Parasitic worms reveal new information about the evolution of sex and sex chromosomes

Abb. 1: Schematic image designed by the authors: During evolution, different chromosomal elements represented by the Lego bricks (NA, NB, NX..etc. in the figure) were added to the ancestral sex chromosomes in different species, forming the great diversity of nematode sex chromosomes. These “Lego” combinations of chromosomal elements are represented by corresponding colors for each “clade” of nematode species. (C: Quzijian)

By studying two highly divergent worm phyla that contain numerous parasites that cause human and livestock disease, Qi Zhou’s research group from the University of Vienna and Zhejiang University shed light on the evolution of sexual reproduction and the subsequent great diversity of sex chromosomes.

Animals or plants with separate sexes are widespread in nature and result from independent transitions from their hermaphrodite ancestor. The actual mechanism involved in the transitions between asexual and sexual modes of reproduction, in other words, how sex originated, remains an important and unanswered question. Excluding insects, about a third of animal species, such as earthworms, snails, and some teleosts, are hermaphroditic. A comparison with their parents who developed separate sexes could reveal how this particular trait originated 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 to the origin of the separate sexes and characterizes the evolution of sex chromosomes in flatworms or roundworms.

Two worm phyla give clues to how sex chromosomes might have evolved

Although the two phyla are called “worms”, from an evolutionary point of view they are very divergent from each other. A common feature of both phyla is that many representatives, such as the tapeworm and schistosomes (commonly called blood flukes), are parasites of humans or livestock and can cause serious symptoms and complications. Identifying and studying their sex-linked genes can provide the basis for disrupting their reproductive cycle in the future for effective parasite control.

The research group surrounding Qi Zhou collected previously published genome and transcriptome data of 41 species of nematodes and 13 species of flatworms, the latter comprising mainly hermaphroditic species except for schistosomes (blood flukes). Among these, they identified the composition of the sex chromosomes of 17 nematode species in terms of “Nigon elements”. They are ancestral chromosomal units common to all nematodes, and named after the nematode biologist Victor Nigon (alongside the “Muller elements” of the fruit fly, another genetic model species). With this comparison, the authors showed that the great diversity of nematode sex chromosomes is the result of different combinations of Nigon elements. By recurrent addition of different Nigon elements, which were previously non-sex chromosomes, onto ancestral sex chromosomes, different species of nematodes extended their sex-linked regions, which subsequently suppressed recombination during evolution.

Blood flukes – from hermaphrodite to separate sexes

Another important finding comes from comparing sexually reproducing blood flukes with related hermaphroditic species. The transition to the state of separate sexes in the parasite occurred relatively recently, about 70 million years ago. The authors showed that during this transition, the gonadal genes of schistosomes became less “feminized”, that is to say showed an overall lower level of ovarian expression compared to their counterpart of related hermaphroditic species. They also identified a candidate gene, mag-1, whose disruption in schistosomes causes testicular enlargement. Mutations in this gene may have played a critical role in the transition to separate sexes of schistosomes.

Publication in Nature Communications:

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

DO I: 10.1038/s41467-022-30578-z

Image:

Abb. 1: Schematic image designed by the authors: During evolution, different chromosomal elements represented by the Lego bricks (NA, NB, NX..etc. in the figure) were added to the ancestral sex chromosomes in different species, forming the great diversity of nematode sex chromosomes. These “Lego” combinations of chromosomal elements are represented by corresponding colors for each “clade” of nematode species. (C: Quzijian)

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