The Aphid X Chromosome Is a Dangerous Place for Functionally Important Genes: Diverse Evolution of Hemipteran Genomes Based on Chromosome-Level Assemblies

Different evolutionary forces shape gene content and sequence evolution on autosomes versus sex chromosomes. Location on a sex chromosome can favor male-beneficial or female-beneficial mutations depending on the sex determination system and selective pressure on different sexual morphs. An X0 sex determination can lead to autosomal enrichment of male-biased genes, as observed in some hemipteran insect species. Aphids share X0 sex determination; however, models predict the opposite pattern, due to their unusual life cycles, which alternate between all-female asexual generations and a single sexual generation. Predictions include enrichment of female-biased genes on autosomes and of male-biased genes on the X, in contrast to expectations for obligately sexual species. Robust tests of these models require chromosome-level genome assemblies for aphids and related hemipterans with X0 sex determination and obligate sexual reproduction. In this study, we built the first chromosome-level assembly of a psyllid, an aphid relative with X0 sex determination and obligate sexuality, and compared it with recently resolved chromosome-level assemblies of aphid genomes. Aphid and psyllid X chromosomes differ strikingly. In aphids, female-biased genes are strongly enriched on autosomes and male-biased genes are enriched on the X. In psyllids, male-biased genes are enriched on autosomes. Furthermore, functionally important gene categories of aphids are enriched on autosomes. Aphid X-linked genes and male-biased genes are under relaxed purifying selection, but gene content and order on the X is highly conserved, possibly reflecting constraints imposed by unique chromosomal mechanisms associated with the unusual aphid life cycle.