The genome of Litomosoides sigmodontis illuminates the origins of Y chromosomes in filarial nematodes

• Published in: PLoS genetics Vol. 20; no. 1; p. e1011116
• Main Authors: Stevens, Lewis, Kieninger, Manuela, Chan, Brian, Wood, Jonathan M D, Gonzalez de la Rosa, Pablo, Allen, Judith, Blaxter, Mark
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 16.01.2024; Public Library of Science (PLoS)
• Subjects: Analysis; Chromosomes; Females; Gene mapping; Genetic aspects; Genetic research; Genomes; Genomics; Identification and classification; Karyotypes; Litomosoides sigmodontis; Males; Methods; Nematoda; Nematodes; Sex chromosomes; Sex determination; Sex determination, Diagnostic; Sex determination, Genetic; Somatic chromosomes; Sperm; X chromosomes; Y chromosome; Y chromosomes; United Kingdom
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1011116

Heteromorphic sex chromosomes are usually thought to have originated from a pair of autosomes that acquired a sex-determining locus and subsequently stopped recombining, leading to degeneration of the sex-limited chromosome. The majority of nematodes species lack heteromorphic sex chromosomes and determine sex using an X-chromosome counting mechanism, with males being hemizygous for one or more X chromosomes (XX/X0). Some filarial nematode species, including important parasites of humans, have heteromorphic XX/XY karyotypes. It has been assumed that sex is determined by a Y-linked locus in these species. However, karyotypic analyses suggested that filarial Y chromosomes are derived from the unfused homologue of an autosome involved in an X-to-autosome fusion event. Here, we generated a chromosome-level reference genome for Litomosoides sigmodontis, a filarial nematode with the ancestral filarial karyotype and sex determination mechanism (XX/X0). By mapping the assembled chromosomes to the rhabditid nematode ancestral linkage (or Nigon) elements, we infer that the ancestral filarial X chromosome was the product of a fusion between NigonX (the ancestrally X-linked element) and NigonD (ancestrally autosomal). In the two filarial lineages with XY systems, there have been two independent autosome-to-X chromosome fusion events involving different autosomal Nigon elements. In both lineages, the region shared by the neo-X and neo-Y chromosomes is within the ancestrally autosomal portion of the X, confirming that the filarial Y chromosomes are derived from the unfused homologue of the autosome. Sex determination in XY filarial nematodes therefore likely continues to operate via the ancestral X-chromosome counting mechanism, rather than via a Y-linked sex-determining locus.