Outbreeding: not what you may think

Mean number of children as a function of geographic distance between Danish marriage partners (Labouriau and Amorim 2008).

Most of us know about the genetics costs of inbreeding. If you do a Google search for "inbreeding is bad," you get 35,900 hits.  "Outbreeding is bad" yields only 2.

Yet outbreeding does incur genetic costs. It can reduce fitness either by introducing alleles that are unsuited to the local environment or by disrupting co-adapted gene complexes. When a native trout species was hybridized with non-native trout, fertility fell by half with as little as 20% admixture (Muhlfeld et al. 2009).

Fertility is the canary in the coal mine. A measurable decline is a sign that some genes are malfunctioning, either at the time of fertilization or during embryonic development. A malfunction can occur because the genes from the mother and father are too similar—the risk is higher that both copies of a gene will be defective. It can also occur because one copy is too different—incompatibilities may develop with other genes.

That's what we know from data on fish and other animals. But what about our species? At what degree of relatedness do the costs of human outbreeding start to exceed the benefits? When you marry a Neanderthal? The answer may surprise you. An Icelandic study found that fertility peaks at marriages between third or fourth cousins. Fertility is lower when the prospective parents are more closely related ... or less.

Our results, drawn from all known couples of the Icelandic population born between 1800 and 1965, show a significant positive association between kinship and fertility, with the greatest reproductive success observed for couples related at the level of third and fourth cousins. Owing to the relative socioeconomic homogeneity of Icelanders, and the observation of highly significant differences in the fertility of couples separated by very fine intervals of kinship, we conclude that this association is likely to have a biological basis. (Helgason et al. 2008)

The data come from a time when birth control was not widely practiced. Nonetheless, there may have been something different about Icelanders who married beyond their fourth cousins. Perhaps they were more likely to go to university, meet someone from the other side of the country, and eventually settle down and have children late in life. 

These socioeconomic factors were controlled in a Danish study that measured geographic distance between marriage partners: 

The Danish study was based on the cohort of all women born in Denmark in 1954 who were alive and living in Denmark in 1969, totaling 42,165 women. This cohort was followed up to the end of 1999. The number of children born to each mother between the ages of 15 and 45 years old was determined and is referred to as fertility. The mean marital radius (MR) associated with each mother in the cohort was estimated using the distance between the centroids of the parish where she was born and the parishes where the partners with which she had children were born. (Labouriau and Amorim 2008)

Fertility peaked at around 75 km. This relationship between fertility and marital radius was not explained by education, family income, urbanicity, or mother's age at first birth. The authors concluded that their findings were consistent with those of the Icelandic study, the cause being the same in both cases: fertility rises with decreasing relatedness up to a peak level and then starts to fall. Inbreeding depression then gives way to outbreeding depression.

How exactly does outbreeding reduce fertility? Joffe (2010) points to the steady decline in sperm quality since the early 20th century, suggesting it may be due to an increase in outbreeding. He rejects the usually cited cause: the rising level of estrogenic compounds in the environment, e.g., dioxin, DDT, PCBs, PBBs, phthalates, etc. This proposed cause fails to explain why the sperm quality decline has varied so much spatially, even within the same country. Why, for instance, has it been steep in Paris and nonexistent in Toulouse? Why is it nonexistent in domestic animals that are just as exposed to estrogenic compounds? Finally, the decline seems to have begun before most of these compounds began to be commercially produced. 

Joffe (2010) also suggests that there may be a parallel decline in egg quality. We don't really know because sperm is much easier to collect than eggs for large-scale study.

Do we now have outbreeding depression?

Today, inbreeding depression has largely disappeared throughout the Western world. For a long time the beneficial effects of outbreeding were shown by a steady increase in height and a steady decrease in the age of menarche. Both trends have now ground to a halt:

In Northern Europe, adult height has largely stabilised, and the age of menarche has also settled at around 13 years, while weight continues to increase due to obesity. (Cole 2003)

The steady rise in IQ, known as the Flynn Effect, has sometimes been attributed to outbreeding, although this explanation has been challenged (Flynn 2007, pp. 101-102; Woodley 2011). In any case, the Flynn Effect, too, is slowing throughout the West (Flynn 2007, p. 143). In Scandinavia, mean IQ peaked during the late 1990s and has since declined (Teasdale and Owen 2005).

Has outbreeding become more problematic than inbreeding? That's what the latest findings suggest, yet that doesn't at all seem to be the current wisdom.

