AbstractHealth concerns about the long-term effects of endocrine disrupting chemicals (EDCs) often fail to reflect a sophisticated understanding of evolutionary theory or how a population will be affected by a selective pressure, even when that pressure arises from human action in the environment. Using niche construction theory, this article for a general audience seeks to explore how endocrine disruption might affect our species. The evidence suggests that EDCs may very well exert a selective influence by disrupting fertility, especially because a large number of EDCs seem to interact and target the same mechanisms. However, niche construction theory highlights the degree to which some of those changes will be reversible types of phenotypic bias and how EDC-resistance is also likely to be the outcome of niche-drive selection.
An Italian study in 2012 found that men’s penises were growing smaller over time — two centimetres lost from grandfather to grandson in the twentieth century. Conservative radio bloviator Rush Limbaugh knew who to blame: ‘feminazis, the chickification, and everything else’ linked to feminism. Other commentators, a bit more scientific, pointed the finger at endocrine disrupting chemicals, such as pesticides and hormones fed to cattle, as likely culprits.
For example, Bucky McMahon at Medium pinned the blame squarely on plastics, offering that ‘virtually all commercially available plastics leach synthetic estrogens,’ implying that plastics are behind the (allegedly) lost penis stature. According to McMahon, plastic-derived xenoestrogens, chemicals that mimic the effects of estrogen, are also responsible for a fall off in the sperm count in men, first reported in 1992 British Medical Journal paper written by a Danish team led by Elisabeth Carlsen (Carlsen E. 1992); see also (Le Moal J. 2014) for more recent review; and (Sharpe 2003).
Some observers argue that the same culprit leads to an opposite trend among women. In 1997, a paper by Marcia Herman-Giddens and colleagues in Pediatrics reported that girls in the United States developed breasts earlier than previously thought: their findings suggested that Euro-American girls were, on average, experiencing the onset of puberty before 10 years of age, and African-American girls, on average, before the age of 9 (Herman-Giddens M.E. 1997). A ‘new normal’ was a more precocious onset of female sexual maturity, in some cases long before the girls were emotionally ready. As Dr. Glenn Braunstein wrote for the Huffington post: ‘childhood for girls is shrinking, while the duration of puberty is expanding.’
The potential causes of early onset for puberty in girls include xenoestrogens, but also obesity and higher childhood body weight, an imbalance between high-energy diet and lower levels of activity, the consumption of sugary soft drinks, even sexual abuse or other severe life stress.
Although all of these findings are controversial — other studies find no decrease in sperm count or penis size, for example (Bergman A 2012) — the worst-case scenario is grim, indeed. McMahon predicts a sad end to our species, driven to sexual dysfunction and the brink of extinction by plastics messing with our hormones:
In the endgame, we’ll be a race of sexed-up tweener girls and sterile dudes with little dicks wandering baffled through a rubbish-filled world. Then those poor mismatched souls will grow old and die. End of story.
Setting aside the question of whether plastics (or obesity or carbonated corn syrup-laced beverages or the presence of step-dads or hormones in beef or any other factor) are behind changes in our patterns of sexual maturity, what about the possible future? Does evolutionary theory support the idea that xenoestrogens and other endocrine disruption could lead us limping to a kind of slow rolling human apocalypse, as people like McMahon suggest?
If xenoestrogens really are a threat to humanity, what would they do to our species? Will plastics lead to the sort of future imagined in America 3000, women (with surprisingly large bosoms and blow-dried hair) dominating men, who are reduced to enslaved ‘seeders’ (presumably those select few with willies still adequate to the task)? Or will it be more like Children of Men, in which mass infertility breaks humanity’s spirit and causes widespread social collapse?
To anticipate how xenoestrogens or any other synthetic chemical that influences fertility might affect human evolution, it helps to consider niche construction theory.
Niche construction theory
In 1881, just before he died, Charles Darwin published his last book: The Formation of Vegetable Mould, Through the Action of Worms. The subject may appear to be an odd choice (although the book sold quite well).
