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. 2024 Jan 16;20(1):e1011116.
doi: 10.1371/journal.pgen.1011116. eCollection 2024 Jan.

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

Affiliations

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

Lewis Stevens et al. PLoS Genet. .

Abstract

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 nematode 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-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 X-autosome 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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. The Litomosoides sigmodontis X chromosome is a fusion of Nigon X and Nigon D.
(A) Hi-C contact map for the nxLitSigm11.1 reference genome derived from the male Hi-C data. (B) Normalized male and female Hi-C read coverage in 100 kb windows in the six L. sigmodontis chromosomes. Normalised coverage (N) was calculated by dividing the coverage in each 100 kb window by the median autosomal coverage. (C) Distribution of counts of BUSCO genes in 500 kb windows in the six L. sigmodontis chromosomes coloured by their allocation to the seven Nigon elements (A-E, N, X).
Fig 2
Fig 2. Filarial nematodes with XY sex chromosomes have undergone recent X-autosome fusions.
(A) Cladogram of filarial nematodes derived from a supermatrix comprising 1,757 single-copy orthologues present in all 16 species. Reported karyotypes are indicated [17,30]. Note that the haploid chromosome number (n) in the genus Setaria varies from n = 3 to n = 6, but the ancestral state is believed to be n = 6 [17,30]. Species with chromosome-level reference genomes figured in (B) are highlighted in bold. (B) Distribution of BUSCO genes coloured by their allocation to the seven ancestral Nigon elements [19] in the chromosome-level assemblies of Dirofilaria immitis, Onchocerca volvulus, Brugia malayi, and L. sigmodontis. The scaffold that comprises the X chromosome is indicated in grey. Species names and karyotypes are indicated above each plot.
Fig 3
Fig 3. Filarial Y chromosomes are derived from unfused homologues of fused autosomes.
Male and female read coverage and Nigon element partitions in the X chromosomes of (A) D. immitis, (B) O. volvulus, and (C) B. malayi. Normalised coverages (N) are calculated by dividing the coverage in each 50 kb window by the median autosomal coverage. The histogram of locations of BUSCO loci allocated to Nigon elements (coloured as in Fig 1C) are binned in 500 kb windows. Regions that have diploid coverage in males are shown by grey shading.

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