Down with the Male-Killers: A Tale of Evolution in Our Time

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Like many parasites, a species of bacteria called Wolbachia takes charge of its own fate. Wolbachia can only survive inside the cells of its hosts–invertebrates such as this lovely common eggfly. This way of life limits Wolbachia’s opportunities for long-term survival. If Wolbachia lives inside a female insect, it can infect her eggs. When those eggs hatch and mature into adult insects, they will be infected by Wolbachia as well. But if Wolbachia should find itself in a male, it has reached a dead end. It cannot infect sperm cells, and thus it has no escape from a male host. When a male host dies, Wolbachia dies as well.

Wolbachia’s solution: kill the males before they kill you.

In many species, Wolbachia is lethal to male embryos. As a result, Wolbachia-carrying females only give birth to Wolbachia-infected females. Male killing boosts Wolbachia’s population in two ways. With fewer Wolbachia-free males around, the proportion of eggflies carrying the bacteria goes up. And without males to compete for food, Wolbachia-infected females may be able to increase their odds of surviving until they can reproduce–and produce more Wolbachia.

Male-killing is not the only weapon Wolbachia uses on its hosts. When some strains infect wasps, they alter the females so that their eggs start spontaneously turning into embryos without any need of sperm. All of these sperm-free embryos become females, which can also produce female offspring without the help of males. In other species, Wolbachia allow males to be born but alters their hormones to feminize them and make them produce eggs. And in other cases, Wolbachia decides which males and females may mate with one another. If a healthy female mates with a male carrying Wolbachia, some or all of her fertilized eggs will die. But a female carrying Wolbachia can mate with either infected or uninfected males and produce viable eggs–all of which have Wolbachia in them.

With all these different ways of manipulating their hosts, Wolbachia has become perhaps the most successful species of infectious bacteria on the planet, infecting millions of species of invertebrates.

Scientists have long wondered if the hosts of Wolbachia have any way of defending themselves against the assaults of the bacteria. In a Wolbachia-infected population, a few males get to mate with a lot of females. Any mutation that can allow eggflies to have sons despite the presence of male-killing should be strongly favored by natural selection. While this explanation makes sense on paper, scientists have until now found little evidence of the suppression of male-killing.

There are two possible explanations for this state of affairs. One is that for some reason the suppression of male killers evolves only rarely. The other is that it actually evolves very quickly. It spreads so quickly through populations that there is little outward sign that the hosts have silenced a male-killer.

Today in the journal PLOS Biology, scientists report that the latter is true: male-killer defenses evolve very fast. Over the past few years the scientists have studied eggflies from Southeast Asia and the Pacific. They’ve found that on some Polynesian Islands, male-killing Wolbachia is a common pathogen. But in other parts of its range, the eggfly is infected by the same strain of Wolbachia, but it produces a normal fifty-fifty split of males and females.

To compare these populations, the scientists bred eggflies from the island of Moorea, where Wolbachia is a male-killer, with eggflies from Thailand and the Philippines, where it is not. They found that female Moorea eggflies produced a normal fraction of males if they could mate with male eggflies from Thailand and the Philippines. But if the hybrid females then mated with eggflies from Moorea, they produced fewer and fewer males over the generations. Experiments such as these demonstrated that eggflies from Thailand and the Philippines have a hereditary ability to stop Wolbachia from killing their sons. They may use only one gene to shut the parasite down.

The authors conclude from their experiments that Wolbachia jumped into the eggflies some time in the past and began killing males as it spread through much of the eggfly’s range. The eggflies then evolved a defense against the bacteria. Females that could produce more males were favored by natural selection, until the ratio of the sexes evened out again at fifty-fifty. They continued to carry the bacteria, but Wolbachia was rendered impotent. The dramatic changes the scientists saw in their breeding experiments, suggest that the gene for suppressing male-killing could have spread very quickly through an eggfly population–perhaps in less than 100 generations (about 25 years). Historical records agree. Scientists in the 1960s found all-female populations of eggflies in Borneo, but they’re gone now, 160 generations later.

The scientists predict that as eggflies flit about the Pacific, females carrying the suppressor gene will outcompete the females vulnerable to male-killing. Soon male-killing will become a thing of the past–at least until some strain of Wolbachia hits on a new way to take control of its eggfly hosts. If the scientists are right, then the history of Wolbachia is even more turbulent than once thought. It is infecting a vast number of invertebrates despite their rapid evolution of defenses against them. As it is muzzled in one population, it finds new ways to manipulate another.

Wolbachia is not alone in distorting the ratio of the sexes. An organism’s own genes may sometimes tip the balance. Sex-distorting genes sit on the chromosomes that determine an animal or plant’s sex. In humans, two X chromosomes produce a female, and an X and a Y produce a male. If a gene on an X chromosome can raise the odds that its chromosome will be passed down to an offspring, that gene will become more common. And it will increase the number of females in a population.

Sometimes called meiotic drive, this evolutionary force is often countered by another: genes that suppress the tilt towards one sex over the other. Plenty of examples of meiotic drive have been documented in flies and other species. A few clues have emerged from studies on humans, but just a few. If the new study on Wolbachia is right, I wonder if some scientists will look more closely at our own selfish genes. There might be some hidden tugs-of-war waiting for someone to discover.

Update 822 1:20 pm: Josh at Thoughts from Kansas knows about the strange ways of Wolbachia first hand.