References

Cole, T.J. (2003). The secular trend in human physical growth: a biological view. Economics & Human Biology 1(2): 161-168.

https://doi.org/10.1016/S1570-677X(02)00033-3

Flynn, J.R. (2007). What is Intelligence? Beyond the Flynn Effect. Cambridge University Press.

https://books.google.ca/books?id=qvBipuypYUkC&printsec=frontcover&hl=fr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false

Helgason, A., S. Pálsson, D.F. Guðbjartsson, þ. Kristjánsson, K. Stefánsson. (2008). An association between the kinship and fertility of human couples. Science 319(5864): 813-816.

http://facelab.org/debruine/Teaching/EvPsych/files/Helgason_2008.pdf

Joffe, M. (2010). What has happened to human fertility? Human Reproduction 25(2): 295-307.

https://doi.org/10.1093/humrep/dep390
https://academic.oup.com/humrep/article/25/2/295/671754

Labouriau, R., and A. Amorim. (2008). Comment on "An Association Between the Kinship and Fertility of Human Couples" Science 322(5908): 1634

https://doi.org/10.1126/science.1161907
http://science.sciencemag.org/content/322/5908/1634.2.full

Muhlfeld, C.C.,  S.T Kalinowski, T.E. McMahon, M.L. Taper, S. Painter, R.F. Leary, F.W. Allendorf. (2009). Hybridization rapidly reduces fitness of a native trout in the wild. Biology Letters, March 18

http://rsbl.royalsocietypublishing.org/content/early/2009/03/13/rsbl.2009.0033.short  

Teasdale, T.W., and D.R. Owen. (2005). A long-term rise and recent decline in intelligence test performance: The Flynn Effect in reverse. Personality and Individual Differences 39(4): 837-843.

https://doi.org/10.1016/j.paid.2005.01.029

Woodley, M.A. (2011). Heterosis doesn't cause the Flynn effect: A critical examination of Mingroni (2007). Psychological Review 118(4): 689-693.

http://dx.doi.org/10.1037/a0024759 

What you don't know can hurt you

In 1972, the U.S. passed the Clean Water Act, despite a presidential veto by Richard Nixon. Did this act also end an era of unusually high estrogen levels in the environment? (cartoon source)

There has been much concern over the presence of “environmental estrogens” in our drinking water and elsewhere in the environment. These are man-made chemicals, like DDT, PCBs, and dioxins, that mimic the effect of natural estrogens. Among other things, they’re blamed for declining sperm counts and rising male infertility.

Yet estrogen also enters our environment from a source that excites much less concern. This is the estrogen that women excrete every day in their urine. Shouldn’t that source also be cause for worry?

At first thought, no. People have been urinating for a very long time. And other animals for even longer. During that time, microorganisms have evolved to break down and feed on whatever is present in urine. Larger organisms have likewise had plenty of time to adapt to this aspect of their environment. Urine is so ubiquitous and unchanging that it could not possibly pose a danger. Or could it?

Actually, two things have changed in recent times. One is that humans have become much more numerous, with the result that much more urine is being discharged into the environment. Another is the way it is discharged.

Before the late 19th century, urine entered the environment via privies, cesspools, and ditch sewers (Rockefeller, 1996). It was thus discharged into a warm stagnant medium rich in organic matter—ideal conditions for rapid breakdown of the estrogen molecule by nitrifying bacteria (Vader et al., 2000). These same conditions, however, increasingly became a threat to public health, particularly in the ever larger and more numerous urban centers.

And so a new disposal system was developed. Human waste was now expedited via sewers to a central facility where the liquid component would be separated and rapidly discharged into the nearest cold body of water—which often doubled as the city’s source of drinking water. It was a perfect system for discharging urinary estrogen into the environment with as little biodegradation as possible … and then bringing it back into the human organism. As for urinary androgen, it was also present in wastewater but at much lower levels because of its lower solubility in water (Tabak et al., 1981).

That system survived until the late 1960s and early 1970s, when concern about pollution brought an upgrading of almost all sewage treatment facilities. If we look at the total number of Americans who produce untreated wastewater, this number peaked at 70 million in 1960 before falling to 2 million after passage of the Clean Water Act in 1972 (Copeland, 1993; US Council on Environment Quality, 1984). Primary treatment removes 35‑55% of estrogen from wastewater, and this proportion rises to 50‑70% for secondary treatment (Tabak et al., 1981). Today, tertiary treatment removes 90% of all natural and synthetic estrogenic compounds (LeQuire, 1999).

But what about the 100-year period when most wastewater went untreated? During that time, the main sources of drinking water must have been highly contaminated with estrogen. What were the effects? The most obvious ones would have been a decline in sperm counts and a rise in male infertility. But were there others? And should we soon see a reversal of these trends?

I tried to publish a paper on this subject, but the reviewers were skeptical. I was indulging in speculation that could never be proved one way or another. There simply are no records of estrogen levels in the environment for the period in question.

So I published my speculations on my blog (here, here, and here) and let the matter lie … while keeping an eye on the literature. Recently, three findings have come to my attention:

Primary treatment less effective than previously thought

A recent paper confirms that tertiary treatment of wastewater removes over 90% of all estrogen. On the other hand, primary treatment is less effective than previously thought, the removal rate being only 10% (Limpiyakorn et al., 2011).

