Half the man his grandfather was

Posted 7 June 2012 by Matt Young

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 [1]. 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. Reference. [1] 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.

21 Comments

John_S · 7 June 2012

“Every man sitting in this room today is half the man his grandfather was!”

Your grandfather may have had 200 million more bullets, but it still only takes one :-)

ianfmusgrave · 7 June 2012

The whole "male fertility declining" idea is a lot more controversial than this article makes it appear. The original analyses have several issues with a range of potential confounders:
see
http://www.biomedcentral.com/1471-2458/10/24
http://www.ncbi.nlm.nih.gov/pubmed/9418697

And while intersex effects are clearly seen in relatively polluted areas, like the alligators of Florida’s Lake Apopka, the levels of consumption with things like BPA are unlikely to cause any harm in humans. To comsume the amount of tinned soup necessary to reach the mandated safe threshold exposure to BPA from tin linings (which is itself 1000 times lower than the dose that causes no effects in animal models, you would be required to drink 100 tins of canned soup a day.
https://theconversation.edu.au/should-the-latest-research-about-plastics-exposure-worry-us-6922

Chris Lawson · 8 June 2012

Actually, genetically speaking I'm 1/4 the man my grandfather was...

Chris Lawson · 8 June 2012

I was so intrigued by the statement that Sarnia has a male:female birth ratio of 50:100 that I decided to track down the paper in question. I found it here: Mackenzie, 2005, and the full text is free online.

This is not a very convincing paper. It is not the authors' fault that the records they assessed only existed from 1984-2003, but they draw a very large conclusion from very small numbers (around 35 births per year in a community of 850 Chippewas over only 20 years). Also, the male:female birth ratio was *above* national averages in some years (albeit non-significantly). Certainly there is no reason to think Sarnia abruptly became more polluted in 1992-93, which is when the observed trend suddenly changed. I also note that there should now be 8 more years of data, which to my knowledge has not been reported.

Finally, the total population of the Sarnia district is around 90,000. I would have expected that anyone trying to establish a link between pollution and sex ratios would have used the larger, and therefore more statistically robust, total population. I can understand why they chose the small Chippewa population (because the Chippewas were worried about an apparent lack of young male softball teams and asked the govt to look into it) -- but this is most certainly not the same thing as saying that this birth ratio was reflective of the population of Sarnia as a whole. In fact, over the same time period, the male:female birth ratio for the Sarnia region was 103:100.

I'm absolutely not dismissing the possible link between feminising pollutants and human health, but this is not a good paper to hang it on.

fnxtr · 8 June 2012

Heh. You want men to take action, threaten their masculinity. Works every time. :-)

Frank J · 8 June 2012

Chris Lawson said: Actually, genetically speaking I'm 1/4 the man my grandfather was...

You only had one grandfather? Well that disproves "Darwinism." ;-)

Paul Burnett · 8 June 2012

Frank J said: You only had one grandfather? Well that disproves "Darwinism." ;-)

Not necessarily...it is entirely possible to have only one grandfather. That is just one of the many surprises that can be discovered when doing genealogical research. In fact, all of Adam and Eve's grandchildren had only one grandfather - right, Byers?

Frank J · 8 June 2012

Not necessarily…it is entirely possible to have only one grandfather.
— Paul Burnert

Impossible. You have 4 grandparents, 8 great-grandparents, etc. Go back 300 generations (and there must have been at least 2 x 10^90 people around. And many more than that for the OECs who think our "kind" has been around for 1000s of generations. (and yes, I like to tease the math-challenged with that).

John_S · 8 June 2012

Frank J said:
Not necessarily…it is entirely possible to have only one grandfather.
— Paul Burnert
Impossible. You have 4 grandparents, 8 great-grandparents, etc. Go back 300 generations (and there must have been at least 2 x 10^90 people around. And many more than that for the OECs who think our "kind" has been around for 1000s of generations. (and yes, I like to tease the math-challenged with that).

You missed Paul's dig. It's possible that your one grandfather got it on with both your grandmothers and that your father and mother were half-siblings :-0 Actually, I'd be amazed if this hasn't happened somewhere in the world fairly often. Go back 300 generations and crossed ancestry like this is almost a certainty, especially in fairly closed societies.

Dave Luckett · 8 June 2012

Ancient north Queensland joke. "What can you expect? His father and both his grandfathers were the same bloke."

harold · 9 June 2012

John_S said:
Frank J said:
Not necessarily…it is entirely possible to have only one grandfather.
— Paul Burnert
Impossible. You have 4 grandparents, 8 great-grandparents, etc. Go back 300 generations (and there must have been at least 2 x 10^90 people around. And many more than that for the OECs who think our "kind" has been around for 1000s of generations. (and yes, I like to tease the math-challenged with that).
You missed Paul's dig. It's possible that your one grandfather got it on with both your grandmothers and that your father and mother were half-siblings :-0 Actually, I'd be amazed if this hasn't happened somewhere in the world fairly often. Go back 300 generations and crossed ancestry like this is almost a certainty, especially in fairly closed societies.

