Relaxation of natural selection in the evolution of the giant lungfish genomes

Abstract

Funding: This work was supported by the University of Ferrara (Italy) and funded by the MIUR PRIN 2017 grant 201794ZXTL to G.B. S.F., G.B., and R.B. are deeply grateful to Jane Hughes and Dan Schmidt for their hospitality at the Griffith University, Queensland, and for their friendship.Nonadaptive hypotheses on the evolution of eukaryotic genome size predict an expansion when the process of purifying selection becomes weak. Accordingly, species with huge genomes, such as lungfish, are expected to show a genome-wide relaxation signature of selection compared with other organisms. However, few studies have empirically tested this prediction using genomic data in a comparative framework. Here, we show that 1) the newly assembled transcriptome of the Australian lungfish, Neoceratodus forsteri, is characterized by an excess of pervasive transcription, or transcriptional leakage, possibly due to suboptimal transcriptional control, and 2) a significant relaxation signature in coding genes in lungfish species compared with other vertebrates. Based on these observations, we propose that the largest known animal genomes evolved in a nearly neutral scenario where genome expansion is less efficiently constrained.Peer reviewe