A Toxic Hand-Me-Down

Environmental contamination can cause cancer and birth defects. Of particular concern are a group of toxic chemicals called endocrine-disrupters, which interfere with reproductive hormones and may cause sterility. A new study, published online this week in the Proceedings of the National Academy of Sciences, suggests that these chemicals can change reproductive behavior as well, and that these behavioral changes can be passed on from parents to offspring. If correct, these changes could alter the course of evolution by giving natural selection new targets to act on.

In 2005, a team led by reproductive biologist Michael Skinner of Washington State University in Pullman reported in Science that the fungicide vinclozolin, an endocrine-disrupter used to spray vineyards and other crops, causes fertility defects in the male offspring of female rats treated with the chemical. These defects are, in turn, passed down to the males of subsequent generations. The toxin did not appear to be altering gene sequences; instead, Skinner and colleagues found, vinclozolin was somehow causing other chemical groups to latch onto certain genes, changing their expression (Science, 3 June 2005, p. 1391). The phenomenon is known as epigenetic inheritance. Last year, Skinner's group identified 15 epigenetically altered DNA sequences in the sperm of the vinclozolin-treated rats.

To see whether these changes led to differences in mating behavior, Skinner's group, together with a team from the University of Texas in Austin co-led by David Crews and Andrea Gore, conducted tests to determine how attractive the male descendants of vinclozolin-treated rats were to females. The researchers used rats from the third generation after the initial chemical exposure. In one experiment, a female was placed in the center of a three-chambered glass cage, while a male rat was put at each end of the cage behind a wire mesh screen. Attractiveness was measured by how long the female spent in each chamber, as well as how much time she spent engaged in behaviors such as touching noses with the male rat and sniffing in his direction. In another experiment, the researchers put wooden beads in the cages with the male rats to absorb their odors, and then measured how much time female rats spent sniffing the beads when they were exposed to them.

All of the females tested strongly preferred males from control lineages that had not been treated with vinclozolin over the male descendants of vinclozolin-treated rats, even after three generations. The team concluded that these epigenetic effects can impact the attractiveness of later generations. The disruption may even influence the evolution of a species by making some individuals more reproductively fit than others.

The study "adds to the mounting evidence that many pesticides and other chemical pollutants in our environment have harmful effects on mammalian behavior as well as physiology and development," says biologist Sarah Zala of the Konrad Lorenz Institute for Ethology in Vienna, Austria. But Emma Whitelaw of the Queensland Institute of Medical Research in Brisbane, Australia, cautions that the jury is still out on whether endocrine-disrupters are acting through epigenetic mechanisms. "Their evidence that the transgenerational effects are solely the result of epigenetic and not genetic changes remains unconvincing," she says.

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