Undesirable sex partners; bacteria manipulate reproduction of insects and other species - Wolbacteria cause cytoplasmic incompatibility in arthropods

Science News, Nov 16, 1996 by John Travis

It took a while before the medical community paid attention. The first known cases of what the tabloids gleefully called virgin births appeared, amusingly enough, in Las Vegas. Then physicians across the United States began documenting similar events. In each case, an unfertilized egg in a woman had spontaneously begun to develop, ultimately producing a healthy female baby. One young researcher, who had analyzed the timing and locales of the virgin births, suggested a spreading infection might be causing the incidents. The Federal Centers for Disease Control and Prevention in Atlanta quickly dismissed the idea, calling it "ridiculous." Several months later came a well-publicized report in the Journal of the American Medical Association concluding that the number of infertile couples was rising rapidly worldwide. The international uproar intensified when physicians began to observe another reproductive curiosity: Some newborns that were genetically male appeared to be female. One week, the New England Journal of Medicine and the National Enquirer ran articles with the headline, "Is this the end of mankind, or just men?"

Science fiction? Definitely. For many insect species and other arthropods, however, the truth can be as strange as fiction when bacteria known as Wolbachia are around.

These microorganisms populate cells in the testes and ovaries of arthropods, often profoundly altering the reproduction of their hosts. In some species, infected males can generate offspring only if they mate with infected females. In others, infected females give birth without the need for the opposite sex. In one arthropod species, Wolbachia even transform embryos that would normally be males into females.

"These traits have all evolved because they increase the transmission of the microorganisms," says John H. Werren of the University of Rochester (N.Y.), who has documented the diversity of animals infected by Wolbachia. There's no evidence that Wolbachia infects mammals, let alone humans, but that hasn't dulled biologists' fascination with them. "It's a very special group of bacteria," says Werren. Scientists first identified the bacteria in the reproductive tissues of a mosquito species in 1924.

Yet it took a mystery and several decades before Wolbachia truly entered the limelight. The mystery emerged in the 1950s, when insect geneticists encountered problems while trying to cross different strains of mosquitoes.

"They started to find all these crossing abnormalities," says Scott L. O'Neill of Yale University Medical School. The most obvious one, dubbed cytoplasmic incompatibility, centered on the failure of certain strains to produce offspring when mating with other strains of the same mosquito species.

Scientists argued for 20 years over what caused cytoplasmic incompatibility, says O'Neill. Then, in 1971, Janice Yen and Ralph Barr, biologists at the University of California, Los Angeles, tabbed Wolbachia as the culprit.

Cytoplasmic incompatibility, the researchers found, occurs when males infected with Wolbachia mate with uninfected females. In such unions, no offspring, or just a few in some host species, result. This reproductive barrier can be eliminated with antibiotics that rid the mosquitoes of the bacteria.

Why does Wolbachia generate cytoplasmic incompatibility? To favor reproduction by infected females, says O'Neill. That helps the bacteria, which dwell in the cytoplasm of egg cells, pass on to future generations.

In species affected by cytoplasmic incompatibility, infected females have no trouble reproducing with infected males. Infected females also breed easily with uninfected males. Both kinds of unions transfer Wolbachia to offspring. Consequently, cytoplasmic incompatibility can spread Wolbachia rapidly through an uninfected population, says O'Neill, who organized a session on Wolbachia at the recent Symbiosis 96! Meeting in Bar Harbor, Maine.

Researchers are finding that Wolbachia infects a surprisingly large variety of species. Werren and Donald Windsor of the Smithsonian Tropical Research Institute in Panama reported last year that 16 percent of Panamanian insect species, including some in all of the major insect orders, harbor Wolbachia. Since the estimated number of insect species ranges from 10 million to 30 million, that means roughly 2 million to 5 million insect species play host to the bacteria.

"That's very much an underestimate," adds Werren, noting that researchers have time to test only a limited number of insects from each species.

Scientists have also found that Wolbachia infects a variety of isopods (a subgroup of crustaceans that includes wood lice), at least one species of mites, and perhaps even a worm species.

Wasps are among the favored hosts of Wolbachia. Take the jewel wasp, Werren's favorite research subject. Wolbachia infections in these insects produce an odd variation on cytoplasmic incompatibility: Uninfected female wasps mating with infected males can produce offspring, but their progeny are all male.