Signals of selection in conditionally expressed genes in the diversification of three horned beetle species

Abstract

Species radiations may be facilitated by phenotypic differences already present within populations, such as those arising through sex-specific development or developmental processes biased towards particular reproductive or trophic morphs. We sought to test this hypothesis by utilizing a comparative transcriptomic approach to contrast among- and within-species differentiation using three horned beetle species in the genus Onthophagus. These three species exhibit differences along three phenotypic axes reflective of much of the interspecific diversity present within the genus: horn location, polarity of sexual dimorphism and degree of nutritional sensitivity. Our approach combined de novo transcript assembly, assessment of amino acid substitutions (dN/dS) across orthologous gene pairs and integration of gene function and conditional gene expression data. We identified 17 genes across the three species pairs related to axis patterning, development and metabolism with dN/dS > 1 and detected elevated dN/dS in genes related to metabolism and biosynthesis in the most closely related species pair, which is characterized by a loss of nutritional polyphenism and a reversal of sexual dimorphism. Further, we found that genes that are conditionally expressed (i.e. as a function of sex, nutrition or body region) within one of our focal species also showed significantly stronger signals of positive or relaxed purifying selection between species divergent along the same morphological axis (i.e. polarity of sexual dimorphism, degree of nutritional sensitivity or location of horns). Our findings thus reveal a positive relationship between intraspecific differentiation due to condition-specific development and genetic divergences among species.

Comparative transcriptional analysis provides insights of possible molecular mechanisms of wing polyphenism induced by postnatal crowding in Aphis gossypii

“…Polyphenism denotes that multiple phenotypes are produced by a single genotype due to environmental induction (Ogawa and Miura 2014). This phenomenon exists commonly in organisms, especially in insects, such as castes in social insects, gregarious and solitary change of locusts, seasonal morphs of butterflies, and sexually selected phenotypes in beetle horns (Corona et al 2016;Klein et al 2016;Pespeni et al 2017;Wang et al 2014). Of the various phenotypes observed in the complex life cycle of aphids, the wing polyphenism seen in most species is conspicuous (Ogawa and Miura 2014).…”

Signals of selection beyond bottlenecks between exotic populations of the bull‐headed dung beetle, Onthophagus taurus

“…Alternatively, this result may be a consequence of assessing gene expression based on whole‐body RNA extractions. Gene expression in O. taurus , like most organisms, is highly tissue‐specific (Pespeni et al, 2017; Snell Rood et al, 2010). RNA extractions for the present study included the entire head and thorax for larvae and prepupae and whole bodies for pupae and adults—a design chosen to maximize sequencing coverage across the whole transcriptome to be able to generate SNP and expression data for as many genes as possible.…”

“…In particular, genes that are expressed in a context‐dependent manner have reduced pleiotropic constraint and thus may be well‐positioned to contribute to the early stages of population adaptation to novel conditions via modifications of their regulation (Hunt et al, 2011; Moczel et al, 2014; Snell Rood et al, 2010). Indeed, several studies have identified signatures of rapid divergence between species in conditionally expressed genes, such as sex‐biased genes in Drosophila melanogaster (Perry et al, 2014), and tissue‐ and sex‐specific genes in horned beetles (Pespeni et al, 2017; Snell Rood et al, 2010; Warren et al, 2014). However, few studies have taken advantage of recent population colonizations to assess potential relationships between geographic variation in allele frequencies and context‐dependent gene expression and its evolution.…”

Fitness costs and benefits of gene expression plasticity in rice under drought

“…The degree to which climatic changes cause plastic adjustments, and the relative importance of plasticity compared to other responses such as migration or evolution, are still debated (Merilä and Hendry 2014). While plasticity is ubiquitous, the extent to which plasticity is adaptive and evolving under selection is poorly understood (Arnold et al, 2019;Dudley and Schmitt, 1996;Hamann et al, 2016;Nussey et al, 2005;Pespeni et al, 2017;Saltz et al, 2018;Sultan, 2004;Van Buskirk and Steiner, 2009;Via et al, 1995), and whether plasticity is costly is also contentious (Auld et al, 2010). responses follow the same or opposite directions as selection on baseline expression-i.e., cogradient or counter-gradient selection sensu Byars and colleagues (2007).…”