The reason for Darwin’s interest in the humble insect is that earthworms fundamentally change the environment in which they live, or else they simply couldn’t survive on land.
Earthworms are closely related to species living in fresh water, and it shows in a range of ways, including their excessive urine (see Laland and Sterelny 2006). Like a freshwater species, they’re inefficient users of water and could easily dehydrate without topsoil. The terrestrial earthworm can only survive in topsoil — not clay or sand — because their predecessors have made topsoil into a kind of accessory kidney. Generations upon generations of earthworms drag vegetable matter into clay and sand and then mulch the mix by eating and excreting it as worm castings; they also shed mucus and eliminate calcite from the soil. The result is that earthworm-pooped-out topsoil is a perfect milieu for earthworms, buffering their peculiar anatomy against the demands of life on land.
The way that earthworms construct topsoil is a signature example used by proponents of Niche Construction Theory (NCT). Niche Construction Theory is a movement in contemporary evolutionary thinking that seeks to describe how organisms — humans included — can so influence the environment around themselves that selective pressures are changed on future generations.
Standard Evolutionary Theory (SET) tends to treat the environment and organism as separate; NCT points out that the two are linked and affect each other over evolutionary time. In addition, in SET the environment is really treated as the actor, shaping species through natural selection. As Kevin Laland and colleagues wrote in a 2014 opinion piece in Nature, Standard Evolutionary Theory:
…treats the environment as a ‘background condition’, which may trigger or modify selection, but is not itself part of the evolutionary process. It does not differentiate between how termites become adapted to mounds that they construct and, say, how organisms adapt to volcanic eruptions. We view these cases as fundamentally different.
Volcanic eruptions are idiosyncratic events, independent of organisms’ actions. By contrast, termites construct and regulate their homes in a repeatable, directional manner that is shaped by past selection and that instigates future selection. Similarly, mammals, birds and insects defend, maintain and improve their nests — adaptive responses to nest building that have evolved again and again. This ‘niche construction’, like developmental bias, means that organisms co-direct their own evolution by systematically changing environments and thereby biasing selection. (Laland K. 2014)
In their programmatic book, Niche Construction: The Neglected Process in Evolution, Odling-Smee and colleagues write, niche construction is ‘the process whereby organisms, through their metabolism, their activities and their choices, modify their own and/or each other’s niches’ (Odling-Smee 2003): 419). Proponents cite examples like termite mounds, beaver dams, bowerbird nest building, and even the way cyanobacteria or ‘blue-green algae’ brought on the Great Oxidation Event, the catastrophic transformation of Earth’s atmosphere about 2.45 billion years ago which paved the way for all oxygen-dependent life as we know it.
These organisms substantially alter the environment, but clearly, humans are ‘niche constructors’ of a different order and versatility. Geographer Yi-Fu Tuan puts it much more poetically:
A human being is an animal who is congenially indisposed to accept reality as it is. Humans not only submit and adapt; they transform in accordance with a preconceived plan. That is, before transforming, they do something extraordinary; namely, ‘see’ what is not there. Seeing what is not there lies at the foundation of all human culture. (Tuan 1998):6)
Neo-Darwinism and its gaps
In 1896, George John Romanes first used the term ‘neodarwinism’ to describe the theory of August Weismann. Weismann emphasized that germ-line genetic material – the material passed on to one’s off-spring in sperm or egg – was immune to organic change during the lifetime. Every organism was born with the biological material that they would pass on to the next generation already in place, immutable. Nothing that happened during the lifespan of an individual organism mattered to evolution except reproduction (or failure to reproduce). Variation only happened through mutation (or unpredictable changes in gene replication) or recombination, the mix of parental genetic material that happens due to sexual reproduction.
