Theme and variation in the evolution of insect sex determination

Abstract

The development of dimorphic adult sexes is a critical process for most animals, one that is subject to intense selection. Work in vertebrate and insect model species has revealed that sex determination mechanisms vary widely among animal groups. However, this variation is not uniform, with a limited number of conserved factors. Therefore, sex determination offers an excellent context to consider themes and variations in gene network evolution. Here we review the literature describing sex determination in diverse insects. We have screened public genomic sequence databases for orthologs and duplicates of 25 genes involved in insect sex determination, identifying patterns of presence and absence. These genes and a 3.5 reference set of 43 others were used to infer phylogenies and compared to accepted organismal relationships to examine patterns of congruence and divergence. The function of candidate genes for roles in sex determination (virilizer, female‐lethal‐2‐d, transformer‐2) and sex chromosome dosage compensation (male specific lethal‐1, msl‐2, msl‐3) were tested using RNA interference in the milkweed bug, Oncopeltus fasciatus. None of these candidate genes exhibited conserved roles in these processes. Amidst this variation we wish to highlight the following themes for the evolution of sex determination: (1) Unique features within taxa influence network evolution. (2) Their position in the network influences a component's evolution. Our analyses also suggest an inverse association of protein sequence conservation with functional conservation.

Distinct developmental mechanisms influence sexual dimorphisms in the milkweed bugOncopeltus fasciatus

“…Transcriptome and genome sequences also supported single instances of these genes in the milkweed bug. The phylogeny inferred for fru also deviates from the accepted relationships among major taxa (electronic supplementary material, figure S3); however, the ix phylogeny is closer to expected relationships (electronic supplementary material, figure S4) [26].…”

“…The maximum-likelihood best tree (electronic supplementary material, figure S1) forms four clades with modest bootstrap supports (45–69%) and excludes most non-insect DMRT sequences. Within each DMRT paralogue clade, topologies do not recapitulate most accepted taxonomic relationships [26]. Disagreement with organismal relationships is also found for a phylogeny inferred from alignment of Dsx alone (electronic supplementary material, figure S2).…”

“…Compared to other genes in insects involved in sexually dimorphic development, such as ix and fru, dsx orthologues evolve rapidly [26]. This could suggest that dsx occupies a space in the developmental network where mutations are more readily tolerated [24].…”

“…The evolution of gene regulatory networks is thought to be constrained by epistasis and pleiotropy, which are expected to impose strong stabilizing selection [24]. Sex determination violates this expectation, with substantial variation among Holometabola [1,3,25,26]. Amidst this variation, dsx is conserved in Holometabola as a point of integration for diverse sex-determining signals, and dsx activity is required for the development of both sexes [1,3,[26][27][28][29][30].…”

“…Sex determination violates this expectation, with substantial variation among Holometabola [1,3,25,26]. Amidst this variation, dsx is conserved in Holometabola as a point of integration for diverse sex-determining signals, and dsx activity is required for the development of both sexes [1,3,[26][27][28][29][30]. However, outside Holometabola the functional conservation of dsx is unclear.…”