Hemimetabolous insects elucidate the origin of sexual development via alternative splicing

• Published in: eLife Vol. 8
• Main Authors: Wexler, Judith, Delaney, Emily Kay, Belles, Xavier, Schal, Coby, Wada-Katsumata, Ayako, Amicucci, Matthew J, Kopp, Artyom
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 03-09-2019; eLife Sciences Publications, Ltd
• Subjects: Alternative Splicing; Animals; Blattella germanica; Cockroaches - genetics; Cockroaches - physiology; development; Developmental Biology; doublesex; Evolution; Evolutionary Biology; Females; Gene expression; Hemiptera - genetics; Hemiptera - physiology; Insect Proteins - biosynthesis; Insect Proteins - genetics; Insects; Isoforms; Males; Nematodes; Phthiraptera - genetics; Phthiraptera - physiology; Principal components analysis; Protein Isoforms - biosynthesis; Protein Isoforms - genetics; Proteins; sex; Sex differentiation; Sexual Development; Splicing factors; Transcription factors; Transcription Factors - biosynthesis; Transcription Factors - genetics; transformer; Vertebrates; United States > US; California; development; evolutionary biology; developmental biology; doublesex; sex; transformer; evolution; Blattella germanica
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/elife.47490

Insects are the only known animals in which sexual differentiation is controlled by sex-specific splicing. The
transcription factor produces distinct male and female isoforms, which are both essential for sex-specific development.
splicing depends on
, which is also alternatively spliced such that functional Tra is only present in females. This pathway has evolved from an ancestral mechanism where
was independent of
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
and
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
pathway evolved via merger between expanding
function (from males to both sexes) and narrowing
function (from a general splicing factor to dedicated regulator of
).