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Comparative Study
. 2020 Apr 23;11(1):1964.
doi: 10.1038/s41467-020-15654-6.

Sex chromosome evolution in parasitic nematodes of humans

Affiliations
Comparative Study

Sex chromosome evolution in parasitic nematodes of humans

Jeremy M Foster et al. Nat Commun. .

Abstract

Sex determination mechanisms often differ even between related species yet the evolution of sex chromosomes remains poorly understood in all but a few model organisms. Some nematodes such as Caenorhabditis elegans have an XO sex determination system while others, such as the filarial parasite Brugia malayi, have an XY mechanism. We present a complete B. malayi genome assembly and define Nigon elements shared with C. elegans, which we then map to the genomes of other filarial species and more distantly related nematodes. We find a remarkable plasticity in sex chromosome evolution with several distinct cases of neo-X and neo-Y formation, X-added regions, and conversion of autosomes to sex chromosomes from which we propose a model of chromosome evolution across different nematode clades. The phylum Nematoda offers a new and innovative system for gaining a deeper understanding of sex chromosome evolution.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Homology between B. malayi, O. volvulus, and C. elegans chromosomes using conserved blocks.
The B. malayi chromosomes were mapped against the a O. volvulus and b C. elegans chromosomes. The correlation between chromosomes was predicted using comparisons of chromosome homology between B. malayi, O. volvulus, and C. elegans. The nematode chromosomes were broken into Nigon elements, with the coloring based on corresponding regions in C. elegans chromosomes. c A model of chromosome evolution is provided according to clades,, where each Nigon element is color-coded and described by the number of the corresponding C. elegans chromosome. The stars denote the PAR in both O. volvulus and B. malayi, color-coded by element, and the pins appearing next to the chromosomes denote the orientation of the Nigon elements between these two species, with "0" representing where the contig in the fasta file begins relative to the diagram. The portion of the Y chromosome that is significantly diverged from the X chromosome yet maintains identity with the Nigon element is illustrated with stripes. The Y chromosomes between O. volvulus and B. malayi have arisen twice from two different autosomes, while the X chromosomes also show significantly different composition, which further correlates to the composition of the Y chromosome. Despite these differences, in both B. malayi and O. volvulus, ND is now part of the X chromosome and is 1N. d Putative B. malayi Y contigs are mapped to relevant O. volvulus chromosomes, and putative O. volvulus Y contigs are mapped to relevant B. malayi chromosomes. The conserved sequences between the B. malayi chromosome Y-specific contigs and the O. volvulus NX span 150 kbp, while they span only 15 kbp for ND and 7–9 kbp for all the remaining Nigon elements. When combined with the PAR, this suggests that chromosome Y is largely derived from NX.
Fig. 2
Fig. 2. B. malayi Chr X mapping across O. volvulus Chr 1 (NX) and Chr X (ND).
An analysis of the B. malayi X chromosome indicates that it is the product of a fusion of two Nigon elements: ND and NX, in contrast with the O. volvulus X chromosome, which is composed of a fusion between ND and NE. The middle panel, which includes combined mummerplots to highlight Nigon element matches, shows the synteny of the B. malayi X chromosome to its corresponding two Nigon elements in O. volvulus. Each axis is marked with a corresponding sequencing depth plot of that chromosome. Thus, the X-axis of the main plot is linked to the sequencing depth of the Brugia malayi X chromosome, which is divided into ND (gray) and NX (blue). The left Y-axis shows the corresponding O. volvulus chromosome X, composed of ND (gray) and NE (yellow), while the right Y-axis shows the corresponding O. volvulus chromosome 1, composed of NA (red) and NX (blue). In both B. malayi and O. volvulus, ND is fused to a Nigon element that was likely autosomal in the most recent common ancestor, but those fusions occur at opposite ends of ND in the two nematodes.
Fig. 3
Fig. 3. Sequencing depth per Nigon element for diverse nematodes.
We provide examples of species across clade III, IV, and V nematodes. a The calculated N (average sequencing depth over a 10 kb window normalized to half the average sequencing depth of the whole diploid genome) is visualized for each of the Nigon elements for a representative set of species in different clades. Haploid regions are likely contiguous, but not visualized as such in these plots since data is plotted by the contig order in the reference genome. On the X-axis, distances between ticks represent 5 Mb. b Box plots showing the calculated N according to Nigon element reveals that B. malayi, B. pahangi, and W. bancrofti all share similar unpaired chromosome segments in males corresponding to ND and NX. L. loa appears to only be unpaired in males for ND, while O. volvulus and O. ochengi are unpaired in males for ND and NE. D. viviparus and N. americanus are unpaired in males for only NX, while P. pacificus is only partially unpaired in males for NX, as expected and previously described. The center line of the box plots is drawn at the median of the depth at each Nigon element, the upper and lower hinges are at the 25% and 75% quartiles of the depth, while the whiskers extend ×ばつ the interquartile range. Outliers are plotted as points outside of that range.
Fig. 4
Fig. 4. Sex-biased gene enrichment.
The percentage of male and female sex-biased genes at 30 and 120 dpi are shown relative to each Nigon element as well as the X chromosome and the Y-specific contigs. The percentage of sex-biased genes is compared to total genes on each particular Nigon element, chromosome, or set of contigs, which is shown as the black line. The stars represent significant statistical enrichment or depletion of sex-biased genes on that particular element as determined by Fisher’s exact test.

References

    1. Coghlan, A. Nematode genome evolution. WormBook, ed. The C. elegans Research Community, (WormBook, 2005). - PMC - PubMed
    1. Blaxter M, Koutsovoulos G. The evolution of parasitism in Nematoda. Parasitology. 2015;142(Suppl. 1):S26–S39. doi: 10.1017/S0031182014000791. - DOI - PMC - PubMed
    1. Blaxter M, Kumar S, Kaur G, Koutsovoulos G, Elsworth B. Genomics and transcriptomics across the diversity of the Nematoda. Parasite Immunol. 2012;34:108–120. doi: 10.1111/j.1365-3024.2011.01342.x. - DOI - PubMed
    1. Blaxter ML, et al. A molecular evolutionary framework for the phylum Nematoda. Nature. 1998;392:71–75. doi: 10.1038/32160. - DOI - PubMed
    1. Ghedin E, Wang S, Foster JM, Slatko BE. First sequenced genome of a parasitic nematode. Trends Parasitol. 2004;20:151–153. doi: 10.1016/j.pt.2004年01月01日1. - DOI - PubMed

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