Invasion of the gender benders: by manipulating sex and reproduction in their hosts, many parasites improve their own odds of survival and may shape the evolution of sex itself

Natural History, Feb, 2003 by John H. Werren

When the bacteria in parthenogenetic insects are killed with common antibiotics such as tetracycline, the insects usually revert to sexual reproduction. Sometimes, however, the insect species have been parthenogenetic for so long that when the Wolbachia bacteria are eliminated, the insects can no longer reproduce sexually. In the small parasitic wasp Encarsia formosa, antibiotics lead to the production of males, but the males cannot mate: the genes needed for male courtship have been lost. Other wasp species have similar stories to tell. In some, the females no longer respond to courtship; in others, the males no longer produce functional sperm. Given enough time, mutations accumulate in the genes for sexual characteristics, and the species can no longer revert to sexual reproduction. Their reproduction becomes completely dependent on the bacteria that live inside their cells.

But perhaps the most intriguing effect of Wolbachia is the ability of some strains to induce an incompatibility between host sperm and eggs, a process that may even implicate the microorganisms in the evolutionary divergence of insect species. The discovery of these capabilities has a long history. Wolbachia bacteria were first observed in the 1920s, when the pathologists Arthur Hertig and S. Burt Wolbach, working at Harvard Medical School, found them inside the eggs of Culex mosquitoes. Hertig later named the bacterial genus in honor of his colleague and mentor. In the 1950s the German biologist Hannes Laven discovered that when males from some strains of the mosquito C. pipiens were crossed with females of another strain, the offspring died as embryos. Laven subsequently showed that the effect was inherited through the mother's lineage. As he viewed it, the cytoplasm in the eggs of certain strains of insects was incompatible with the sperm from certain other strains. Laven was apparently unaware, however, that bacteria had earlier been discovered in the eggs of the insects.

It wasn't until the early 1970s that two other investigators, Janice H. Yen and A. Ralph Barr of the University of California, Los Angeles, made the connection. They showed that Laven's "cytoplasmic incompatibility" was caused by the bacteria. Antibiotic treatments that eliminated the bacteria also changed the compatibility relationships between males and females.

The basic pattern is that eggs from uninfected females are incompatible with sperm from infected males. The Wolbachia present in the testes of males biochemically "encrypt" the developing sperm, probably by altering proteins that bind to the sperm DNA. The same strain of Wolbachia must then be present in the egg to "decode" the encrypted sperm. Otherwise the chromosomes from the sperm are not properly processed in the fertilized egg, and the embryo dies. The actual mechanisms are still a mystery, but it is already clear to investigators that there are many different kinds of Wolbachia, which differ in their encryption systems.

The diversity of the encryption mechanisms raises the possibility that Wolbachia could play a role in the evolution of new insect species. If different populations of a species, or closely related species, are infected with different strains of Wolbachia, the bacteria could prevent the insects' gene pools from mixing. Just such a circumstance may have arisen in jewel wasps, a genus (Nasonia) of small parasitic wasps that kill fly pupae. There are three closely related species of jewel wasps, but each is infected with its own distinct Wolbachia. The bacteria render any matings between the different wasp species incompatible, thereby preventing the development of hybrids.