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Category: Evolution • Organisms • Reproduction • Science
Posted on: July 13, 2007 1:14 PM, by PZ Myers
If you've been reading that fascinating graphic novel, Y: The Last Man(amzn/b&n/abe/pwll), you know the premise: a mysterious disease has swept over the planet and bloodily killed every male mammal except two, a human named Yorick and a monkey named Ampersand. Substantial parts of it are biologically nearly impossible: the wide cross-species susceptibility, the near instantaneous lethality, and the simultaneity of its effect everywhere (there are also all kinds of weird correlations with other sort of magical putative causes, which may be red herrings). On the other hand, the sociological part of the story seems very plausible. There is no feminist utopia, the world goes on in a traumatized and rather complicated way, and the reactions everywhere vary from crazed euphoria to a more common despair. One thing that isn't at all implausible, and actually has been observed, is a plague that selectively exterminates males.
It's called Wolbachia. It's not quite as dramatic as the plague that turns males into hemorrhaging corpses in the graphic novel — it kills developing males as embryos, or more sneakily, disrupts sex determination so that all the embryos develop as females. This is advantageous to the bacterium, because it is transmitted in the cytoplasm of the egg, so males won't pass it on to their progeny and are useless from the point of view of Wolbachia. It is, like the plague in Y, something that infects a huge range of species, but each species varies in the severity of its response to the bacterium.
My readers with simple camera eyes will be relieved to know that the disease only affects arthropods. Those of you with compound eyes ought to worry: Wolbachia is also being being considered for use as a biological pesticide.
Now here's a disease that can have dramatic effects on a population—in some cases, the sex ratio can shift from 50:50 females:males to 99:1. That can be devastating to a population, although of course it's nowhere near as severe as if that ratio were reversed. Here's where evolution comes into play. What if a mutation for resistance to the sex-distorter effects of Wolbachia arose? What if, say, one of the rare males carried an allele that made his male progeny able to fight off the deleterious effects of infection with Wolbachia?
I think you can guess. That would be a greatly beneficial mutation that would spread with extraordinary rapidity. Since the rare male carriers would face little competition and would be fertilizing many females, they ought to produce lots of progeny and lots more males, who would spread the resistance further.
Now such an example of evolution in action has been directly observed. Butterflies of the species Hypolimnas bolina, the Blue Moon butterfly, in the Polynesian islands have been known for several years to be suffering from an extreme case of the sex-ratio distorter infection, with populations consisting of greater than 99% females. In 2005-2006, males were found to be making a comeback, and a complete shift from a highly skewed sex ratio to the more normal 50:50 proportions was observed to occur in only 10 generations — about a year. It's a beautiful example of how rapidly natural selection can transform a population when selection pressures are high.
The cause of the change is not eradication of Wolbachia — the animals are still carrying the bacterium. It is also not a result of the bacterium reducing its virulence autonomously, since introgression of Wolbachia from resistant populations into susceptible ones showed a full return of the male-killing ability of the bacterium. Something in the nuclear genome of the butterfly had changed to confer resistance.
Now here's one thing that bugs me about Y: The Last Man. For this rapid dispersal of resistance to spread, resistant males should be procreating profligately. In the book, Yorick seems to be obstinately abstinent! (Some of the women, at least, understand the principle, and there are plots with attempts to capture the last man for breeding stock for their group.) I can understand how the author might want to resist turning the story into a boring male fantasy of having the only penis among teeming millions of fertile females, but come on, biological reality has to intrude at some point. The future of the human race demands it!
Charlat S, Hornett EA, Fullard JH, Davies N, Roderick GK, Wedell N, Hurst GDD (2007) Extraordinary flux in sex ratio. Science 317:214.
''H. bolina'' is  known colloquially as the Blue Moon Butterfly or Great or Common Eggfly and is found mainly in the South Pacific.
Scientists reported that they had documented very fast evolution in the butterfly species ''Hypolimnas bolina''. After infection by ''Wolbachia'', the fraction of the population that was male dropped drastically to about one percent of the total population. However, after approximately ten generations (about a year) the male population had rebounded to about 39 percent of the overall population. 

In the case of ''H. bolina'', infected females were unable to have male offspring since the male embryos died early on. However, a gene arose which suppressed ''Wolbachia'''s ability to kill the male offspring, and this gene spread rapidly through the natural ''H. bolina'' population.

At this time, it is unknown if the novel gene was a mutation or a pre-existing gene. However, researchers said that regardless, the findings constituted strong evidence that parasites can drive and substantially alter evolution. The research was performed by scientists at the University of Berkeley lead by Sylvain Charlat, a post-doc at Berkeley.

Public Library of Science / Scott O'Neill

''Wolbachia'' is a bacterium that is very effective at jumping from species to species, generally infecting arthropods such as insects. Since the bacterium resides in the cytoplasm of cells, males cannot pass ''Wolbachia'' onto their offspring because sperms only pass on their nucleus with the DNA, but females can. ''Wolbachia'' has thus adapted a number of strategies, such as killing male embryos of infected females or preventing infected males from reproducing with uninfected females.

''Wolbachia'' is dangerous to hosts because it is able to easily jump species barriers and so has little reason to restrain itself -if an infectious organism kills its host, it generally dies along with it. The bacterium is believed to be responsible for some extinction events as well as some speciation events.