Frank is kidding, but of course, but having one grandfather either because of founder effect or inbreeding has not been that terribly unusual throughout human history. Back on the topic - I'm not aware of strong evidence that general population sperm counts are decreasing. I looked for some and didn't find any strong studies addressing the general human population of the US (provide links or citations if I am wrong). The probable reason I could not find this is that male semen/sperm quality is rarely a subject of public health research. Our direct information about human male reproductive health comes mainly from the fertility medicine or urology communities. Having said that, both men and women in the US are currently experiencing a significant environment-induced but poorly understood health issue - obesity. There is almost no question that the current obesity rate is due to change in environmental factors; the rate has increased far too rapidly to be due to any type of change in allele frequencies. (Prior to that, as another example of how environmental conditions can have dramatic impact, the human population of the US experienced a high rate of certain health problems due to a different, somewhat transient environmental issue - an extremely high rate of cigarette smoking.) Among other things, it's conceivable that greatly increased mean level of body fat could be related to a population mean decrease in male fertility, or at least male semen/sperm quality. There could be an underlying third factor that is a risk factor for both. Or to some degree, and excessively fat body habitus could itself have an impact on reproductive health. Or both.

Ron Okimoto · 9 June 2012

Frank J said:
Chris Lawson said: Actually, genetically speaking I'm 1/4 the man my grandfather was...
You only had one grandfather? Well that disproves "Darwinism." ;-)

He could have only one Grandfather, but his parents would have to be sibs. Then he would be half the man his grandfather was.

SensuousCurmudgeon · 9 June 2012

Dave Luckett said: Ancient north Queensland joke. "What can you expect? His father and both his grandfathers were the same bloke."

That's good. My friend, John, had a knotted family tree. His grandfather married his deceased wife's sister, and he had kids by both of them. Those kids were either full or half siblings, and (in a way) were also their mother's nieces and nephews. In the next generation, their kids were closer than cousins. They were actually half-cousins. John's father was his (second) grandmother's nephew, but that was the only grandmother John ever knew. In a way, because his father was the son of her nephew, John was thus his own cousin.

Henry J · 9 June 2012

Having said that, both men and women in the US are currently experiencing a significant environment-induced but poorly understood health issue - obesity. There is almost no question that the current obesity rate is due to change in environmental factors; the rate has increased far too rapidly to be due to any type of change in allele frequencies.

Could it be related to the larger fraction of jobs in which most time is spent sitting at a desk?

harold · 10 June 2012

Henry J said:
Having said that, both men and women in the US are currently experiencing a significant environment-induced but poorly understood health issue - obesity. There is almost no question that the current obesity rate is due to change in environmental factors; the rate has increased far too rapidly to be due to any type of change in allele frequencies.
Could it be related to the larger fraction of jobs in which most time is spent sitting at a desk?

That's a good question. When I first started hearing about the issue, in the 1990's (around the same time I became aware of political creationism), I thought reduced activity was a no-brainer explanation. After all, as recently as the seventies, children used play outdoors all day, people used to walk a lot more, more people used to be active in spare time, more people had jobs at least as active as assembly line work, etc. However, no, there has also been a substantial increase in calorie consumption according to the USDA; in fact, studies seem to suggest that activity hasn't gone down that much in adults (because they mainly weren't that active before), and eating more food is the issue. Incidentally, another sometimes proposed partial explanation is smoking cessation. It's probably true that many adults were mildly thinner than they would otherwise have been during the 1950's and 1960's because of the high rate of cigarette smoking. But that doesn't explain all of adult obesity, and doesn't explain increased childhood obesity at all. I remind everyone that food calories are stated based on completely oxydizing food in a bomb calorimeter, including the oxydization of all amino acids rather any incorporation of any into proteins, at very high efficiency, and merely provide an estimate of the relative energy contents in foods available to humans. Likewise, estimates of how many food calories activities "burn" are very approximate and relative; they are based on observational studies of how many calories normal weight people with varying levels of daily activity ate, done decades ago. However, this body of work has proved surprisingly useful. Nevertheless, we are left with the confusing question of why people voluntarily consume more food, while simultaneously not exercising any more (maybe exercising less), and why this trend is so strongly associated with income level. Possible partial explanations include - marketing of new food types and portion sizes (far more chain fast food, chip-type snack food, giant-sized sodas, etc, everywhere), new food economics (fast food, junk food, and snack calories getting cheaper than low cost traditional meal calories), widespread sleep deprivation (known to provoke body fat gain), a nihilistic or defeated attitude in the face of constant confusing claims about diet (in particular, even when proposed dietary regimes actually are healthy, they are often posed to compete with other equally healthy recommendations, and often take a perfectionistic stance, "do it perfectly or don't even bother", an attitude also frequently seen attached to exercise recommendations), widespread unrealistic claims that fat can be rapidly shed, and one I think is very likely to play a role, breakdown of the tradition of eating together with other humans at regular times. And yes, chemical pollutants could conceivably play a role; there's not necessarily much need to invoke this idea, but maybe compounds in plastic packaging could stimulate appetite or some such thing. But the reason I bring this up here is that if there is a trend of reduced male fertility - and as I said, that's nowhere near as clear - not only does the increase in obesity provide a model of how dramatic environmental influences can be, even if they are gradual and subtle, but excess body fat itself might partly explain an estrogenic effect in men.

surprisesaplenty · 10 June 2012

Other commenters, please correct me: I am not trying to be racist but I am basing the opinion below on 'common knowledge' that I feel is or was part of my upbringing.

