Lewontin's legacy

 

Lewontin assumed that genetic diversity between populations is qualitatively similar to genetic diversity within populations. So comparing the two would be like comparing apples with apples. He was wrong. The second kind of diversity is less functionally significant.

 

 

The geneticist Richard Lewontin died last Sunday at the age of 92. He became prominent during the 1970s, particularly through his 1972 paper "The Apportionment of Human Diversity." Using data from blood groups, serum proteins, and red blood cell enzymes, he found far more genetic diversity within human populations than between them:

 

The results are quite remarkable. The mean proportion of the total species diversity that is contained within populations is 85.4%, with a maximum of 99.7% for the Xm gene, and a minimum of 63.6% for Duffy. Less than 15% of all human genetic diversity is accounted for by differences between human groups!

 

It is clear that our perception of relatively large differences between human races and subgroups, as compared to the variation within these groups, is indeed a biased perception and that, based on randomly chosen genetic differences, human races and populations are remarkably similar to each other, with the largest part by far of human variation being accounted for by the differences between individuals.

 

His reasoning seems sound. It ignores, however, two aspects of population genetics:

 

1. Genetic differences between populations are qualitatively different from genetic differences within populations. A population boundary is usually a boundary between different environments, either natural environments or cultural environments. It is thus a boundary between different pressures of natural selection and, hence differences in adaptation. An allele may work just fine on one side of the boundary, but not so well on the other side. Conversely, genetic diversity within a population is less meaningful because the end result tends to be the same. Everyone is adapting to the same environment. Genetic differences are less likely to produce real functional differences.

 

2. Genetic differences vary considerably in their functional significance, with the overwhelming majority having little or none. Many of these differences are found in junk DNA.

 

Lewontin discovered the obvious. Most genetic differences have little or no functional significance, and such differences account for most of the diversity within human populations. The more a genetic difference has real consequences, the less likely it will be found within a population because that is where the pressures of selection are uniform. It will more likely be found at a population boundary where the pressures of selection are different.

 

We see this, for example, in dog breeds. Although they differ considerably in anatomy and behavior, they are barely discernable in the genetic data. There is much more diversity within breeds than between them:

 

... genetic and biochemical methods ... have shown domestic dogs to be virtually identical in many respects to other members of the genus. ... Greater mtDNA differences appeared within the single breeds of Doberman pinscher or poodle than between dogs and wolves. ... there is less mtDNA difference between dogs, wolves, and coyotes than there is between the various ethnic groups of human beings, which are recognized as a single species. (Coppinger & Schneider 1995)

 

Well, dog breeds have been created through human-directed selection. What about subspecies that have arisen through natural selection? We see the same fuzziness, not only between subspecies but also between many sibling species that are anatomically distinct. In the deer family, genetic diversity is greater within some species than between some genera (Cronin 1991). Some masked shrew populations are genetically closer to prairie shrews than they are to other masked shrews (Stewart et al. 1993). Only a minority of mallards cluster together on an mtDNA tree, the rest being scattered among black ducks (Avise et al. 1990). All six species of Darwin's ground finches seem to form a genetically homogeneous genus while showing very little concordance between mtDNA, nuclear DNA, and morphology (Freeland & Boag 1999). In terms of genetic distance, redpoll finches from the same species are not significantly closer to each other than they are to sibling species (Seutin et al. 1995). Different species of haplochromine cichlids cannot be easily told apart by means of nuclear or mitochondrial genes, yet they are well differentiated morphologically and behaviorally (Klein et al., 1998). Neither mtDNA nor allozyme alleles can distinguish the various species of Lycaedis butterflies, despite clear differences in morphology (Nice & Shapiro 1999). An extreme example is a dog tumor that spreads through sexual contact: canine transmissible venereal sarcoma. It looks and acts like an infectious pathogen, yet its genes would show it to be a canid, and some beagles may be genetically more similar to it than they are to Great Danes (Yang 1996; see Frost 2011 for a full discussion).

