Most evolutionary biologists distinguish one species from another based on reproductivity: members of different species either won’t or can’t mate with one another, or, if they do, the resulting offspring are often sterile, unviable, or suffer some other sort of reduced fitness.

For most of the 20th century, scientists believed that this reproductive incompatibility evolved gradually between species as a by-product of adapting to different ecological circumstances: if two species were geographically isolated, they would adapt differences based on their environment. New research conducted at the University of Rochester, in collaboration with the University of Nebraska, shows, however, that there are more factors at play—specifically the presence of selfish genes called meiotic drive elements, whose flow among species may dictate whether two species converge or diverge. In a new paper published in the journal eLife, the researchers show that sex chromosomes evolve to be genetically incompatible between species faster than the rest of the genetic chromosomes and reveal the factors at play in this incompatibility.

When members of a species mate and exchange genetic material, this is known as gene flow. But, when there are genetic incompatibilities between species, gene flow is reduced. “Genes from one species can’t always talk to genes from the other species,” says Daven Presgraves, a Dean’s Professor of Biology at Rochester. Though genes may work fine in their own genetic background, they can have negative effects when they are moved into the genetic background of another species. “All of the gene copies in you and me function well in the human genome. But if we take a gene from us and stick it into a chimpanzee, it may not function properly— it hasn’t seen this genome before, and it might not work together with the chimpanzee’s genes. That could compromise some aspect of development or fertility.”

This is what happened when Presgraves and members of his lab crossed two different species of fruit flies, one from Madagascar and the other from the island of Mauritius. When the two species were crossed, their hybrid female offspring were fertile, but their hybrid male offspring were completely sterile. “One of the steps during the gradual evolutionary build up of complete reproductive incompatibility is that the XY sex becomes sterile first,” Presgraves says.

Chromosomes are divided into two types: sex chromosomes and autosomes. Sex chromosomes are the XY chromosomes that denote a male in both fruit flies and humans and the XX that denote a female. When the researchers mapped the factors that cause hybrid males to become sterile, they found that there were many more incompatibility factors on the X sex chromosome compared to on the autosomes. This means that sex chromosomes become functionally different between species much faster than non-sex chromosomes, Presgraves says.

But what is it that makes sex chromosomes evolve genetic incompatibilities faster than the rest of the genome?

The researchers found that a class of “selfish genes” called meiotic drive elements are partly responsible for making sex chromosomes genetically incompatible at a faster rate. In general, selfish genes are parasites of the genome—they propagate themselves at the expense of other genes. Meiotic drive elements in particular subvert the rules of typical inheritance: in normal Mendelian inheritance, a gene is transmitted to half of the offspring. Meiotic drive elements, however, manipulate reproduction so they can transmit themselves to greater than 50 percent—more than their fair share. In male fruit flies, meiotic drive elements usually kill sperm that don’t carry them, leaving only (or mostly) sperm that do.

“When multiple meiotic drive elements from both parental species are unsuppressed in hybrids, their combined action can cause sterility,” says Colin Meiklejohn, an assistant professor of biology at the University of Nebraska and former postdoctoral researcher in Presgraves’s lab.

In a twist, however, the researchers also found that if meiotic drive elements have the opportunity for gene flow between species, they can also help bring species together. During the early stages of speciation, when two different species are just beginning to break away from one another, reproductive incompatibility can be incomplete and “leaky”—some parts of the genome may still be compatible and exchangeable.

“If two populations are leaky and there is opportunity for gene flow, a selfish gene can migrate from one species to another and spread there,” Presgraves says. If the selfish gene is functional in the other species, instead of becoming incompatible, “that part of the genome will become perfectly exchangeable. In some cases, then, a selfish gene can erase the buildup of incompatibilities for a part of the genome.”

That is, meiotic drive elements can cause incompatibilities between species if they do not experience gene flow, or they can cause a convergence of the species, if the species does experience gene flow. A major factor in determining whether or not a species is compatible hinges on how much gene flow occurs between the species, Presgraves says. “Species— even ones that are geographically isolated—are leakier than we thought.”

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Category: Science & Technology