January 1997

In Praise of Superfly

By David Tenenbaum

When population geneticist Lisa Meffert began growing houseflies in her lab at the University of Houston back in 1982, she probably never expected that her experiments with the fast-breeding arthropods would throw into question some of the basic axioms of conservation biology. But her findings have done just that, and in the process have created a great deal of consternation among conservation biologists who adhere to traditional breeding techniques, particularly those trying to replenish dangerously low populations of endangered species.

Essentially, biologists have two options for bringing animals back from the brink of extinction. They can aim for the maximum number of offspring, or try to maximize genetic diversity: call it quantity versus quality. Usually biologists prefer quality, breeding the surviving adults as equally as possible, thus limiting the mating of prolific breeders-and thereby detrimental inbreeding-while allowing slow breeders to catch up and gain better representation among the progeny.

This strategy is based on the assumption that all the parents carry equally desirable genes and are equally deserving of representation. By preserving maximum genetic diversity in this way, breeders contend, the offspring will have the genes they need to cope with potential variations in future environments-say, changes in climate, prey behavior, or disease conditions. Overall, the goal is "to change the gene pool as little as possible" from that of the animals that were captured in the wild, says Jon Ballou, a conservation biologist who heads the captive-breeding program of golden lion tamarin monkeys at the National Zoo in Washington, D.C.

To ensure that the offspring best represent the entire population of adults, biologists such as Ballou typically use what's called a "pedigree" breeding program, which assigns breeding opportunities according to the relative rarity of one's offspring. The strategy ensures that all members of the "founder" generation have similar numbers of children, grandchildren, and great-grandchildren.

But could seeking quantity-the other breeding strategy-simultaneously improve quality as well? That's the implication of a series of experiments conducted by Meffert and Edwin Bryant, also a biology professor at the University of Houston, which have challenged the conventional wisdom of animal breeding. The researchers began thus by removing all but one or two pairs of randomly chosen males and females creating so-called "bottlenecks" in their housefly populations. To build up one population, they used a pedigree breeding strategy, but in another, they allowed the flies to breed at will.

Surprisingly, the pedigree technique favored by breeders of captive endangered species led to "nightmare population crashes" and lethargic flies that Meffert, with classic scientific drollery, says would be "selected against"-that is, eaten-in the wild. But when the scientists let nature take its course, leaving the males to compete for the opportunity to mate, the "superfly males," as Meffert calls them, bred with abandon, often with cousins and sisters (though not with mothers or daughters, since flies do not live long enough to mate with their offspring), and the offspring were much more vigorous.

Ballou of the National Zoo says that Meffert and Bryant's work is interesting, but he questions its relevance for captive breeding of animals for the wild. The fact that the offspring of the self-bred flies were more vigorous might be an artifact of an artificial breeding situation, he says, so what may seem like "letting nature takes its course" in captivity could be anything but. If certain parents produce more offspring, it could mean they are more fit to survive. But it could also mean that they are better suited to a captive environment and could be more vulnerable in the wild, he says. "We don't know enough about natural selection to impose our view of it."

Ballou points to another limitation on results from the Houston housefly experiments: they experienced much tighter bottlenecks than most endangered species undergo. Still, because the growing extinction crisis will put more and more animals ominously close to extinction, he concedes that it would be a good idea to test the Meffert-Bryant results with small vertebrates. Toward that end, Meffert is planning to conduct experiments with two endangered birds, the Micronesian kingfisher and Attwater's prairie chickens.

Another surprising Meffert-Bryant finding, which could bring breeders some solace, is that bottlenecks appear to be less damaging to genetic diversity than feared. These results come from tests involving so-called quantitative genetics. Unlike molecular biology, which can identify single genes, in quantitative genetics scientists use direct observation to examine traits that result from the interactions of many genes. Mating is one such trait, Meffert notes, because on the male side, for example, it requires genes that allow the fly to detect eligible females as well as to perform the mating dance and act.

A Good Word for Inbreeding?

Through such observations, Meffert and Bryant found a surprising rebound of genetic diversity-as measured by remarkable variation in mating behavior-in post-bottleneck flies. (The rapid but elaborate mating dance of the housefly is best appreciated in slow-motion video, Meffert says.) "It's an unexpected result," says Lukas Keller, an expert in the genetics of song sparrows at University of Wisconsin-Madison. Right now, he adds, most experts believe that "a highly inbred population, or one based on a few parents, should be written off-that it's doomed to extinction" because of a lack of genetic diversity.

Meffert argues instead that a bottleneck can be an opportunity for getting rid of undesirable genes. It gives a chance to "purge bad genes from the population," she says, since only the fittest animals get to breed. In other words, she says, uttering another heresy, "inbreeding may be useful."

Meffert does admit, however, that bottlenecks could also purge positive genes, and thus would have to be used cautiously as a captive-breeding technique. In fact, she notes that some human populations have experienced bottlenecks, typically when small populations move to new islands or remote regions. In such cases, she observes, "Either they all died, or they [inadvertently] cleaned up their genetics and came up with a solution that worked for them."

So how best to ensure the survival of endangered species? Is there a middle ground that maximizes the genetic representation of today's individuals among tomorrow's generations but that still exploits the counterintuitive findings that animals may know better than animal breeders? Though more work needs to be done to verify her results with other species, Meffert says that combining her techniques with traditional methods could give biologists a new tool for replenishing severely depleted populations of endangered species. For example, she says, biologists could separate fast breeders into one group, essentially creating an artificial bottleneck, and let them reproduce with abandon, without fearing a loss of critical genetic diversity. Meanwhile, for added assurance, they could try to coax the reluctant breeders to reproduce as well. Afterward, assuming offspring from both groups survived, she says, the biologists could choose the animals they believed were most suitable for reintroduction into the wild.