Evolution of sexual systems, sex chromosomes and sex-linked gene transcription in flatworms and roundworms

Many species with separate male and female individuals (termed ‘gonochorism’ in animals) have sex-linked genome regions. Here, we investigate evolutionary changes when genome regions become completely sex-linked, by analyses of multiple species of flatworms (Platyhelminthes; among which schistosomes recently evolved gonochorism from ancestral hermaphroditism), and roundworms (Nematoda) which have undergone independent translocations of different autosomes. Although neither the evolution of gonochorism nor translocations fusing ancestrally autosomal regions to sex chromosomes causes inevitable loss of recombination, we document that formerly recombining regions show genomic signatures of recombination suppression in both taxa, and become strongly genetically degenerated, with a loss of most genes. Comparisons with hermaphroditic flatworm transcriptomes show masculinisation and some defeminisation in schistosome gonad gene expression. We also find evidence that evolution of sex-linkage in nematodes is accompanied by transcriptional changes and dosage compensation. Our analyses also identify sex-linked genes that could assist future research aimed at controlling some of these important parasites.