Weismann’s approach emphatically rejected Lamarckian evolutionary dynamics, or the idea that traits acquired during an organism’s lifetime could be inherited, which Darwin himself had said was entirely possible. Weismann and other ‘neodarwinists’ also rejected the ideas of ‘saltationists’ (those who believed evolution happened by ‘jumps’) and ‘orthogenecists’ (those who argued for progress in evolution or a form of teleology). For all these reasons, ‘neodarwinism’ was a crucial intellectual leap, one that cleared away a lot of intellectual detritus held over from pre-Darwinian ways of thinking about species change.
Today, the term ‘Neo-Darwinist’ has a modified meaning, but it still refers to a particular synthesis of Darwin’s theory of Natural Selection with population genetics (although people like Ernst Mayr argue ‘Neo-Darwinist’ is a misnomer, preferring ‘modern synthesis’). A simple Neo-Darwinist definition of evolution, for example, is change in gene frequencies in a species over time due to natural selection. The approach highlights that evolution is not change in the individual organism during a single lifetime, but change in the species’ gene pool over time.
Critics argue that ‘Neo-Darwinism’ can be overly focused on genetic transmission and natural selection to the exclusion of other processes, including not just niche construction, but also phenotypic plasticity (the way an individual organism adapts during its lifetime), inclusive inheritance (biological material in addition to DNA transmitted to offspring, such as in epigenetics), and developmental bias (the way that patterns of organism development constrain variation) (see (Laland K. 2014) for a short but comprehensive discussion, or an interview with Denis Noble).
One way to simplify what’s already a simplification it is to say that extreme Neo-Darwinism focuses only on differential gene transmission, treating organisms as survival machines for passing on genes. Like any other radical theoretical reduction, it’s a powerful reorientation of how we think, but it leaves a lot of intellectual casualties on the cutting room floor. But it holds up change in a species’ gene pool over generations as the only real form of evolution.
Niche construction: agriculture, for example…
Ironically, the desire among proponents of NCT to demonstrate the evolutionary potency of niche construction leads them to focus primarily on examples where an altered niche can be shown to affect the gene frequencies in a population. That is, the desire to pass this Neo-Darwinist litmus test — to show that niche construction can be so potent as a selective pressure that it affects gene frequency at the population level — is a bias that leads to discussing only the most long-term, severe, and sustained environmental alterations because they leave distinctive genetic fingerprints.
For this reason, most of the examples used in accounts of NCT are drawn from the history of agriculture (although language and tool-use are also sufficiently long-term cultural innovations to potentially qualify – and I try to argue in a paper under review that cities count as well).
Certainly, agriculture and the domestication of animals have had a significant impact geologically and ecologically on the planet. Agriculture has led to the modification of approximately three-quarters of the planet’s land surface.
Examples often discussed in NCT include:
§ Co-evolution between dairy farming and mutations of the LP allele linked to lactase persistence in adult humans (Gerbault P. 2011); see also (Bersaglieri T. 2004); (Durham 1991); (Holden 2009); (Simoons 1970).
§ Domesticated rice affected the copy number of gene AMY1, which offered a selective advantage to individuals possessing salivary amylase, the enzyme responsible for breaking down starch into more simple, digestible sugars (Laland K. 2014) (Perry G.H. 2007).
§ The link between yam cultivation, irrigation and forest clearing, increased prevalence of mosquitos as a vector for malaria transmission, and selective pressures favouring the HbS allele or sickle-cell genes (Durham 1991); (O’Brien 2012).
In all of these cases, researchers have drawn compelling links between human-altered environments or technologies and a genetic pattern in the populations with that cultural institution. All three cases — lactase, salivary amylase and malaria resistance — demonstrate the genetic consequences of a cultural innovation. All pass the Neo-Darwinist litmus test, with fairly clear relations between human-altered environment and increased frequency of a particular genetic variant in our species.
Niche construction, in these cases, works through the same mechanisms as natural selection: differential reproductive success leads to a change, over time, in the underlying genetic variation in a species. In a sense, these cases break down the distinction between natural and artificial selection because they all involve a complicated mix of human and non-human causes. They are all really astonishing bits of research, but they don't really tell us whether plastic will give men tiny penises or turn women into 'sexed-up tweeners' at an earlier and earlier age...
