Chromosomal fusion drives sex chromosome evolution in treehoppers despite long-term X chromosome conservation

Abstract

Sex chromosomes follow distinct evolutionary trajectories compared to the rest of the genome. In many cases, sex chromosomes (X and Y, or Z and W) significantly differentiate from one another resulting in heteromorphic sex chromosome systems. Such heteromorphic systems are thought to act as an evolutionary trap that prevents subsequent turnover of the sex chromosome system. For old, degenerated sex chromosome systems in which turnover is unlikely, chromosomal fusion with an autosome may be one way that sex chromosomes can refresh their sequence content. We investigated these dynamics using treehoppers (hemipteran insects of the family Membracidae), which ancestrally have XX/X0 sex chromosomes. We assembled the first chromosome-level treehopper genome from Umbonia crassicornis and employed comparative genomic analyses of 12 additional treehopper species to analyze X chromosome variation across different evolutionary timescales. We find that the X chromosome is largely conserved, with one exception being an X-autosome fusion in Calloconophora caliginosa. We also compare the ancestral treehopper X with other X chromosomes in Auchenorrhyncha (the clade containing treehoppers, leafhoppers, spittlebugs, cicadas, and planthoppers), revealing X conservation across more than 300 million years. These findings shed light on chromosomal evolution dynamics in treehoppers and the role of chromosomal rearrangements in sex chromosome evolution. SignificanceThe evolutionary forces underlying sex chromosome stability versus turnover have been challenging to disentangle. We present the first chromosome-level treehopper genome and find evidence of long-term X chromosome conservation within treehoppers - and among treehoppers and other hemipteran insects. A key exception is the evolution of neo-XX/XY sex chromosomes via an X-autosome fusion. Sex chromosome-autosome fusions may play an important role in the evolution of otherwise trapped (i.e., old and degenerated) sex chromosome systems.