By Yan Linhart, Professor Emeritus of Ecology and Evolutionary Biology, University of Colorado at Boulder
Lou Guillette, an expert on sexual development, explained to a congressional committee in 1993 that sperm counts have been decreasing for decades and warned the congressmen, “Every man sitting in this room today is half the man his grandfather was!” Since Guillette’s testimony, we have learned further that the sex ratios of newborn babies are changing in some industrialized regions: the proportion of newborn males to females is decreasing.
These dramatic changes are associated with our increasing exposure to multiple chemicals and may shape our evolution as a species. Gender-bending chemicals affect some individuals more than others and some populations more than others. In addition, they can reduce the frequency of fertile males in populations of humans and wildlife.
Some time after Guillette’s testimony, writer Deborah Cadbury provided similar admonitions in her book The Feminization of Nature. Cadbury describes a world in which males are scarce to nonexistent, so that the basic concept of “the human condition” takes on a whole new meaning. Such extreme predictions may not come to pass, but the declines in frequency, fertility, and general health of males in numerous species are undeniable, and such declines will be especially severe in populations exposed to intense chemical pollution.
The pollutants responsible for the changes are found in products we use daily. These chemicals end up in soils, rivers, and lakes. Indeed, Guillette had his “eureka” moment in a lake in Florida, while he was studying alligators. Many of the gators in Florida’s Lake Apopka had deformed genitals, and Guillette wondered whether the deformities had anything to do with rising levels of pollution. Discussions with colleagues and some chemical sleuthing led to the finding that Lake Apopka was full of toxins, such as organochlorine pesticides (including breakdown products of the banned pesticide DDT) and heavy metals. These toxins have endocrine-disrupting properties, meaning that they mimic the hormone estradiol (a feminizing hormone) and inhibit the actions of testosterone (a masculinizing hormone). The gators spent their lives in a hormone soup that altered their development. Guillette’s research, which indicated that similar defects were found in other animal species, eventually led to his being invited to speak to the U.S. Congress.
Some time later, a team led by David Norris of the University of Colorado, one of Guillette’s mentors, noticed abnormalities in fish downstream from the city of Boulder. In studies conducted over several years, they observed that specimens below the Boulder Waste Water Treatment Plant showed “gonadal intersex, altered sex ratios, reduced gonad size, disrupted ovarian and testicular histopathology, and vitellogenin induction consistent with exposure to estrogenic wastewater contaminants” compared to those upstream. Vitellogenin is a protein involved in egg yolk production and is not found in normal males. In addition, the downstream fish showed a female-biased sex ratio at the effluent site .
These abnormalities reflect the presence of a diversity of chemicals detected by very precise analyses of the water. Many of these chemicals involve pollutants including pesticides and household products such as bisphenyl A (BPA), which is used in polycarbonate plastics, resins lining food and beverage cans, thermal inks, and other products. These compounds mimic female hormones. Hormones from ingested birth control pills also get into water supplies. Subsequent tests by Norris and his collaborators showed that exposing fish to wastewater effluents produce those changes. Mind you, these pollutants are in the water of Boulder, Colorado, one of the greenest and most environmentally conscious towns in North America, where everybody is pathologically healthy and would never consider dumping chemicals into a sink. The good news is that such pollution and its impacts are reversible. In a recent paper, Norris and his collaborators have found that a serious upgrade of the treatment plant has improved the efficiency of removal of many endocrine-disrupting chemicals. As a result, fish exposed to the cleaner water showed less endocrine disruption.
These observations indicate that we need to reduce our exposure to this cocktail of sex-changing products. If we do not, the results are predictable. In fact we have already run that experiment on ourselves several times. Humans show patterns similar to those in other animals. Our development has gone awry, as we exhibit increased incidences of abnormal genitalia, decreases in testosterone in adult men, reduced fertility, increased cancer rates, and changes in sex ratios of newborns.
An unfortunate case study is provided by Sarnia, Ontario, where there is an impressive concentration of Canadian and international petrochemical companies, including Dow, Shell, and Imperial Oil. Currently, there are about 60 large industrial plants on the Canadian side and another dozen or more on the U.S. side. As a result, the region has been nicknamed “chemical valley.” Residents have been exposed to these chemicals for the past forty years; if this valley were near a major urban area like New York or Tokyo, we would all have heard about it. However, it is tucked into a small corner of Canadian tribal lands, so it has produced only a small blip on the radar screen of most watchers of public health.
The Canadian National Pollutant Release Inventory for 2005 showed that in that year alone 131 million kilograms of demonstrably toxic air pollutants were disgorged by these companies, which works out to about 1,800 kg per resident. Since then, little has changed, according to Jim Brophy, a health researcher who runs the local occupational health clinic. As a result, a recent World Health Organization survey has identified Sarnia as the most polluted city in Canada.
The normal sex ratio in human populations is about 105 newborn boys for every 100 girls. In this valley, the sex ratio of newborns is an astonishing 50 boys for every 100 girls. Although this deviation from the normal sex ratio is most extreme in Sarnia, gradual declines in frequencies of males have also been noted in other industrialized countries, including populations monitored in Europe, Japan, Taiwan, and North America.
These skewed sex ratios represent a fundamental change in the biological organization of our species. The pollutants are associated with a dramatic reduction in either the production or the survival to term of male embryos. To date, no specific cause for these changes has been established; however, the fact that it is detectable in several populations is a powerful alarm call. Our environments are changing, and these changes have genetic and evolutionary consequences.
Males thus have an unexpected - and unwelcome - role to play in public health: We are canaries in a coal mine for a problematic experiment, which shows no signs of ending soon. For example, in late March 2012, the FDA declined to ban BPA in food packaging because it maintains that there is not enough evidence to show that BPA is harmful to humans, even though its estrogen-mimicking properties have been known since the 1930’s.
When Professor Guillette testified before the congressional committee, the second part of his statement was a question: “Are our children going to be half the men we were?” What he was trying to warn us about almost twenty years ago was the possibility that, if our exposure to chemicals remains at current rates, we may well be heading toward a very different world. We have not heeded the warnings, and the experiment continues.
 Vajda, Alan M., Barber, Larry B., Gray, James L., Lopez, Elena M., Woodling, John D., and Norris, David O. 2008. Reproductive Disruption in Fish Downstream from an Estrogenic Wastewater Effluent. Environmental Science and Technology, vol. 42, pp. 3407-3414.