Aphids (family Aphididae) are a diverse group of insects with over 5000 species, including many agricultural pests. Their genomes show high rates of gene duplication and unusual sex chromosome evolution. As in many members of order Hemiptera, aphids have XO sex determination. Contrasting with autosomes, the aphid X chromosome exhibits conserved gene content and synteny, overrepresentation of male-biased genes, and faster sequence evolution. These genomic features likely stem from aphids’ unusual life history, in which all-female generations alternate with a sexual generation. Cyclical parthenogenesis also characterizes the related family, Phylloxeridae, also within infraorder Aphidomorpha. To determine whether the distinctive genome evolution of aphids coincides with their shared life history with phylloxera, we used Hi-C technologies to generate a chromosome-level assembly for the grape phylloxera and identified the X chromosome by resequencing males. We found that the conservation of X chromosome content and rearrangement in autosomes extend to phylloxera. Compared to chromosome-level genome assemblies for other Hemiptera, rates of interchromosomal rearrangements of Aphidomorpha autosomes are elevated, although sequence evolution is faster for X-linked genes than for autosomes. Our results extend the unusual patterns of aphid genome evolution to the origin of cyclical parthenogenesis, over 160 million years ago. Potentially, interchromosomal rearrangements arise during the numerous annual asexual generations, but movements of genes to and from the X may be removed by selection on XO males.
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