The nutritionally responsive transcriptome of the polyphenic beetle Onthophagus taurus and the importance of sexual dimorphism and body region

Abstract

Developmental responses to nutritional variation represent one of the ecologically most important classes of adaptive plasticity. However, knowledge of genome-wide patterns of nutrition-responsive gene expression is limited. Here, we studied genome-wide transcriptional responses to nutritional variation and their dependency on trait and sex in the beetle Onthophagus taurus. We find that averaged across the transcriptome, nutrition contributes less to overall variation in gene expression than do sex or body region, but that for a modest subset of genes nutrition is by far the most important determinant of expression variation. Furthermore, our results reject the hypothesis that a common machinery may underlie nutrition-sensitive development across body regions. Instead, we find that magnitude (measured by number of differentially expressed contigs), composition (measured by functional enrichment) and evolutionary consequences (measured by patterns of sequence variation) are heavily dependent on exactly which body region is considered and the degree of sexual dimorphism observed on a morphological level. More generally, our findings illustrate that studies into the developmental mechanisms and evolutionary consequences of nutrition-biased gene expression must take into account the dynamics and complexities imposed by other sources of variation in gene expression such as sexual dimorphism and trait type.

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). …”

“…All dsx RNAi individuals used in the present study ( N = 78) presented phenotypes that fully replicated those described in previous work (Kijimoto et al, 2012; Ledón-Rettig et al, 2017). To produce dsRNA, we used plasmid vectors (Agilent, Santa Clara, CA, U.S.A.) containing different dsx fragments (either a part shared between sexes or one specific to females) following procedures detailed in Kijimoto et al (2014). To execute dsx RNAi knockdowns, we then injected 0.5 μg of dsRNA into larvae during the first 5 days of the final, third instar.…”

“…Control animals were reared under the same conditions as dsx dsRNA-injected animals but were instead injected with dsRNA from a 220 bp PCR product derived from a pSC-A vector as described in Kijimoto et al (2014). We injected 1 μg of dsRNA into larvae during the first 5 days of the final, third instar.…”

“…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.…”

Extending the integrated phenotype: covariance and correlation in plasticity of behavioural traits

“…Phenotypic plasticity has been reported in a multitude of traits over the last decades, including morphological traits, life-history, behaviour, but also in patterns of gene expression and protein production [5,6]. It is now generally accepted that plastic responses to environmental conditions during development or adult life can have important fitness consequences.…”