Signals Of Selection In Conditionally Expressed Genes In The Diversification Of Three Horned Beetle Species

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.