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Exploring the integration of innovation in the dorsal head of Onthophagus beetles using head compartment-specific RNAseq

ABSTRACT: The general morphology of the insect head has remained relatively unchanged through more than 400 million years of evolution. Yet throughout this period this same region has also become a hotspot for evolutionary novelty, yielding structures such as the eyestalks of stalk-eyed flies or the cephalic horns of dung beetles. How novelty can be integrated within ancient complex traits without disrupting the function and formation of that trait is a foundational, yet largely unresolved question in developmental and evolutionary biology. Here, we approached this question by performing unique, head compartment specific RNAseq using the heads of Onthophagus taurus beetles, which bear impressive posterior horns in males. We sequenced the transcriptomes in horned males and hornless females from six distinct head compartments covering two major axes of patterning: anterior to posterior (AP) and medial to lateral (ML). Our results provide evidence of differential compartmentalization of the head along both AP and ML axes, and reveal striking parallels between morphological and transcriptomic complexity – that is, head regions with more complex morphologies, such as the posterior region, are more transcriptionally intricate compared to morphologically homogenous regions, such as the anterior of the head. Our findings support the hypothesis that the integration of novel traits within ancestral trait complexes may require the recruitment of additional genes and pathways into the networks instructing within and among compartment development. However, sexual dimorphism in posterior horn development was not paralleled by a corresponding sexual dimorphism in transcriptional complexity, instead hornless females exhibited approximately the same diversity of differentially expressed genes across posterior head compartments than did horn-bearing males.

ORGANISM(S): Onthophagus taurus

PROVIDER: GSE136677 | GEO | 2020/01/01

REPOSITORIES: GEO

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Project description:Developmental mechanisms play an important role in determining the costs, limits, and evolutionary consequences of phenotypic plasticity. One issue central to these claims is the metaphor of developmental “decoupling,” where alternate morphs result from evolutionarily independent developmental pathways. We test this assumption through a microarray study that explores differences in gene expression between alternate morphs relative to differences between sexes, a classic example of developmental decoupling. We then examine whether morph-biased genes are less conserved, relative to morph-shared genes, as predicted if developmental decoupling relaxes pleiotropic constraints on divergence. We focus on the developing horns and brains of two species of horned beetles with spectacular sexual- and morph-dimorphism in the expression of horns and fighting behavior. We find that patterns of gene expression were as divergent between morphs as they were between sexes. However, overall patterns of gene expression were also highly correlated across morphs and sexes. Morph-biased genes were more evolutionarily divergent, suggesting a role of relaxed pleiotropic constraints or relaxed selection. Together these results suggest that alternate morphs are somewhat developmentally decoupled, and that this decoupling has significant evolutionary consequences. However, alternative morphs may not be as developmentally decoupled as sometimes assumed and such hypotheses of development should be revisited and refined. We compared gene expression in three focal epidermal tissues (head, prothorax, legs) relative to a "control" tissue (dorsal abdominal epidermis) without any outgrowths. We also surveyed gene expression in the brain, relative to ganglionic neural tissue. We compared such patterns of gene expression between two male morphs (horned, fighter and hornless, sneaker males) and between males and females. We focused our array analyses (N = 48 arrays) on Onthophagus taurus (the species for which the array was designed), but also ran 19 arrays on thoracic tissue of Onthophagus nigriventris, a species which expresses thoracic horns as adults (O. taurus expresses head horns). Finally, we included a small subset of arrays (N = 4) directly hybridizing head epidermis tissue of O. taurus male morphs to validate our overall estimates of morph-biased expression. For more detail, refer to Snell-Rood et al. 2010, Evolution.

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Exploring the integration of innovation in the dorsal head of Onthophagus beetles using head compartment-specific RNAseq

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