Frogs renew their sex chromosomes

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The small European green frog (Pelophylax lessonae) is among the 28 species stud
The small European green frog (Pelophylax lessonae) is among the 28 species studied. - Christophe Dufresnes (DEE, UNIL)

A study reveals that over the course of their evolution, frogs of the family Ranidae have changed their sex chromosomes at least thirteen times. This is the highest documented turnover among vertebrates. Unlike humans and other mammals, ranids use at least five different pairs of sex chromosomes. In the red frog, the most common amphibian in Switzerland, the main gene that determines the sex of an individual - male or female - is located on chromosome pair 1. In its green cousin, it is located on chromosome pair 3. This indicates that in the course of their evolution, some species have diverged from their common ancestor to change their sex chromosome.

By creating a phylogenetic tree, a diagram that shows the relationships between 28 species of ranids, Daniel Lee Jeffries and Guillaume Lavanchy, respectively post-doctoral and doctoral students at the Department of Ecology and Evolution of the Faculty of Biology and Medicine of the University of Lausanne, were able to quantify and date these transitions.

Over the last 55 million years, the chromosome that determines sex has changed at least thirteen times. This figure is largely underestimated because we cannot quantify the intermediate transitions," says Guillaume Lavanchy, cofirst author of the study published in the scientific journal Nature Communications. However, to date, this is the highest turnover documented in vertebrates. By way of comparison, the Y chromosome (male) of some 6000 known species of mammals has not moved in 170 million years.

New conductor

Led by Professor Nicolas Perrin, the study was made possible thanks to the collaboration of research groups that sent frog DNA samples from around the world, including Japan, Spain, the United States and Armenia. The UNIL biologists put forward two possible explanations for these changes in sex chromosomes.

It could be that the main gene that determines sex, which is then responsible for activating a cascade of other genes, moves from one chromosome to another," explains Guillaume Lavanchy. But it is more likely that it is one of these secondary genes that, following a mutation, acquires the function of ’leader’. A hypothesis supported by the fact that the choice of the new sex chromosome is not random: only five of the thirteen pairs of chromosomes that frogs possess are recruited to take on this function.

In the agile frog (Rana dalmatina), the gene that determines sex is located on chromosome pair 5. - Christophe Dufresnes (DEE, UNIL)

Fighting against the degeneration of the Y

In addition to documenting these numerous and rapid sex chromosome changes, the study also provides insight into their causes.

At the time of meiosis (creation of eggs or sperm), part of the chromosome inherited from the mother mixes with that of the father. In male ranids, these recombinations take place only at the ends of the chromosomes. The central part of the Y no longer exchanges any genes, which favors the accumulation of deleterious mutations. By changing the sex chromosome, we believe that the frogs have found a way to overcome the degeneration of the Y. They create new males with a better quality Y which, little by little, take precedence over those whose Y has degenerated’, says Guillaume Lavanchy.

The male chromosome of humans suffers the same fate, but the chances of it being renewed are almost nil. Mammals have developed other mechanisms to compensate for the loss of genes on the Y," explains Nicolas Perrin.

at high speed

The scientists also point out the speed at which these sex chromosome transitions occur in ranids. Of thirteen observed changes, at least three have occurred in the last two million years, an evolutionary blink of an eye.

like the Japanese frogs living in the east and west of the island, three species use two distinct sex chromosomes simultaneously. This difference indicates that the change has taken place very recently and that the transition is underway. Eventually, one of the two types of males should disappear," says Nicolas Perrin.

More broadly, this study in population genetics overturns many of the knowledge of the mechanisms of evolution of sex chromosomes. Often perceived as static, it can turn out to be extremely rapid and dynamic," concludes the professor.