genealogy

I had a great session with my advanced students yesterday running through different evolutionary scenarios for the X-Woman. This and some later posts will follow up on my initial thoughts ("Hobbit version 2.0: the undiscovered hominin").

May I just say, "X-Woman" is one of the more dopey nicknames for an ancient piece of bone? I mean, it's better than "Twiggy", but jeesh. I can't be the only one who thinks of John Singer Sargent:

"Madame X", the once-shocking salon portrait by John Singer Sargent. Fulfilling my lifelong dream of bringing Sargent together with Neandertals.

Meanwhile, I have some great e-mails about Madame X, some of which I can share. First, an exchange on the topic of incomplete lineage sorting:

I'm confused by your suggestion of an ancient divergence among Neanderthals. Wouldn't that lead to a tree with the Siberian DNA and other Neanderthal DNA samples forming their own clade, to the exclusion of human DNA? As things stand, the Neanderthals are closer to humans than to the Siberian DNA.

Not at all; it could be either way.

Consider humans today. Africans have mtDNA lineages (the L clades) that are deeper in the human tree than any outside of Africa and basically absent elsewhere except for recent migration. But Africa also contains many of the mtDNA lineages that are present in Europe, India and West Asia.

Now imagine that the human population divides into two species, Africans and non-Africans, and those species persist for 100,000 years. Assuming no huge bottlenecks in either of these species, they both ought to retain the major clades present today. If we sample their genes at that time, 100,000 years in the future, we'll discover that Africans will be more genetically diverse than non-Africans. And the Africans will have L clades that are outgroups to the clades (M and others) that include *some* Africans and *all* non-Africans.

Subsequent population bottlenecks or selection could eliminate those ancient clades, but they will hang around unless they are eliminated. That's also the explanation for why humans and gorillas are more genetically similar at some loci than either is to chimpanzees, even though humans and chimpanzees speciated more recently. The variation in that ancestral H-C-G population was retained in the ancestral H-C population, to some extent, and lineage sorting sometimes gave humans the more gorilla-like clade.

An interesting question is whether the rest of the Neandertal sample would be so relatively invariant, if some part of their population included this quite divergent mtDNA haplotype.

It's quite hard to answer that question given the small sample of Neandertal mtDNA -- only less than twenty individuals, sampled from a range of times. A "lopsided" tree, with a lot of similar sequences and a few divergent ones, is not an unlikely genealogy in a small sample. The variance in the lengths of the deep branches in a genealogy is intrinsically high, even in the simple Wright-Fisher model with no population structure or selection. A "lopsided" tree is just one possibility on a continuum, in which the deepest coalescence time in the sample is high relative to the next deepest -- not an unlikely event at all.

For those who would like to explore this process, I put together a Mathematica demonstration ("Coalescent Gene Genealogies") that generates random gene trees under the neutral Wright-Fisher model. Strange-looking trees are normal, in the sense that they occur often enough that they are not statistically unlikely for a single gene locus.

Obviously what you'd want to do is compare multiple gene loci -- in this case, to get nuclear genomic sequence. Since the Max Planck group is actively pursuing further sequencing (and already has had some success, according to their press conference), I expect they're already making progress toward testing the neutral hypothesis.

If mtDNA proves to be unusual compared to other loci, then it's either intrinsic coalescent variability, or selection. Testing those two alternatives would require a larger sample of Neandertal mtDNA.

If, on the other hand, the nuclear genetic diversity is also substantially not shared with Neandertals (or living people), then the hypothesis of population structure in Late Pleistocene-age Eurasia would be strongly supported. It's a bit more complicated to test whether a speciation had occurred, but with whole genomes such a test can almost certainly be done.

Larry Moran tells an interesting personal story about long-distance gene flow among Roman-era elites in Europe (What does Marcus Antonius tell us about evolution?). He describes the genealogical connection between Mark Antony and the dark-age Irish warlord, Niall of the Nine Hostages, Y-chromosomal progenitor of a large proportion of Irish (and British) men.

But the strange thing is that after this story, describing how one man's descendants covered more than a thousand miles in a few generations, Moran gives this conclusion:

New beneficial alleles will not make much headway in 2000 years because gene flow between subpopulations is very low. There's no reason to assume that it was any different in the ancient past—it may even have been worse. Think about that the next time you hear about some hypothetical allele that arose 50,000 years ago and became fixed in the entire species. That's not very likely.

I would conclude just the opposite from the story. Garlic mustard has spread across North America after being introduced from Europe less than 500 years ago. It is currently invading formerly "wilderness" spaces such as the remaining patches of prairie here in Wisconsin. This has not happened by a slow, plodding spread from one square meter to the next. It has happened because every so often a few mustard seeds get stuck in the tread of someone's shoe, or tire, or in mud stuck in wheel-wells of cars and four-wheelers. Those seeds get carried into wilderness areas, many miles from their sources.

Only a very small fraction of garlic mustard seeds get themselves stuck in shoes. We might think that surely this small number should be no threat to Wisconsin prairies. It would take hundreds or thousands of generations for them to make any difference, right?

But garlic mustard grows exponentially, particularly if that area has been disturbed by fire, plowing, traffic or overbrowsing. A tiny number of seeds are all it takes to spread invasively into a new place. A small amount of long-distance movement has been sufficient to permeate almost every suitable mustard habitat in North America, in less than 500 years.

A selected gene is like garlic mustard. We may say that only a few members of the Roman elite intermarried with Britons. But if a single Roman married a Briton, carrying an advantageous gene, that gene has the chance to grow exponentially. That chance is not a guarantee, any more than a single garlic mustard seed is a guarantee. A single copy of an advantageous gene still has a very high probability of being lost by chance. But selected genes have a much higher chance of spreading than neutral ones. A very slight amount of long-distance gene flow can cause a selected gene to spread vastly faster than diffusion across a population.

Besides that, in this case, the history is incomplete. Roman legions occupied Britain for more than 400 years. Those legions were not only Italian, but included soldiers from across the empire, including in one famous instance thousands of Sarmatians. Sarmatians carried with them genes from the steppes of Central Asia, much farther than Rome. Soldiers were stationed for years, and many left the service and became local merchants, landowners, or minor nobles. They were not celibate. For that matter, neither were the early Latin clergy...

This massive flow of genes into the British Isles did not erase the standing genetic variation, some of which persisted from Neolithic and Paleolithic Britons. But the immigrants were more than enough to spread advantageous genes into the British population. We need not imagine one hitchhiking like mustard seed in the grandchildren of Mark Antony, although that is certainly possible. Antony's descendants were joined by thousands of lonely Roman soldiers stationed for years in backwater British towns, horny Vikings, pillaging Saxons, conquering Normans, and the occasional German prince.

Early gene flow would have been more influential on the present composition of the British population than later gene flow. But if the question is whether a gene could traverse the European population in a few thousand years, there have been ample opportunities. And if we go back 50,000 years, even relative isolates like Australia and the Americas had their chance to get such genes.

All this just says that it is plausible for genes to have spread widely through the human population recently. It's no proof that they actually did so, or that they had substantial effects on human similarities or differences. For that we must turn to empirical evidence.

In that vein, here's a question that I know is of interest to a number of people: How similar should the selected genes in Britain, or Northern Europe generally, be to those of Central Asia, or the Near East, or Italy? We have samples of genetic variation in each of these places (and many others) that would answer the question empirically. We know that the majority of the genome, presumably neutral to selection, shows significant population differentiation among those places. But what does theory tell us? Should we expect selected genes to have a different pattern?

On this, I'll have to save my answer for later....