Sexual System And Sex Chromosome Evolution In Worm Species

Sexual dimorphism(i.e.sex differences between members of the same species)is widespread across eukaryotes,and many independent transitions have been documented from hermaphroditic ancestors to dioecy in plants and the equivalent sexual system in animals(termed as gonochorism),and the reverse.While gynodioecy(presence of females as well as hermaphrodites)is regularly observed in plants,and may sometimes represents an intermediate step in the evolution of dioecy,it is extremely rare in animals,with only one verified gynodioecious animal species reported so far.Androdioecy(polymorphism of males and hermaphrodites)is rare in both plants and animals,and generally represents a transition from gonochorism to hermaphroditism.Evolution of separate sexes from hermaphroditism requires at least two mutations,an initial mutation that produces females,followed by a second mutation to produce males(or vice versa).Selection then favors closer linkage between the two loci,potentially leading to a fully sex-linked region that may include other genes without sex-determining functions.The mechanisms that regulate sexual development can change rapidly during evolution.Flatworms and roundworms(worms)encompass major parasites causing chronic diseases of humans and livestock,but also comprise a great paradigm for elucidating the molecular mechanism of transitions between hermaphroditism and gonochorism as well as that of turnovers of sex chromosomes.Here we combined 41 Nematoda and 13 Platyhelminthes species genomics and transcriptome data,and identify the sex-linked regions and/or annotate their corresponding sex-related Nigon element related genes in 17 species that are not reported before.In addition to identifying sex-linked sequences in the homogametic sex of the species studied,we also seek to identify Y-or W-linked genes.As such genes may not be well assembled,due to presence of repetitive sequences or very long introns,we further identify genes whose de novo assembled transcriptome sequences showed sex differences in genomic read coverage values from sexed animals.Combined with genes directly assembled from genomic reads,we annotate between 6 and 219 Y/W-linked genes in 6 individual species studied.Except for identifying sex chromosomes,we then determine how they have changed over time.Based on homologous Nigon elements detected in the sex-linked region of all studied nematodes species,the results help us to reconstruct the history of chromosome fusions and that led to the current sex chromosomes in each nematode clade;and our work suggests that species may have undergone independent translocations of different autosomes and some of the clades independently evolved the use of sex chromosomes.Events causing loss of recombination at different times are detectable from different levels of divergence(termed ‘evolutionary strata’)between sequences on the two sex chromosomes.Although neither the evolution of gonochorism,nor translocations fusing ancestrally autosomal regions to sex chromosomes,causes inevitable loss of recombination,we further dissect the history of these X chromosomes into strata with different characteristics of recombination,repeat number,etc.to estimate the different strata states,and we document that formerly recombining regions have stopped recombining in both taxa,and become strongly genetically degenerated,with loss of most genes.Given that non-recombining regions have recently formed between sex chromosomes of both nematodes and schistosomes,it is interesting to ask whether genes in these regions followed the evolutionary trajectory of canonical ancestral sex chromosomes,including evolution of dosage compensation(DC),and a different distribution of sex-biased genes relative to autosomes.We suggest that dosage compensation has been established in these species,but that it is not complete while in individual genes(incomplete DC,i DC).We also observe the accumulation of female-biased expression on the X chromosome,and the loss of male-biased expression,patterns inverted for Z chromosomes.Comparisons with hermaphroditic flatworm transcriptomes,transitions into gonochorism with ZW sex chromosomes(as in Schistosomes)involves masculinization and defeminization of gonad gene expression.Similarly,the reverse transition from a gonochoristic ancestor to the androdioecious seems mainly to have involved defeminization and masculinization of the gene transcription.Our work illuminates the origin of separate sexes,and the dynamic translocation of sex chromosomes and gene expression in the two phyla of worms,and the newly identified sex-linked genes can aid future studies aimed at controlling of some of the parasites.