Parasitic worms reveal new insights into sex and sex chromosome evolution

ab. 1: Schematic picture designed by the authors: During the evolution, different chromosome elements represented by the Lego bricks (NA, NB, NX, etc. in the figure) were added to the ancestral sex chromosomes in different species, giving the great diversity of sex chromosomes of nematodes . These ‘Lego’ combinations of chromosome elements are shown as corresponding colors for each ‘clade’ of nematode species. (C: Quzijian)

Qi Zhou’s research group of the University of Vienna and the University of Zhejiang is studying two very diverse phyla of worms that harbor numerous parasites that cause disease in humans and livestock and shed light on how sexual reproduction and the subsequent great diversity of sex chromosomes may have evolved. .

Separated-sexed animals or plants are widespread in nature and are the result of independent transitions from their hermaphroditic ancestor. The actual mechanism involved in the transitions between asexual and sexual reproductive modes, in other words, how sex originated, remains an important and unanswered question. With the exception of insects, about a third of animal species, such as earthworms, snails and some teleosts, are hermaphrodites. A comparison with their relatives who developed separate sexes could reveal how this particular trait arose and evolved in animals.

A new paper in Nature Communications, published by Qi Zhou of the Department of Neuroscience and Developmental Biology at the University of Vienna and Zhejiang University in China, provides clues about how segregated sexes originated and characterizes how sex chromosomes evolved in flatworms or roundworms.

Two worm phyla provide clues as to how sex chromosomes may have evolved

Although both phyla are called “worms”, they are very different from each other from an evolutionary point of view. A common feature of both phyla is that numerous representatives, such as tapeworms and schistosomes (commonly known as blood fins), are parasites to humans or livestock and can cause severe symptoms and complications. Identification and investigation of their sex-related genes may provide the basis for disruption of their reproductive cycle in the future for effective parasite control.

The research group around Qi Zhou collected already published genome and transcriptome data from 41 nematode species and 13 flatworm species, the latter mainly comprising hermaphroditic species, except schistosomes (bloodworms). Of these, they identified the sex chromosome composition of 17 nematode species in terms of “Nigon elements”. These are ancestral chromosome units shared by all nematodes, and named after the nematode biologist Victor Nigon (parallel to fruit fly “Muller elements”, another genetic model species). With this comparison, the authors showed that the great diversity of sex chromosomes of nematodes is the result of different combinations of Nigon elements. By repeated addition of several Nigon elements, which were previously non-sex chromosomes, to the ancestral sex chromosomes, several nematode species expanded their sex-linked regions which later suppressed recombination during evolution.

Blood fins – from hermaphrodite to separated sexes

Another important finding comes from the comparison of the sexually reproducing blood fins with related hermaphroditic species. The transition to the segregated state in the parasite occurred relatively recently, about 70 million years ago. The authors showed that during this transition, the gonad genes of schistosomes became less “feminized,” in other words, they generally showed a lower ovarian expression level compared to their counterpart in the hermaphrodite related species. They also identified a candidate gene, mag-1, whose disruption in schistosomes causes enlarged testis. Mutations in this gene may have played a critical role in the transition to the separate lineages of schistosomes.

Publication in Nature Communications:

Wang, Y., Gasser, RB, Charlesworth, D. et al. Evolution of sexual systems, sex chromosomes and sex-linked gene transcription in flatworms and roundworms. Nat Commun 13, 3239 (2022).

DOI: 10.1038/s41467-022-30578-z

Image:

ab. 1: Schematic picture designed by the authors: During the evolution, different chromosome elements represented by the Lego bricks (NA, NB, NX, etc. in the figure) were added to the ancestral sex chromosomes in different species, giving the great diversity of sex chromosomes of nematodes . These ‘Lego’ combinations of chromosome elements are shown as corresponding colors for each ‘clade’ of nematode species. (C: Quzijian)

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