Leaving X: How scale insects repeatedly evolved alternatives to chromosomal sex determination

Abstract

Reproduction is a core feature of life, yet it is still unclear why sex determination systems are conserved for hundreds of millions of years in some taxa but repeatedly turn over in others. A prime example is the true bugs; the vast majority of families employ a conserved X sex chromosomal system, but in scale insects (Coccomorpha), sex determination systems are more varied. Scale insects may retain X chromosomes, employ a form of haplodiploidy known as paternal genome elimination (PGE), or reproduce via selfing as simultaneous hermaphrodites. We sequenced 17 new scale insect species to study sex determination transitions. We recovered two independent losses of the X, once in the family Monophlebidae and a second time at the base of the PGE families. In the former, genomic rearrangements begin before the X is lost, leading to a pair of massive autosomes to which the X fuses in hermaphrodites. In the latter, the X chromosome has multiple fates, from being preserved intact, albeit without sex determination function, to being reshuffled as part of a massive whole genome rearrangement in mealybugs. We analyzed ortholog conservation across the transitions and found few genes lost, with only one orthogroup lost in both, and a number of orthogroups gained, suggesting these transitions did not require large changes to gene content. Finally, extreme sexual dimorphism of gene expression predates sex determination turnover and lingers on some formerly X-linked sequences. Together, these results illustrate the multiple routes to sex determination turnover, refine causal hypotheses, and provide a wealth of new resources for genomic study of scale insects.