Endocrine disruption and the Neo-Darwinist litmus test
Could endocrine disrupting chemicals be affecting our species’ evolution? The short answer is, yes. EDCs and some other pollutants affect reproduction directly in lab animals and wildlife, and similar patterns of changing fertility do seem to be happening in humans, although the data is controversial (see Marques-Pinto and Carvalho, 2013, for an open access review).
Grindler and colleagues (2015) reported in detail in PLOS One, for example, on correlations between early onset of menopause and the presence of fifteen chemicals known to be endocrine disrupting. Early menopause might impinge especially strongly upon reproduction rates in the wealthiest societies because social factors push back the start of women’s reproductive careers. If you don’t start reproducing until late, menopause can become a limit on your rate of reproduction, affect which genes stay in the gene pool in subsequent generations.
Grindler’s team drew on the National Health and Nutrition Examination Survey (NHANES), a survey of the health and nutritional status in the US administered by Centers for Disease Control and Prevention. Using data back to 1999, they wound up with a total of 1442 women who had gone through menopause and had comprehensive examinations for EDCs from either blood serum or urine tests.
They checked for 111 chemicals known to disrupt hormone activity: these included dioxins or furans (the byproducts of combustion), PCBs (polychlorinated biphenyls, used as coolants but now widely banned), phthalates (plasticizers), phytoestrogens (plant-derived estrogens, like those in soy), phenols (industrial pollutants), pesticides, PAHs (polycyclic aromatic hydrocarbons, also a product of combustion), flame retardants (used widely in clothing and home furnishings), and surfactants (some detergents and emulsifiers) (ibid.).
The women with the highest levels of EDCs in their bodies were likely to go through menopause up to four years before those with lower levels. The causal relationship between early onset of menopause and EDCs is hard to track, not only because the study is correlational – there’s no way to run a controlled trial – but also because these chemicals appear to interact with each other.
The bottom line is that, if EDCs lead to premature menopause, then they certainly would affect human reproductive success. Worldwide estimates of infertility vary, but one fairly well argued case puts it at 9% (Marques-Pinto 2013): 2:15). The same could be said about EDCs and male infertility; xenoestrogens are frequently cited as a potential culprit in lower-than-viable sperm concentrations and the broader problem of 'testicular dysgenesis syndrome' (Sharpe 2003); see also (Bergman A 2012).
However, if the pattern is simply that ‘more EDCs cause earlier menopause,’ then arguably, EDCs would not constitute a directional pressure on human evolution. If they affect everyone equally when they are exposed, EDCs could reduce the overall human population without affecting the genetic profile of our species in any consistent way. That is, there might be fewer humans, but no selection to that process.
If the effects were merely proportional to exposure, then EDCs would constitute a population ‘bottleneck’ in evolutionary terms. EDCs would fail to pass the ‘Neo-Darwinist litmus test’ as a way in which niche construction affected human evolution.
Are we all equally susceptible to EDCs?
Because of the diversity of EDCs and the multiple mechanisms through which they can impinge on human reproduction, there’s no simple story to tell (see also McLachlan 2001). However, the evidence suggests that all individuals are not equally susceptible.
A Japanese research team led by Masanori Watanabe investigated the relationship between congenital abnormalities in boys’ reproductive organs and variants in the gene for estrogen receptors. They anticipated that variable sensitivity to estrogen might explain why some boys were affected by EDCs in utero, especially important given controversial research suggesting an increased incidence of genital abnormalities in Japan (Watanabe 2007). In particular, Watanabe's team looked at patients with hypospadias, micropenis or spermatogenic failure, to see if these boys also had a gene polymorphism that had already been linked to cryptorchidism, or the absence of one or both testicles from the scrotum.
Hypospadia occurs when the urinary channel does not form completely, so the urethra opens, not at the end of the penis, but rather along the bottom axis, usually in or close to the head or glans, but sometimes closer to the scrotum. Although hypospadias can generally be fixed, it does correlate with male infertility and suggests a disruption of the masculinization process in utero.
