we examined three basal, hemimetabolous insect orders: Hemiptera, Phthiraptera, and Blattodea. We show that tra and dsx have distinct functions in these insects, reflecting different stages in the changeover from a transcription-based to a splicing-based mode of sexual differentiation. We propose that the canonical insect tra-dsx pathway evolved via merger between expanding dsx function (from males to both sexes) and narrowing tra function (from a general splicing factor to dedicated regulator of dsx).

Keywords: Blattella germanica; development; developmental biology; doublesex; evolution; evolutionary biology; sex; transformer.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alternative Splicing*
  • Animals
  • Cockroaches / genetics
  • Cockroaches / physiology*
  • Hemiptera / genetics
  • Hemiptera / physiology*
  • Insect Proteins / biosynthesis*
  • Insect Proteins / genetics
  • Phthiraptera / genetics
  • Phthiraptera / physiology*
  • Protein Isoforms / biosynthesis
  • Protein Isoforms / genetics
  • Sexual Development*
  • Transcription Factors / biosynthesis*
  • Transcription Factors / genetics

Substances

  • Insect Proteins
  • Protein Isoforms
  • Transcription Factors