Given the dramatic difference in the size and sequence of the human X and Y chromosomes, it’s hard to imagine that they were once a perfect matching pair. But in fact all sex chromosomes start out that way. New research published today (July 19) in Science examines the early phase of sex chromosome evolution in a strain of fruit flies that recently—1 million years ago—converted a normal pair of chromosomes into a new mismatched X and Y duo.
“This paper is definitely an exciting contribution to the understanding of the early days of sex chromosome evolution,” said evolutionary biologist Manyuan Long of the University of Chicago, who was not involved in the research. “Now we know that, in nature, sex chromosomes can evolve very rapidly.”
The human X and Y chromosomes are thought to have originated from a matching pair of non-sex chromosomes, or autosomes, some 200 million years ago. And now, they are so different that they share just a tiny length of sequence. Indeed, “the human X has about 1,000 genes, and the Y only has about 50,” explained Doris Bachtrog of the University of California, Berkeley, who led the new study.
Most research on sex chromosome evolution has been limited to recent changes, usually after the chromosomes have already diverged quite significantly in structure. But as luck would have it, Bachtrog knew of a fruit fly species in which new sex chromosomes had arisen relatively recently. Drosophila miranda flies, developed their new X and Y chromosomes about a million years ago when an autosome fused with the preexisting Y chromosome. This fusion generated a neo-Y, only carried by males, and the autosome’s matching partner became a neo-X, of which males get one copy and females get two. In closely related D. pseudoobscura flies, which share an ancestor with D. miranda, this fusion did not occur. Comparison of these two species’ genomes thus allowed Bachtrog to examine how D. miranda’s new X and Y have changed since becoming sex chromosomes.
The fusion event that formed the neo-X and -Y in D. miranda led approximately 3,000 genes to become sex-linked, said Bachtrog. And after a million years, more than 40 percent of those genes on the neo-Y have already lost their function. “Really quickly after you become a sex chromosome, the Y chromosome massively degenerates,” Bachtrog said.
Degeneration of Y chromosomes is a commonly accepted phenomenon, “but what was surprising was just how quickly it can happen,” Bachtrog said. “It is very surprising that in such a short period of time, more than one third of the genes become silenced,” agreed Long.
As for the remaining functional neo-Y genes, a significant subset has evolved male-specific functions. “The Y chromosome is becoming masculinized,” said Bachtrog. These genes not only experienced high rates of adaptive protein evolution, she said, but they also tended to be expressed in male-specific tissues, such as the testes and prostate.
Meanwhile on the neo-X, both female- and male-specific forces are at play. “The X chromosome is actually undergoing quite peculiar evolutionary pressures,” said Bachtrog. “On young X chromosomes we see this male-specific selection to be the dominant force, but the older it becomes, the more the gene content switches and you start accumulating female-specific genes.”
“This quick burst of [male]-adaptive evolution on the neo-X is really surprising,” said Judith Mank of University College, London, who was not involved in the research. She explained that while people had proposed it might occur—because males carry only one copy of X chromosome genes, so the selection pressure for male-beneficial mutations is strong—the evidence for it in the animal kingdom was scarce. “[It] is not as pervasive as one would think,” Mank said. The new work suggests that it does happen, but only early in X evolution. When researchers study older X chromosomes, the female-beneficial changes have already taken over.
This switch to female-beneficial genes takes place because females carry two copies of the X chromosome, meaning that the chromosome is under selection in females twice as often as it is in males. However, due to the fact that males also carry a copy of the X, mutations that benefit females but not males take longer to spread through the population. Also, unlike the male-beneficial mutations to the X that occur early in X evolution and are a compensatory response to the fact that males suddenly have only one X copy, female-beneficial changes often involve larger-scale events, such as new gene functions or movement of female-related genes from other chromosomes. “Gene trafficking is just a much slower process compared to just incorporating new amino acids,” explained Bachtrog.
As sex chromosomes continue to evolve, degeneration of the Y chromosome could even lead to its eventual loss, requiring the emergence of a new sex determination mechanism on another chromosome. Though such a possibility has been ruled out in humans, said Bachtrog, the way males and females arise “is completely variable between species and even within species.” In some fly families, for example, sex chromosomes have even been incorporated back into autosomes. “Sex chromosomes are not necessarily this evolutionary trap that you end up with and they never change,” she said.
Q. Zhou, D. Bachtrog, "Sex-specific adaptation drives early sex chromosome evolution in Drosophila," Science, doi: 10.1126/science.1225385, 2012.