The dominant theory on the evolution of sex chromosomes challenged

In many animals and plants, sex chromosomes show marked differences both in structural and genetic terms. This is related to the fact that these chromosomes have lost the ability to recombine over part of their length. This is particularly the case in the human species between the X chromosome and the Y chromosome whose size is considerably reduced. The leading hypothesis postulates that successive deletions due to suppression of recombination results from the integration within these chromosomes of genes associated with the secondary sex characteristics specific to each of the two sexes, like the size of the mane in the lions or the bright coloration of the male plumage of certain birds. However, proof that such genes are carried by sex chromosomes is lacking and little evidence exists to support this theory.

A team of researchers, including Marco Coelho, post-doc researcher at UCIBIO in FCT NOVA, led by Tatiana Giraud at the Orsay Laboratory of Systematic Evolution (ESE, CNRS / Université Paris Sud / AgroParisTech) examine if other mechanisms dissociated from the determination of secondary sexual characteristics could be at the origin of the evolution of sex chromosomes. As a model study they have used five fungal species of the genus Microbotryum as a model of study, which have the particularity of being devoid of male and female sexes. These fungi are castrating floral smut pathogens that parasitize plants in the Caryophyllaceae. When infected by the fungus, plants eliminate pollen production in the anthers and replaces the pollen with fungal spores, which can then be transferred by pollinator to other plants, resulting in the spread of the infection.

Using new sequencing techniques allowing obtaining complete genome assemblies, “we have found that the chromosomes pairs involved in sex-type determinism had undergone successive waves of recombination suppression and deletions as evolution progressed despite the fact that these organisms do not show any phenotypic differentiation between males and females”, explains Marco Coelho, team member of the Yeast Genomics Lab. The results, published in PNAS, therefore underline that other mechanisms would be involved in the differentiation of sexual chromosomes. As such, the researchers hypothesized that chromosomal inversions or other rearrangements could have randomly affected one of the two sex-linked chromosomes during evolution. Once fixed by genetic drift, these changes may have led to the progressive extension of genomic regions incapable of recombining at the level of sex chromosomes. These advances therefore challenge the notion that sexual antagonism drives sex chromosome evolution.

Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism
Sara Branco, Hélène Badouin, Ricardo C. Rodríguez de la Vega, Jérôme Gouzy, Fantin Carpentier, Gabriela Aguileta, Sophie Siguenza, Jean-Tristan Brandenburg, Marco A. Coelho, Michael E. Hood and Tatiana Giraud
Proc Natl Acad Sci USA, 114(27):7067-7072
DOI: 10.1073/pnas.1701658114