Two novel genomes of fireflies with different degrees of sexual dimorphism reveal insights into sex-biased gene expression and dosage compensation

Abstract

Sexual dimorphism arises because of divergent fitness optima between the sexes. Phenotypic divergence between sexes can range from mild to extreme. Fireflies, bioluminescent beetles, present various degrees of sexual dimorphism, with species showing very mild sexual dimorphism to species presenting female-specific neoteny, posing a unique framework to investigate the evolution of sexually dimorphic traits across species. In this work, we present novel assembled genomes of two firefly species, Lamprohiza splendidula and Luciola italica, species with different degrees of sexual dimorphism. We uncover high synteny conservation of the X-chromosome across ~ 180 Mya and find full X-chromosome dosage compensation in our two fireflies, hinting at common mechanism upregulating the single male X-chromosome. Different degrees of sex-biased expressed genes were found across two body parts showing different proportions of expression conservation between species. Interestingly, we do not find X-chromosome enrichment of sex-biased genes, but retrieve autosomal enrichment of sex-biased genes. We further uncover higher nucleotide diversity in the intronic regions of sex-biased genes, hinting at a maintenance of heterozygosity through sexual selection. We identify different levels of sex-biased gene expression divergence including a set of genes showing conserved sex-biased gene expression between species. Divergent and conserved sex-biased genes are good candidates to test their role in the maintenance of sexually dimorphic traits.