Increased evolutionary rate in the Z-chromosome ofMorphobutterflies and implications for speciation

Abstract

The evolution of reproductive isolation between populations shapes divergence in genome structure and content: comparing the genomes of closely-related species can thus enlighten the speciation process. Comparisons of genomes of allopatric vs. sympatric species sharing similar vs. dissimilar ecological niches allows to specifically investigate the effect of reinforcement and ecological specialization on genome evolution. In the butterfly genus Morpho, several species can be found in sympatry presenting specialisation in different microhabitats and temporal niches. Here, we sequenced, assembled and annotated the genomes of 8 Morpho species and used previously published genomes of three other Morpho species to study genomic rearrangements and signatures of positive selection. We found extensive chromosomal rearrangements in the Z chromosome compared to the autosomes, particularly among closely related sympatric species occupying similar niches, pointing at the putative role of inversions in preventing gene flow at a postzygotic level. We also detected a higher proportion of genes under positive selection on the Z-chromosome compared to the autosomes, suggesting a potential role of the Z-chromosome in driving adaptive evolution in Morpho. Finally, because of the divergence in daily activities between species, we studied the evolution of eight genes involved in the circadian clock and detected a signature of positive selection on the gene Period, located in the Z chromosome. By studying the evolution of genome structure and coding sequences, our study indicates fast evolution of the Z-chromosome, partly driven by selection, throughout this genus, highlighting the putative implication of this sexual chromosome on pre and post-zygotic isolation.