The transcriptomic basis of tissue‐ and nutrition‐dependent sexual dimorphism in the beetle Onthophagus taurus

Abstract

Sexual dimorphism accounts for a large fraction of intraspecific diversity. However, not all traits are equally sexually dimorphic; instead, individuals are mosaics of tissues that vary in their ability to exhibit dimorphism. Furthermore, the degree of a trait's sexual dimorphism is frequently environment‐dependent, with elaborate sexual dimorphism commonly being restricted to high nutritional conditions. Understanding the developmental basis and evolution of condition‐dependent sexual dimorphism can be critically informed by determining – across tissues and nutritional conditions – what sex‐biased genes are deployed and how they interact and translate into functional processes. Indeed, key theories concerning the evolution of condition‐dependent sexually dimorphic traits rest on assumptions regarding their developmental genetic underpinnings, yet, have largely gone unexamined by empirical studies. Here, we provide such evidence by investigating the transcriptomic basis of tissue‐ and nutrition‐dependent sexual dimorphism in the bull‐headed dung beetle Onthophagus taurus. Our findings suggest (1) that generating morphological sexual dimorphism requires sex‐biased gene expression in and developmental remodeling of both sexes, regardless of which sex exhibits externally visible trait exaggeration, (2) that although sexually dimorphic phenotypes are comprised of traits underlain by independent repertoires of sex‐biased gene expression, they act similarly at a functional level, and (3) that sexual dimorphism and condition‐dependence share common genetic underpinnings specifically in sexually‐selected traits.

doublesex alters aggressiveness as a function of social context and sex in the polyphenic beetle Onthophagus taurus

“…Importantly, our results show that aggressiveness is significantly affected by dsx knockdown, thus raising the possibility that dsx 's role in behaviour modulation may itself be condition dependent. If correct, these conclusions would parallel those that have emerged from several recent transcriptomic and functional studies in the same species, which document that dsx affects sex-specific morphological differentiation via a target gene repertoire that is not only specific for each tissue type and sex, but also modulated heavily by environmental conditions (Kijimoto et al, 2014; Ledón-Rettig & Moczek, 2016; Ledón-Rettig et al, 2017). …”

“…Advances in sequencing technology and the experimental analyses of pathway functions have greatly contributed to the understanding of the conditional differentiation of specific traits (e.g. Ledón-Rettig et al, 2017; Ledón-Rettig & Moczek, 2016; Kijimoto et al, 2014), yet how multiple, complex traits may be co-regulated in a context-dependent manner remains poorly understood. In particular, the developmental genetic regulation of complex behavioural phenotypes and their integration with morphology can provide important insights in how developmental processes enable genotype–phenotype maps to be sensitive to context during ontogeny, and how such context sensitivity may diversify during evolution.…”

Evidence of developmental niche construction in dung beetles: effects on growth, scaling and reproductive success

“…While the transcriptomic (Kijimoto et al . ; Ledón‐Rettig & Moczek ), cellular (Moczek ; Kijimoto et al . ) and endocrine factors (Emlen et al .…”

Sexual dimorphism and heightened conditional expression in a sexually selected weapon in the Asian rhinoceros beetle

“…However, these studies − like all those focused on candidate genes − are limited and necessarily biased in scope due to their reliance on prior knowledge of gene function from related taxa. Several recent studies have leveraged high‐throughput sequencing (e.g., RNAseq) to provide transcriptome‐wide screens for differential gene expression associated with extreme trait growth (Gotoh et al., ; Kijimoto et al., ; Ledón‐Rettig & Moczek, ; Ledón‐Rettig, Zattara, & Moczek, ; Ozawa et al., ; Pointer, Harrison, Wright, & Mank, ; Wilkinson, Johns, Metheny, & Baker, ), providing unbiased glimpses into the genetic architecture of sexually selected traits.…”