@ Chris Lawson: I don't know but I suspect the Native American group was described in the study because they eat more fish than the more diverse Sarnia population.

I read Our Stolen Future about 15 years ago and it discusses similar problems, focusing on the Great Lakes.
http://www.amazon.com/Our-Stolen-Future-Threatening-Intelligence/dp/0452274141/ref=sr_1_1?ie=UTF8&qid=1339366414&sr=8-1&keywords=our+stolen+future

Chris Lawson · 11 June 2012

surprisesaplenty said: @ Chris Lawson: I don't know but I suspect the Native American group was described in the study because they eat more fish than the more diverse Sarnia population.

From the original paper: "Members of the Aamjiwnaang First Nation community near Sarnia, Ontario, Canada, voiced concerns that there appeared to be fewer male children in their community in recent years. In response to these concerns, we assessed the sex ratio (proportion of male births) of the Aamjiwnaang First Nation..."

eric · 11 June 2012

Chris Lawson - thanks for your response, I also had a very eyebrow-raising moment when I read that 50:100 figure. A smaller decrease I would've believed (was due to pollution, without any further evidence). But that is so big that, IMO, statistical shennanigans becomes a far more likely explanation. And bang, there's your post, identifying that this ratio occurred in a single sub-population in that region. Which makes it sound like someone drew the bullseye after they shot the arrow.

Still, even if the effect is smaller than reported, I pretty much agree with fnxtr's political point: so long as our country is ruled by rich men, stressing pollution's effect on male gonads may be one of the few conservation arguments that actually work.

Frank J · 11 June 2012

I don't see what all the fuss is about. Just do what millions of people have been demanding for decades. Just get rid of "chemicals." Start with this nasty stuff.

BTW, I know I have been fighting a futile battle with the word "creationism" and its variants, but I'm even more militant when it comes to "chemical." If it were up to me, the word would never be used as a noun, and only sparingly as an adjective.

Chris Lawson · 11 June 2012

Eric,

I'm all in favour of robust political action to reduce pollution, but I think it's critical that we use the best evidence available. Dressing up unimpressive papers has an awful tendency to backfire and it turns a battle for best practice into a battle for political spin (and in a fight between dishonest bastards, the richer, more powerful bastard will generally win). Even if it helps the battle at hand, say reducing pollution in Sarnia, it can have unexpected knock-on effects, say increasing unwarranted fear of chemicals and feeding anti-vaccination rhetoric, or closing down chemical plants with good waste and safety practices along with the cowboy operators.

Matt Young · 21 June 2012

Comment by the author, Yan Linhart: Several comments express doubts about whether the declines in male fertility and sex ratio are real, and provide some references to support their skepticism. In fact there is plentiful evidence to indicate that there is reason for concern on both fronts. For example, the breezy comment about the need to consume 100 tins of canned soup a day to be exposed to meaningful levels of BPA is countered by several recent papers. Thus, a bisphenol A expert panel provided the following consensus statement:

The published scientific literature on human and animal exposure to low doses of BPA in relation to in vitro mechanistic studies reveals that human exposure to BPA is within the range that is predicted to be biologically active in over 95% of people sampled. [Various studies show a] wide range of adverse effects of low doses of BPA.

In addition, a second panel involving a combination of personnel from the FAO and WHO noted that three epidemiological studies investigated the association of urinary BPA concentrations with semen quality. All three studies, although of relatively modest sample size (ranging from 190 to 302 men), reported associations of increased urinary BPA concentration with one or more measures of reduced semen quality. Other recent (2012) studies also report declines in semen quality in developed countries; see here and here. As for the issue of declining sex ratios, yes, the Sarnia study involves a small data set, but as noted in my original article, similar patterns are detectable in other countries including the Netherlands, Denmark, the United States, Japan and elsewhere. For that reason, a recent review states that

The similarity of the findings [of studies done at different scales] shows the need to undertake calculations of sex ratio at scales from the local to the regional, national and international levels. The findings also indicate that less-conventional sources of data may be useful to document a local phenomenon. Different kinds of epidemiologists may be needed for each scale. At the regional and larger scales, trained epidemiologists are required for accessing massive databases and for undertaking calculations.

The new references I cite here are a sampling of what is available. It seems that these changes are real, and invoking, as some comments do, “statistical shenanigans” and the “dressing up of unimpressive papers” does not make these patterns go away. The interested reader can also consult the research of Louis J. Guillette Jr. and David O. Norris to explore some of the broader aspects of these issues. Finally, one reason for bringing up these patterns is the hope that some young researcher in search of a hot topic will follow up on these data. And I agree that a good place to start would be a detailed analysis of sex ratios in the population of the Sarnia area. A second reason is that, like so many other complex topics in science, we always need more and better evidence, but I hope that we can agree that the next generation should not incur the cost of providing such evidence if we can start paying attention now.