 

When populations diverge under the impact of divergent pressures of natural selection, changes initially occur only within a fraction of the genome. Later, with the passage of time, the two populations will drift apart over the rest of the genome. But the human species is still young. The genetic split between Africans and non-Africans goes back only 60,000 years, and other splits are younger still.

 

This doesn't mean that genetic diversity between human populations is trivial. In fact, almost the opposite is true. It is the diversity within populations that is largely trivial.

 

 

References

 

Avise, J.C., C.D. Ankney, and W.S. Nelson. (1990). Mitochondrial gene trees and the evolutionary relationship of mallard and black ducks. Evolution 44: 1109-1119.

https://doi.org/10.1111/j.1558-5646.1990.tb03829.x

 

Coppinger, R. and R. Schneider (1995). Evolution of working dogs. In: J. Serpell (ed.) The Domestic Dog: Its Evolution, Behaviour and Interactions with People. Cambridge: Cambridge University Press, pp. 21-47.

https://books.google.ca/books?id=4fB7DQAAQBAJ&printsec=frontcover&hl=fr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false

 

Cronin, M. (1991). Mitochondrial-DNA phylogeny of deer (Cervidae). Journal of Mammalogy 72: 533-566.

https://doi.org/10.2307/1382139

 

Freeland, J.R. and P.T. Boag. (1999). The mitochondrial and nuclear genetic homogeneity of the phenotypically diverse Darwin's ground finches. Evolution 53: 1553-1563.

https://doi.org/10.1111/j.1558-5646.1999.tb05418.x

 

Frost, P. (2011). Human nature or human natures? Futures 43: 740-748.

https://www.researchgate.net/profile/Peter_Frost2/publication/251725125_Human_nature_or_human_natures/links/004635223eaf8196f0000000.pdf  

 

Klein, J., A. Sato, S. Nagl, and C. O'hUigin. (1998). Molecular trans-species polymorphism. Annual Review of Ecology and Systematics 29: 1-21.

https://doi.org/10.1146/annurev.ecolsys.29.1.1

 

Lewontin, R.C. (1972). The apportionment of human diversity. Evolutionary Biology 6: 381-398.

https://emilkirkegaard.dk/en/wp-content/uploads/Lewontin-1972-The-Apportionment-of-Human-Diversity.pdf

 

Nice, C.C. and A.M. Shapiro. (1999). Molecular and morphological divergence in the butterfly genus Lycaeides (Lepidoptera: Lycaenidae) in North America: evidence of recent speciation. Journal of Evolutionary Biology 12: 936-950.

https://doi.org/10.1046/j.1420-9101.1999.00111.x

 

Seutin, G., L.M. Ratcliffe, and P.T. Boag. (1995). Mitochondrial DNA homogeneity in the phenotypically diverse redpoll finch complex (Aves: Carduelinae: Carduelis flammea-hornemanni). Evolution 49: 962-973.

https://doi.org/10.1111/j.1558-5646.1995.tb02331.x

 

Stewart, D.T., A.J. Baker, and S.P. Hindocha. (1993). Genetic differentiation and population structure in Sorex Haydeni and S. Cinereus. Journal of Mammalogy 74: 21-32.

https://doi.org/10.2307/1381902

 

Yang, T.J. (1996). Parasitic protist of metazoan origin. Evolutionary Theory 11: 99-103.

Apples, oranges, and genes

Publicly funded misinformation. Source: PBS website

In human genetics, a ‘population’ is a group of individuals who share ancestry and hence genes. This sharing is not absolute. There is always some gene flow from outside, and sometimes “outside” means another species. We humans, for example, have received genes not only from Neanderthals and Denisovans but also from … viruses.

In addition, new gene variants are constantly arising through mutation. Most of them are harmful or useless. But some are useful and will thus spread through the population.

So below the species level, and often even at the species level, population boundaries tend to be fuzzy. Genes vary both between and within populations.

