Hemimetabolous insects elucidate the origin of sexual development via alternative splicing.

Emily Kay Delaney,Judith Wexler,Matthew J Amicucci,Xavier Belles,Ayako Wada-Katsumata,Artyom Kopp,Coby Schal

doi:10.7554/elife.47490

Emily Kay Delaney, Judith Wexler + Show 5 more

Open Access

https://doi.org/10.7554/elife.47490

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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).

Highlights

Sex determination and sexual differentiation evolve on drastically different time scales
To explore the origin of the insect sexual differentiation pathway based on the transformer-doublesex axis, we examined the expression of these genes in three hemimetabolous insects: the kissing bug Rhodnius prolixus (Hemiptera), the louse Pediculus humanus (Phthiraptera), and the German cockroach Blattella germanica (Blattodea) (Figure 1—figure supplement 1)
We examined sexual differentiation in hemimetabolous insects to investigate the evolutionary origin of this unique mode of sexual differentiation

Summary

Introduction

Sex determination and sexual differentiation evolve on drastically different time scales. The mapping of male and female RNA-seq reads to the four RpTraA isoforms identified by RACE further confirmed the sex-specificity of these isoforms: no female reads mapped to the male-specific stop codons in RpTraA_1 and RpTraA_2, and no male reads mapped to female-specific exon junctions of RpTraA_3 and RpTraA_4 (Figure 1—figure supplement 4) This pattern – a male-specific premature stop codon that is located in an alternatively spliced exon and results in the production of full-length Tra protein in females but not in males – follows the same pattern as in holometabolous insects including D. melanogaster, A. mellifera, and Tribolium castaneum (Hasselmann et al, 2008; Shukla and Palli, 2012a; Sosnowski et al, 1989).

11.46 Scaffold KQ034467

D WT male ovarioles dsTra female WT female

Discussion

Materials and methods

Findings

Funding Funder National Science Foundation