Estrogen content of wastewater higher than previously thought

In the past, estrogen levels were measured only for the three most common kinds of estrogen: estrone (E1), estradiol (E2), and estriol (E3). Other natural estrogens, however, are present in urine. The total estrogen level in wastewater is thus 18-34% higher than previously thought:

[…] the total excretion rates of EEQ [estrogen equivalent] by estrone (E1), 17β-estradiol (E2), and estriol (E3) only accounted for 66–82% of the total excretion rate of EEQ among four different groups, and the other corresponding natural estrogens contributed 18–34%, which meant that some of the other natural estrogens may also exist in wastewater with high estrogenic activities. (Liu et al., 2009)

River and ocean sediments reveal formerly high estrogen levels in the environment

It is possible to look into the past by taking cores of sediments from the bottoms of lakes, rivers, and coastal waters. A study of the River Thames has found that estrogen levels are higher in river sediments deposited before the 1960s:

There is an indication of higher concentrations of E1 and E3 in samples deemed to be deposited before the mid-1960s, prior to the introduction of biological treatment at STWs [sewage treatment works] discharging to the estuary. […] This provides indirect evidence that historical improvements to wastewater treatment have resulted in a decrease in the concentrations of steroids in the effluent, as observed for PCBs and DDT from the same core (Gomes et al., 2011)

A similar finding comes from a study of sediment cores from Japanese coastal areas:

The concentration of natural estrogens such as 17β-estradiol (E2) and estrone (E1) in the sediment of coastal areas in Japan was determined […] Core samples were sliced every 2cm from the surface to 20cm deep for the measurement of estrogen. Although the concentrations of estrogens decreased with the depth of core samples, fairly high levels of estrogens were again noticed at the layer deeper than 16cm. (Matsuoka et al., 2005)

Conclusion

The most promising line of research seems to be the use of sediment cores to estimate past levels of estrogen in the environment. One problem will be calibration of sediment dating. Gomes et al. (2011) have pointed to a possible solution by noting that the mid-1960s correspond to the first sediment layer that contains synthetic estrogen, i.e., from birth control pills. Another problem is that estrogen seems to degrade gradually over time, even in river or ocean sediments.

References

Copeland, C. (1993). Wastewater Treatment: Overview and Background [93-138 ENR] Washington, D.C.: Congressional Research Service.

Frost, P. (2009). The urinary estrogen theory. Part I, Evo and Proud, March 11

http://evoandproud.blogspot.ca/2009/03/urinary-estrogen-theory-part-i.html

Frost, P. (2009). The urinary estrogen theory. Part II, Evo and Proud, March 18

http://evoandproud.blogspot.ca/2009/03/urinary-estrogen-theory-part-ii.html

Frost, P. (2009). The urinary estrogen theory. Part III, Evo and Proud, March 26

http://evoandproud.blogspot.ca/2009/03/urinary-estrogen-theory-part-iii.html

Gomes, R.L., M.D. Scrimshaw, E. Cartmell, & J.N. Lester.  (2011). The fate of steroid estrogens: partitioning during wastewater treatment and onto river sediments, Environmental Monitoring and Assessment, 175, 431–441.

http://www.springerlink.com/content/052274881l4186g5/

LeQuire, E. (1999). Something in the Water. InSites, 7(1),

http://eerc.ra.utk.edu/insites/ins7-1.htm#Something

Limpiyakorn, T., S. Homklin, & S.K. Ong. (2011). Fate of estrogens and estrogenic potentials in sewerage systems, Critical Reviews in Environmental Science and Technology, 41(13), 1231-1270.

Liu, Z., Y. Kanjo, S. Mizutani. (2009). Urinary excretion rates of natural estrogens and androgens from humans, and their occurrence and fate in the environment: A review, Science of the Total Environment, 407, 4975–4985

Matsuoka, S., R. Sakakura, M. Takiishi, Y. Kurokawa, S. Kawai, & N. Miyazaki. (2005). Determination of natural estrogens in the sediment of coastal area in Japan, Coastal Marine Science, 29(2), 141-146.

http://repository.dl.itc.u-tokyo.ac.jp/dspace/handle/2261/5593

Rockefeller, A.A. (1996). Civilization and sludge: Notes on the history of the management of human excreta. Current World Leaders, 39, 99‑113.

Tabak, H.H., R.N. Bloomhuff, & R.L. Bunch. (1981). Steroid hormones as water pollutants II. Studies on the persistence and stability of natural urinary and synthetic ovulation‑inhibiting hormones in untreated and treated wastewaters. Developments in Industrial Microbiology, 22, 497‑519.

U.S. Council on Environment Quality. (1984). Annual Report. Washington D.C.

Vader, J.S., C.G. van Ginkel, F.M.G.M. Sperling, J. de Jong, W. de Boer, J.S. de Graaf, M. van der Most, & P.G.W. Stokman. (2000). Degradation of ethinyl estradiol by nitrifying activated sludge. Chemosphere, 41, 1239‑1243.