You’ve undoubtedly heard that there is much more genetic variation within human populations than between them, this being true even for the large continental populations we used to call ‘races.’ This was the finding of the geneticist Richard Lewontin (1972), and others have concluded likewise. You’ve probably not heard, however, that the same kind of genetic overlap exists between many sibling species that are nonetheless distinct in anatomy and behavior (Frost, 2011).

How come? First, keep in mind that genes vary a lot in adaptive value. Some are little more than ‘junk DNA.’ Others code for structural proteins that form the building blocks of flesh and blood. Others still are very important because they code for regulatory proteins that control how other genes behave and, hence, the way an organism grows and develops. The last kind of gene accounts for only a tiny fraction of the genome. Most genes have modest effects, or none at all.

Second, keep in mind that different populations occupy different environments and are thus exposed to differences in natural selection. In most species, these differences are due to physical environments that differ in climate, vegetation, and wildlife. Humans also have to adapt to cultural environments that differ in social structure, belief systems, and technology. In either case, when a gene varies between two populations the cause is probably a difference in natural selection, since the population boundary also separates different selection pressures. Conversely, when a gene varies within a population this variation is less likely to have adaptive significance. It hasn’t been flattened out by the steamroller of similar selection pressures.

This is one aspect of “Lewontin’s fallacy.” Within-population variation isn’t comparable to between-population variation. It’s like comparing apples and oranges.

Another aspect of Lewontin’s fallacy is that natural selection within a population exercises a leveling effect only on phenotypes, and not on genotypes. If two gene variants have a similar phenotypic effect, natural selection will take longer to replace one with the other. Sometimes, this sort of diversity will persist indefinitely because epidemics often spare individuals whose surface proteins are somewhat different from those of their neighbors.

Thus, within-population variation tends to consist of different gene variants at different loci whose effects nonetheless point in the same general direction. To some degree, these variants can stand in for each other. If one is absent, another one might do the trick. This is probably why population differences are more sharply defined if several gene loci are compared simultaneously. If we chart how each gene varies geographically and then superimpose these maps on top of each other, the resulting composite map will show population differences in sharper relief (Edwards, 2003; Mitton, 1977; Mitton, 1978; Sesardic, 2010).

This point has been made by Emmanuel Milot, the principal author of the paper I reviewed in my last post. His research team found that the time between marriage and first birth steadily shrank among succeeding generations of French Canadians on Île aux Coudres (Milot et al., 2011). In the land-rich environment of the New World, there was strong selection for married women to get pregnant faster. A genetic difference has thus developed between French Canadians and the French who remained in France.

But this difference is not due to a few genes. As Milot points out, natural selection tends to produce effects at many different genes:

“We should not think that there are genes that code specifically for age at first reproduction. In fact, this type of trait is probably influenced by hundreds, even thousands, of genes. These genes act on other characteristics, like body weight at birth, age at first menstruation, or even personality traits, which impact on age at first birth” (Bourdon, 2011)

This point is important. If two populations differ at one gene, and if the difference is sensitive to natural selection, they probably also differ at many other genes. The same selection pressure that caused one difference has almost certainly caused others. Typically, we see only the tip of the iceberg—a gene variant that produces an obvious effect in affected individuals, such as illness. Most gene variants, however, don’t cause medically recognized illnesses, and their effects also tend to be subtler.

References

Bourdon, M-C. (2011). L’espèce humaine. Toujours en évolution. UQAM. Entrevues
http://www.uqam.ca/entrevues/entrevue.php?id=965

Edwards, A.W.F. (2003). Human genetic diversity: Lewontin’s fallacy. BioEssays, 25, 798-801.

Frost, P. (2011). Human nature or human natures? Futures, 43, 740-748. http://dx.doi.org/10.1016/j.futures.2011.05.017

Lewontin, R.C. (1972). The apportionment of human diversity. Evolutionary Biology, 6, 381-398.

Milot, E., F.M. Mayer, D.H. Nussey, M. Boisvert, F. Pelletier, and D. Réale. (2011). Evidence for evolution in response to natural selection in a contemporary human population, Proceedings of the National Academy of Sciences (USA), early view

Mitton, J.B. (1977). Genetic differentiation of races of man as judged by single-locus and multilocus analyses, American Naturalist, 111, 203-212.

