Doublesexmediates species-, sex-, environment- and trait-specific exaggeration of size and shape

Abstract

Context-dependent trait exaggeration is a major contributor to phenotypic diversity. However, the genetic modifiers instructing development across multiple contexts remain largely unknown. We use the arthropod tibia, a hotspot for segmental differentiation, as a paradigm to assess the developmental mechanisms underlying the context-dependent structural exaggeration of size and shape through nutritional plasticity, sexual dimorphism and segmental differentiation. Using an RNAseq approach in the sexually dimorphic and male-polyphenic dung beetle Digitonthophagus gazella , we find that only a small portion (3.7%) of all transcripts covary positively in expression level with trait size across contexts. However, RNAi-mediated knockdown of the conserved sex-determination gene doublesex suggests that it functions as a context-dependent master mediator of trait exaggeration in D. gazella as well as the closely related dung beetle Onthophagus taurus . Taken together, our findings suggest (i) that the gene networks associated with trait exaggeration are highly dependent on the precise developmental context, (ii) that doublesex differentially shapes morphological exaggeration depending on developmental contexts and (iii) that this context-specificity of dsx -mediated trait exaggeration may diversify rapidly. This mechanism may contribute to the resolution of conflict arising from environment-dependent antagonistic selection among sexes and divergent developmental contexts in a wide range of animals.

A role for sex‐determination genes in life history evolution? Doublesex mediates sexual size dimorphism in the gazelle dung beetle

“…Previous work shows that dsx not only mediates sexual dimorphism but also nutritional plasticity in secondary sexual traits (Casasa et al., 2020; Gotoh et al., 2014; Rohner et al, 2021). I found that body size increased with nutritional quality (log pronotum width: Χ 2 (1) = 191.00, p < .001; log pupal weight 1/3 : Χ 2 (1) = 191.00, p < .001; PC1: Χ 2 (1) = 152.42, p < .001).…”

Genetic, morphometric, and molecular analyses of interspecies differences in head shape and hybrid developmental defects in the wasp genus Nasonia

“…Studies have found that the key determinant in primary sex determination in metazoans, doublese x, plays an important role in evolutionary changes in sexually dimorphic traits within and between species ( Kopp 2012 ), such as horn size in dung beetles ( Rohner et al 2021 ), mimicry in butterfly wings ( Kunte et al 2014 ), wing size ( Loehlin et al 2010 ), and antennal pigmentation ( Wang et al 2020 ) in Nasonia . Here, we show that dsx also has an important role in sexual differences in male head shape between closely related Nasonia species.…”

Secondary reversion to sexual monomorphism associated with tissue‐specific loss of doublesex expression

“…2017; Palmer and Kronforst 2020; Rohner et al. 2021), and it is this fact that has a profound influence on the evolution of sexual dimorphism. For any sex‐specific structure to evolve, dsx must be expressed in the cells that either give rise to that structure or induce it by cell‒cell signaling.…”

“…Sex-specific cell differentiation is due to the distinct effects of DsxM and DsxF proteins on target gene expression (Burtis et al 1991;Williams et al 2008;Shirangi et al 2009;Arbeitman et al 2016). Importantly, dsx is transcribed in controlled spatial patterns (Hempel and Oliver 2007;Sanders and Arbeitman 2008;Loehlin et al 2010;Rideout et al 2010;Robinett et al 2010;Tanaka et al 2011;Kijimoto et al 2012;Ledón-Rettig et al 2017;Palmer and Kronforst 2020;Rohner et al 2021), and it is this fact that has a profound influence on the evolution of sexual dimorphism. For any sex-specific structure to evolve, dsx must be expressed in the cells that either give rise to that structure or induce it by cell-cell signaling.…”