An unusually small penis is defined as a ‘micropenis’ if it is more than two-and-a-half standard deviations below mean penis size: that’s around seven centimetres (or 2 ¾ inches). Both hypospadias and micropenis are developmental abnormalities, and have been linked – like cryptorchidism – to exposure to EDCs while in utero.
The Japanese team found that homozygosity for a particular haplotype at the estrogen receptor gene ESR1 (the ‘AGATA’ haplotype) evidenced a pattern of hypersensitivity. Boys with this genetic profile were more likely to have cryptorchidism, hypospadias and micropenis; spermatogenic failure, however, was not linked to the gene variant, possibly because it emerges later in life, and thus might have even more complicated etiology. Although direct cause cannot be demonstrated, the researchers suggest that individuals with the homozygous ‘AGATA’ genetic variant might be more vulnerable in utero. Since so many EDCs mimic estrogen, this mechanism could affect male fertility.
Similarly, research on endocrine disruption in different strains of mice led by Jimmy Spearow (Spearow et al.\n 1999) found that male mice had quite different developmental outcomes from exposure to human estradiol, the primary female sex hormone. Some were relatively unaffected, even by large doses of estradiol. But others had their reproductive capacity eliminated entirely by relatively low doses; mature sperm simply did not form in these mice when they were dosed with extra estradiol.
The irony is that those lab mice with the highest fecundity — the best breeders — were also the most likely to be used in laboratories because of their low cost. This meant that the economics of lab mice were favouring those animals most resistant to estradiol disruption. Spearow and colleagues warned the method of screening for medical risks in humans might underestimate the effects of endocrine disruption processes in males because labs tended to use fast reproducing mice with the highest endocrine resilience.
Finally, in a study reported in 2007 by Aleksander Giwercman and colleagues, men from Greenland, Sweden, Poland and Ukraine were tested to see how their sperm quality related to their exposure to persistent organic pollutants, and whether some men had a genetic resistance. They looked at the androgen receptor (AR) gene, and specifically at the number of repeats of the CAG sequence in that gene. The number of repeats of CAG in the AR gene can vary from fewer than 10 to about 36 (more than that can lead to genetic disorders or greater chance of some cancers).
Giwercman’s team looked at the level of a specific PCB — 2,2′,4,4′,5,5′-hexachlorobiphenyl (CB-153). This PCB has been found to be good index of overall persistent organic pollution exposure. Those men with fewer than 20 repeats of CAG in their AR gene evidenced greater effect when they had higher-than-average EDC exposure; the drops in their sperm count and sperm densities were more pronounced than subjects with more than 20 repeats of the CAG sequence. The findings suggest that CAG repeats may buffer reproductive fitness against the effects of some EDCs.
All of these findings suggest that artificial endocrine disruption as a trait of our human-constructed niche will not influence every individual equally. Although these three cases focus on male infertility, female infertility is also common and, according to some researchers, increasing. Many of the ‘ideopathic’ cases of infertility, or cases in which the cause is unknown, may be linked to endocrine disruption, whether that’s from chemicals, stress, naturally occurring xenoestrogens, or another toxin.
If resistance to EDCs varies within the population, then those with vulnerability are more likely to experience reproductive failure. Given enough time, EDCs might lead to the sort of population-level genetic shifts that would pass the Neo-Darwinist litmus test. It’s hard to say, but at least in theory, it’s possible that EDCs would select humans in such a way to develop a population-wide resistance to endocrine disruption.
Although cultural factors affecting reproduction patterns might be stronger in the short term, EDCs — if they are, in fact, having this impact — would even act on artificial forms of reproduction, such as sperm and egg donation. Vulnerable individuals, such as men with low numbers of CAG repeats exposed to high levels of persistent organic pollutants, would more likely fall below acceptable thresholds for sperm donation. Even reproductive technology assistance might disproportionately favour those with EDC resistance.