Mitton, J.B. (1978). Measurement of differentiation: reply to Lewontin, Powell, and Taylor, American Naturalist, 112, 1142-1144.

Sesardic, N. (2010). Race: a social destruction of a biological concept, Biology and Philosophy, 25(2), 143-162.

Thoughts on the crisis

Historians will argue back and forth over the causes of the current economic crisis, just as they still argue over the causes of the Great Depression. But there is consensus on some points:

• The U.S. government wanted to increase home ownership among Hispanic and African Americans. Since it was politically unacceptable to impose racial quotas on mortgage money, this could be done only by pressuring banks to relax lending practices, even to the point of eliminating down payments (!). The rules were thus loosened across the board for everyone.
• The increase in home buyers set off an inflationary spiral that became self-perpetuating. People bought houses with the intention of reselling them at a much higher prices.
• The rising house prices fuelled demand for housing construction. Entire exurbs of McMansions were being built until the crisis began.
• The Federal Reserve kept all of this going by providing lenders with cheap money.

In sum, the boom kept going as long as enough people could borrow enough money to buy more and more homes at higher and higher prices.

It couldn’t go on forever. On the one hand, wages have not kept pace with housing prices, not to mention the rising cost of oil and food. On the other, mortgages were being given to people who were, by any honest measure, insolvent.

Will the crisis be resolved by the proposed $700 billion bailout? This one might be resolved, at least for now. But the same kind of speculative bubble could happen elsewhere in the economy for similar reasons. The U.S. economy is increasingly geared to creating illusory value.

In all fairness, the bailout may buy time to dismantle the bubble economy before more damage is done. The U.S. government could stop badgering lenders to relax their lending criteria. The Federal Reserve could stop providing cheap money. The speculators and deadbeats could be stripped of their ill-gotten gains.

It won’t happen.

What then? A full-blown recession will likely be averted for another two years. By then, any further bailout would reach astronomical figures and simply drag down those who were wise enough to shun speculation and improvidence.

When I was an undergrad, I remember reading a Marxist book on economics. Among other things, it argued that the boom-bust cycle is inevitable. Once a boom has set in, decision-making becomes less and less optimal. Market discipline slackens and incompetence increasingly goes unpunished. Even if you do get fired or if your company goes under, you can always get rehired elsewhere. Many people also take advantage of the boom to make money through pure speculation, and they will do their utmost to keep the boom going until speculation has become the main driving force. Why not? It’s their bread and butter … or rather their cocaine and cognac.

And so, the longer the boom goes on, the greater the load of inefficiency that the economy has to bear. Eventually a crisis becomes inevitable and even desirable … to clean all the gunk out of the system.

But there is another wrinkle to the current boom-bust cycle. It is playing out against the backdrop of a worsening commodity crisis. Demand is increasing faster than supply for the basics of life, particularly oil, food, and water. Resource-rich countries will be all right. But things will be less rosy for areas that have a high ratio of people to resources, like the Eastern U.S., California, Western Europe, and many areas of the Third World.

Nonetheless, many of these same areas have embarked on a program of aggressive population growth through immigration. The U.S. is projected to grow by 135 million in just 42 years—a 44% increase (Camarota, 2008). The United Kingdom is slated to grow by 16 million in 50 years—a 26% increase (United Kingdom – Wikipedia).

This situation might be manageable if the immigrants were going into export sectors that can earn foreign exchange and pay for increased imports of oil, food, and water (yes, fresh water will become an item of international trade). But they aren’t. For the most part, they are being brought in to serve the needs of agribusiness, slaughterhouses, landscapers, homebuilders, hotel and restaurant services, and so forth.

Yes, we are living in interesting times.

Reference

Camarota, S.A. (2008). How many Americans? The Washington Post. Tuesday, September 2, 2008; Page A15