On natural selection in humans
In the Rival del Garda meeting we were happy to see Luca Cavalli-Sforza for the first time in many years. Luca, a towering figure in human genetics in the last third of the 20th century, was one of the most important conceptual leaders in uniting population (evolutionary) genetics, along with culture and language, in accounting for current human diversity. Luca, long at Stanford but who retired back home in Italy a few years ago, is well into his '80s, but still spry enough and intellectually lively. Ken had interacted with him extensively in the past, including a mid-70s sabbatical in his lab at Stanford, and subsequently in the attempt to organize a global human genome diversity project (HGDP).
Luca gave a talk at the meeting on natural selection in humans. We wondered whether, at his age and removal from Stanford he could really be up to date with the huge, rapidly emerging literature on searches of the human genome for signatures of selection. Intense, highly technical genomewide comparison of variation between humans and other primates, but especially among human continental groups, has been undertaken by many investigators using HGDP-like samples and the genetic variation in the HapMap project.
There, the idea is to find genes or genome regions in which variation is reduced in ways suggesting that specific selection has taken place--such as to produce lighter or darker skin color in various continents and/or climates, or the ability of humans to resist malaria, or of adults to digest milk (these are the classic examples).
Such searches are for classically Darwinian effects. That is, they're about who in a population has higher 'fitness'--net reproductive success because they survive better or simply have higher fertility. The search is difficult and only a few specific instances have been found, for reasons too much to go into in this post. But there is at least widespread belief that there's been quite a lot of such selection since we spread out from our African ancestral home to become a globally distributed species: how could we inhabit the globe's diversity of environments without this being the result of natural selection?
Well, Luca surprised us. His point was about culture rather than genes per se. He quite correctly noted that our having culture helped us adapt quickly to diverse environments (clothing and fire, rather than fur, to protect against cold, for example, or language to communicate among coordinated hunters or gatherers).
Non-Darwinian group selection
Luca's evidence was thus entirely unrelated to the current genomewide statistical searches, but instead related to our rapid global expansion that could not be explained by genes--except by our species' shared genes related to thinking ability, that made us capable of culture.
Humans have clearly expanded rapidly at the expense of other species. We have invaded every environment, and displaced other species where needed, advancing some such as cattle or wheat for our own use instead. Our numbers have increased in a few thousand years from a few thousand to a few billion. Nothing could be clearer as proof of natural selection in humans.
However, this is not Darwinian selection in the usual sense! Instead it is a kind of group selection, the favoring of our group vis-a-vis groups of other species that we displaced. It is closer to the version of selection and evolution proffered by Alfred Wallace (who came to his ideas independently of Darwin). Wallace gave more stress to group competition and group struggle against environments, while Darwin clearly and strongly stressed competition among individuals within groups.
The two are not incompatible at all, and both processes can be occurring at any or every time. But it's not what people have in mind these days, in their frenetic hunt for good and bad genes. So Luca may or may not be up to date in that area of work, but he certainly pointed out what is, for our species, clearly and by far the most important aspect of selection involving humans! Far more important than the rather minor kinds of selection we know about at the specific gene level--even including malaria and skin color effects.
Politically correct, if scientifically incorrect
However, in stressing this view, Luca went on to argue that because selection in humans was culture-based, there was little evidence for racial differences that could be attributed to selection. Race differences (here, let's ignore the problems with the term 'race'), he said, are superficial only. They don't reflect natural selection beyond such traits as skin color. The argument is one Luca has been making for decades, as he has been perhaps by far the leader in trying to relate human genetics to human culture, such as correlating language with geography with genetic variation. But his argument unfortunately reflected a quite out-dated view, that in some ways can even be said to be politically correct, if scientifically incorrect. To see why, let's look at the case that was made.
Luca has long pointed out that, to a considerable degree, human genetic differences are correlated with geography. The farther apart geographically that two people are (here, we refer to 'indigenous' people rather than recent intercontinental migrants), the more different they are genetically. This is called 'isolation by distance.' There is quibbling about the details, but the idea is basically accurate: French and Swedish people are genetically more like each other than French and Koreans are. This, Luca argued, shows that there cannot be much due to natural selection, because selection is related to local environmental conditions, which can be very different in nearby regions, or very similar in distant regions, would not leave such a generic pattern of differences.
But there's a subtle fallacy here. Selection of a given trait affects only the genes that produce that trait, not the whole genome. Even if selection is affecting all genes at all times, each gene is affected by different environmental conditions. And selection works not with global variation, but only with variation present in any local area. Thus, even with selection, we see isolation by distance effects.
More importantly, isolation by distance is studied by using genomewide variation. There is often a deliberate choice of genetic variants that are thought not to be involved in functionally important traits (so-called selectively neutral parts of the genome), and hence variants that are not involved in selection. Isolation by distance in the genome overall, especially at such neutral regions, is perfectly compatible with all sorts of selection going on at individual genes, but differently in different world regions.
We can see this easily in another way. Two people can have a trait, like blue eyes, diabetes, or color blindness for the same genetic reason. As a rule, the same genetic variant found in two people are descendant copies of a single original mutation that occurred sometime in the past. In that sense, they are close relatives at that particular gene. But if you look at genomewide variants, they will have no particular relationship relative to other people in the population.
So, whatever you think about the pervasiveness or importance of natural selection in the history of different human 'races', the isolation by distance argument is basically irrelevant.
Thus, while the massive global expansion of humans is overwhelming and persuasive evidence for culture-based group selection favoring humans, the global human expansion is perfectly compatible with all sorts of local selection taking place. How much of that has actually happened is a separate question requiring its own kind of evidence; and so far, that evidence has been very hard to come by.