Studying two highly divergent phyla of worms that contain numerous parasites that cause human and livestock diseases, new research sheds light on how sexual reproduction and subsequent great diversity of sex chromosomes might have evolved

Yifeng Wang, Robin B. Gasser, Deborah Charlesworth, Qi Zhou. Evolution of sexual systems, sex chromosomes and sex-linked gene transcription in flatworms and roundworms. Nature Communications, 2022; 13 (1). Jun 10 2022. DOI: 10.1038/s41467-022-30578-z

Abstract: 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.

Popular version: Parasitic worms reveal new insights into the evolution of sex and sex chromosomes Two worm phyla give clues on how sex chromosomes might have evolved. Jun 15 2022. https://www.sciencedaily.com/releases/2022/06/220615102849.htm

Discussion

The evolution of sex chromosomes in some taxa involves the primary transition from a hermaphroditic system or from environmental sex determination to a dioecious/gonochoristic species with genetic sex determination. Such transitions usually are accompanied by potential suppression of recombination in and around the sex-determining gene(s), and the recombination suppression sometimes even extends to other sex chromosome regions. In other species, turnover events may create new sex-determining regions, which may also evolve into non-recombining regions. In either case, autosomal regions that fused or translocated to sex chromosomes may sometimes also become completely sex-linked, either in species that lack recombination in the heterogametic sex26, or potentially in species with recombination in both sexes through subsequent recombination loss.

Schistosomes have evolved gonochorism from hermaphroditism and exhibit strong morphological sexual dimorphism (see above). As explained earlier, the first step in such a primary transition must either involve a mutation creating females (producing a gynodioecious population), or one creating males (producing an androdioecious population). A mutation in the highly conserved oogenesis-related or feminising gene mag-1 might have produced males in the ancestor of schistosomes. However, it seems unlikely that such a mutation could have greatly increased male fitness, compared with that of the ancestral hermaphrodite, as required for the establishment of androdioecy. Females could have arisen due to a dominant mutation in the reported W-linked candidate sex-determining gene U2AF2 (Fig. 5k)85,86. The involvement of these genes in the evolution of schistosome sex-determination needs to be tested in the future.

Our finding that the evolution of the present schistosome sex-linked regions was followed by transcriptional changes of many genes in gonads (Fig. 5d–g) is consistent with the hypothesis of sexual antagonism in the hermaphroditic ancestor, favouring re-allocation of resources after separate sexes evolved75. Assuming that higher transcription levels reflect advantageous changes, the results in schistosomes suggest that conflicts were resolved and a new optimum reached more frequently in males (masculinisation and overwhelming defeminisation) than in females (feminisation) in the gonads. In the transition to dioecy in Silene latifolia, with male, instead of female heterogamety, and an XY sex chromosome system, transcriptional changes occurred most frequently in females92. The results suggest transcriptional changes after the X or Z chromosome became hemizygous in one sex, resulting in masculinisation of the schistosome Z (as shown in Supplementary Fig. 16) and feminisation of the X chromosome in S. latifolia.

Following the origin of gonochorism, both schistosome and nematode ancestral sex chromosomes have undergone translocations of autosomes, like those in many other taxa26,56 (Figs. 3 and 5a). The translocated autosomes, or large parts of them, have become completely non-recombining in both phyla, and in nematodes they have become strongly degenerated like the ancestral sex chromosomes. How loss of recombination happened is an interesting question. Recombination between the autosomes involved in a fusion or translocation with sex chromosomes often maintain autosomes’ former recombination patterns. However, the study of fusions between the C. elegans X chromosome and chromosome IV62 suggested that crossovers may be re-positioned away from the fusion junction, creating a new chromosome with two arm regions (whereas the two participating chromosomes each contained two arm regions). In the fused chromosome, a potentially large former arm region close to the fusion point may thus have greatly reduced recombination, and if the fusion involves the X chromosome, this will occur specifically in males. Such events can therefore create new sex-linked regions without involving selection for suppressed recombination.

Translocations of autosomes to ancestral sex chromosomes may be common in nematodes because some, though not all, nematodes have holocentric chromosomes93. Such chromosomes may be more prone to fusions or fissions than monocentric ones, in which such rearrangements may lead to a loss or multiplication of centromeres94. However, a recent comparison of insects with different centromere types found no evidence supporting this hypothesis95.

Finally, we annotated many Y- or W-linked genes additional to those already known in the flatworm and roundworm species studied here (Figs. 4 and 5). We also found homologs of C. elegans sex-determination pathway genes that may have undergone duplications in different nematode species. These genes could be involved in the divergence of the sex-determination pathways, as has already been documented between C. elegans vs. C. briggsae96. Functional verification in other nematode species is needed in the future. The present study could not identify further changes that may have occurred after lineage-specific duplications of these genes, and possible changes also need to be studied further. For example, gld-1 was independently recruited into the sex-determination pathways of C. elegans and C. briggsae; in C. elegans it acts to promote spermatogenesis, but it promotes oogenesis in C. briggsae97. Its co-factor, fog-2, evolved by a duplication and acquisition of a new GLD-1-binding domain in C. elegans88,98. The newly annotated, candidate sex-determining genes could be a useful resource for future studies of parasite control through interfering with their sexual life cycles.