What about the penises?!
Some of you, however, are still hanging on to find out whether our far-future great-great-great-grandsons will have tiny penises. The simple answer is: possibly, yes.
But it’s most likely the shrinkage will be a reversible effect of niche construction on individual development, a phenotypic bias, rather than a trait that becomes locked into our species’ DNA.
First of all, this comes with a pile of caveats — it’s really more of a thought experiment: If average penis size has, indeed, shrunk as a result of EDCs (both parts of this statement are controversial); and if we continue to put those pollutants or equally endocrine-disrupting and penis-shrinking chemicals into the environment; then, yes, we can expect our niche construction efforts, however inadvertently tragic and unfair, to favour the development of tiny penises, if boys are encountering these EDCs in utero. Since many of these EDCs are concentrated as they transition up the food chain and persist in the environment for quite some time, it's quite possible that boys will be born, on average, with smaller penises (remember all the caveats).
HOWEVER, it’s difficult to think of a way that this smaller penis state of affairs would be selected for genetically because it’s hard to imagine how even an endocrine disrupting niche would favour the reproductive success of genes for small-penis-susceptibility over genetic polymorphisms for other penis sizes (unless small penis genes were linked to other traits that were being selected for). In other words, artificial changes to our environment might shrink men’s penises, but it’s difficult to think of a scenario where that niche would favour smaller over larger in reproductive success, and that’s the key for the Neo-Darwinist litmus test.
For that reason, small penis size would be a trait transmitted by the environment rather than enshrined in the species’ gene pool. Small penises, like any niche-evoked trait, could be quite stable and enduring, but only as long as the environment continued to exert penis-shrinking influence (that is, as long as we continued to put these chemicals into the environment at a sufficient rate to replace those that were degrading).
So Bucky McMahon is probably wrong in at least a couple of ways: endocrine disruption may lead to early onset of puberty in girls, but it is probably also leading to early menopause or otherwise disrupting women’s fertility. ‘Sexuality’ as a psychological reality is a much more complex phenomenon, affected by how we see ourselves and how people interact with us, so no amount of dosing girls with xenoestrogens is going to ‘sex them up.’ If anything, it’s more likely to disrupt girls' reproductive lives.
In men, even if EDCs lead to smaller penises, they will also lead — given enough time — to a population more and more resistant to their effects, as selective pressures from this chemically constructed niche rebound back on us. And the penis shrinkage — if it is a reality — will most likely be reversible as soon as the substances responsible for it are removed or dissipate from the environment (although some EDCs do have transgenerational effects in animals in laboratory tests).
The bottom line is that niche construction theory encourages us to see the ways that organisms modify their environments so that the selective pressures they face change. In some cases, the niche that animals construct may be stable. But with humans, it’s anything but consistent at the moment, especially when we’re talking about the unpredictable effects of thousands of new chemicals introduced each year.
Whereas anthropologists may have once thought that culture and technology buffered our species from evolutionary processes, repealing the laws of natural selection, we now are much more ambivalent. Rapid change in our environment, even when we ourselves are driving that change, can lead to new selective pressures, radical shifts in the forces that shape our species’ survival and reproductive success. New elements in our constructed niches, like endocrine disrupting chemicals, can affect our evolution in quite subtle ways. Whether they will remain in our niche long enough to have substantial effect remains to be seen.
One reason I'm a strong advocate of niche construction theory is that it draws attention away from progressive accounts of human evolution that argue our future will be determined by our intentions and aspirations, made manifest in technological advances. The study of phenomena like endocrine disruption highlight the indirect links between cultural processes — innovations in chemistry and manufacturing — and natural selection through environmental change. Without being apocalyptic, the examination of EDCs and their effects on our fertility and penis size make clear that all evolution does not necessarily lead to a 'happy ending.'
[Sorry, had to get a final pun in.]
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This piece was originally published at: http://blogs.plos.org/neuroanthropology/2015/04/19/plastics-and-human-evolution/
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