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How Supergenes Shape Evolution | Scientific American

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Conventional wisdom holds that sexual reproduction evolved because it enables organisms to shuffle, or recombine, different alleles (versions of a gene) in the next generation, producing the genetic variation that is foundational to natural selection and adaptation. But in recent years researchers have started to find that all regions of the genome do not shuffle equally. Some regions, which can contain just a few genes or sometimes hundreds, rarely shuffle. As a result, the same combination of alleles is transmitted all together to the next generation. These genetic units, called “supergenes,” have so far been found in ants, butterflies, birds, fish, plants and fungi—and many more likely still await discovery.

Researchers hypothesize that supergenes evolve in much the same way that sex chromosomes have: over evolutionary time, alleles that work well in males but not in females were selected to be transmitted together, leading to a growing region of suppressed recombination between the X and Y chromosomes in mammals, for example. This region of suppressed recombination can expand as more alleles that are advantageous in one sex but not the other occur near the original region of suppressed recombination and become included within that region. This phenomenon is called sexually antagonistic selection. Now researchers have revealed that sex chromosomes are just a special case of a broader phenomenon. Supergenes (regions of suppressed recombination) can be involved in the regulation of a variety of other traits. In fact, they are capable of regulating social organization—in this case, in Formica wood ants.

“There is an evolutionary force [antagonistic selection] that will be expected to cause sex chromosomes to expand, and the presence of that evolutionary force was also expected to be observed in supergenes. And here we are confirming it for the first time,” says Buck Trible, who studies ant supergenes at Harvard University.

Supergenes can have a big impact on the organization of Formica wood ant societies. The ants have a supergene on chromosome 3 that controls whether the colonies have single or multiple queens. Researchers at the University of California, Riverside, recently discovered that these wood ants have yet another supergene on chromosome 9 that regulates the size of the queens: one version of this supergene produces miniature queens that are about 20 percent smaller than the normal-sized queens.

The researchers found that the miniature queens almost exclusively occur in colonies with multiple queens. In other words, the version of the supergene on chromosome 9 that produces multi-queen colonies is tightly linked to the version of the supergene on chromosome 3 that makes miniature queens.

The chromosomes do not appear physically fused together, and the researchers observed that more than 20 percent of ant eggs have “mismatched” supergene combinations—for instance, an ant might have the version of chromosome 3 that makes single-queen colonies as well as the version of chromosome 9 that produces miniature queens. Few of these individuals with mismatches survive to adulthood, suggesting that there is strong selection against mismatched combinations.

“Our hypothesis is that whenever there are these mismatches, the individual tends to develop into a worker (rather than a queen),” explains entomologist Giulia Scarparo, lead author of the new paper. In addition, “there is a mechanism that is [negatively] affecting the development of the individuals, which is why we don’t see this mismatch commonly in the adult stage.”

The strong selection against mismatched combinations is what the researchers call “socially antagonistic” selection because it parallels the sexually antagonistic selection that drives the evolution of sex chromosomes.

Typically, in single-queen colonies, when new queens reach maturity, they go on a nuptial flight and then establish a new colony, using their own body fat and muscles to produce the first brood. Small queens are less likely to be successful in establishing a colony on their own because they have fewer metabolic resources. Thus, smaller queens can only survive and reproduce inside colonies of multiple queens.

In fact, the researchers think that the evolution of multi-queen colonies was a necessary precondition for the evolution of the miniature queens, which can then rely on resources from the workers produced by other queens in the multi-queen colony to provide for their offspring. Some of these tiny queens then invest a disproportionate amount of their resources into producing more tiny queens without producing their fair share of workers that contribute to the upkeep of the colony. “We hypothesize that the small queens could be social parasites,” Scarparo says.

There are several hundred species of workerless social-parasite ant species, which live inside the nests of their close relatives and parasitize the food and labor of the host colony to raise their brood. How these socially parasitic species evolved exactly has remained a mystery, though it’s likely that these social supergenes are involved.

The most common way that recombination is suppressed in supergenes is by inversions on chromosomes—a section of a chromosome gets flipped from top to bottom and the order of genes in that sequence is reversed. That inversion prevents corresponding, or homologous, regions from lining up and recombining during meiosis, the process of cell division that produces sex cells (sperm or eggs). The absence of genetic shuffling can lock together two mutations in different genes that work well together. “And once something like an inversion occurs, all the genetic variation that just happened to be present with the two beneficial mutations is now essentially forever locked with them, sort of like a historical accident,” explains Marcus Kronforst, who studies supergenes in butterflies at the University of Chicago.

Within many supergenes, including the social supergene in these ants, several genes probably work together—and many others are just innocent bystanders stuck in the region of suppressed recombination. In the wood ants, “there are about 500 genes on the social supergene, but we suspect that only a small fraction of those actually contribute to colony queen number directly, and other things are carried along for the ride,” says Jessica Purcell, senior author of the new paper, who studies ants at UC Riverside.

That has implications for the evolution not only of the traits controlled by the supergenes but all the traits regulated by genes that get caught along for the ride on the supergene. The flip side of locking together beneficial combinations is that over time, regions of suppressed recombination can accumulate bad mutations, and they are near impossible to purge from the gene pool because they are tied to the other beneficial traits in the supergene.

So part of what maintains multiple versions of a supergene in the population is that “you’ll have some benefit associated with the inversion haplotype, but there’s also some detriment associated with it, because it’s forever connected with some amount of deleterious genetic variation,” Kronforst explains.

Kronforst studies a supergene in swallowtail butterflies that controls the color pattern and shape of their wings. In the swallowtail Papilio polytes, females have four possible different wing color patterns, three of which mimic a different poisonous butterfly (only females of the species demonstrate the mimic wing patterns on their wings).

A few years ago Kronforst’s team sequenced the genome of the swallowtail to better understand the supergene that regulated the wing shape and color, expecting to find hundreds of genes contained within it. But it turned out that the shape and color were controlled by just one gene, called doublesex, which is also involved in controlling sexual dimorphism, differences in body type displayed by different sexes in members of the same species. The butterflies have co-opted doublesex to control wing patterning in females, Kronforst explains.

In this swallowtail butterfly, doublesex exists in four versions (haplotypes). The gene is within a supergene that is inverted on the chromosome such that recombination rarely if ever occurs within the gene. This is critical because if recombination were to occur, the resulting wing pattern would be a mishmash of different patterns that would not mimic any toxic butterfly—thus making butterflies with the mixed-up wing patterns extremely vulnerable to being eaten by predators. The supergene inversion, with its suppressed recombination, ensures that the four wing patterns remain distinct and do not mix and match.

Kronforst’s team is now studying how the mimicry is regulated in close relatives of the swallowtail Papilio polytes. The researchers have found that other species also use doublesex, but in some of them there is no inversion to keep the different haplotypes separate from one another. “We have no idea what’s preventing recombination between the alleles in these other species,” Kronforst says. They are clearly not recombining very much—but how the butterflies pull that off isn’t clear. What it shows is that inversions are just one way to suppress recombination, and there are other ways that still need to be discovered.

“I think variation in the recombination landscape across the genome is one of the next frontiers in thinking about evolution,” Purcell says. “We know that there are parts of chromosomes where there’s a lot of recombination and parts where there’s less. And the degree of linkage between genes in those regions can have really important implications for the evolutionary trajectory of whatever traits are under their control.”

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