The inevitability of introgression18 Dec 2006
I'd like to draw your attention to my new article on genetic introgression from archaic humans, written with Gregory Cochran. The article is in PaleoAnthropology, and is completely open access.
I can't say enough good things about this process and the value of having open access research results, which can be downloaded free anywhere on the planet.
A search for "introgression" here on the weblog will bring up a lot of relevant material, including the introgression and MCPH1 FAQ, a quick note about the importance of introgression in wild species, an opinion about why "introgression" doesn't imply "speciation", and the all-important Neandertal genome FAQ. I've been writing about the subject a lot, because we've been thinking about it a lot.
If you read nothing more, this is the most important quote (p. 104):
If the modern human population expanded at a rate of 1 percent per generation, then an introgressive allele with s = 0.01 (i.e., a 1 percent fitness advantage) would have a 95 percent probability of fixation in modern humans, with only 74 archaic-modern matings. For an allele with a 5 percent fitness advantage, the corresponding number of events would be only 24.
Here, I don't want to repeat all of what I've written already, but I want to jot down some of the reasons why our new paper is worth reading:
- The central point of the paper is exceedingly simple. Haldane demostrated in 1927 that the fixation probability of a single copy of a new adaptive allele is 2s. This means that if archaic humans had any alleles that would have been adaptive for modern humans, it would take only a very small amount of interbreeding for modern humans to pick up these alleles, with a near-100 percent likelihood.
- One may point out that if this simple genetic observation were accurate, then natural populations ought to display many examples of introgression. In fact, they do. We have laid out a very extensive review of instances of introgression among natural populations. We focused on cases where the introgressive gene had adaptive importance. This included a large number of instances of introgression from wild to domesticated species and vice-versa, which are well-known from breeding experiments. However, there have been a growing number of examples of adaptive introgression between different natural populations as well. The use of more nuclear markers has begun to uncover many, but importantly many species have adaptive introgression of mitochondrial DNA. Those European mice are not unique -- the phenomenon is widespread.
- The neatest example we drew upon was the extended phylogenetic history of cattle-bison introgression. It's too long to quote, but it may by itself be worth reading the paper. The geographic and ecological differentiation of cattle may be a strong parallel to the different Pleistocene populations of Homo.
- In case you think bovines are too weird to apply to hominids, we also review many domesticated mammals from Eurasia that have very strong east-west biogeographic differentiation with substantial introgression in recent times, in many cases involving two or more wild progenitor species. Ecological change -- including domestication -- appears to be the biggest factor underlying adaptive introgression in animals. One of the most important mechanisms in wild populations is the absorption of endemics by cosmopolitan species through introgressive hybridization. Both mechanisms may have driven modern human origins.
- The simple predictions for adaptive genes differ greatly from the predictions for neutral genes. We expect that introgression was centrally important for the evolution of adaptive features of modern humans, both within and outside of Africa. This does not conflict with the observation that the ancestry of a neutral locus is predominantly or even exclusively African. Indeed, our paper suggests that the ecological circumstances surrounding an African population dispersal may have strongly favored the introgression and subsequent redispersal of Eurasian alleles.
- One of the big reasons why our paper differs from earlier work is that we consider genetic effects rather than species definitions. There is a long literature on species concepts that -- to varying degrees -- discuss mammalian hybrids. I especially recommend work by Trent Holliday in a 2003 review of species concepts and a forthcoming book chapter, a long series of articles by Clifford Jolly (culminating in a 2001 review article, Darren Curnoe and Alan Thorne in a series of articles (e.g., 2001). Analogy with the systematics of other taxa will always be important in paleoanthropology, because we cannot observe the reproductive behavior of extinct hominids. All these studies and many others agree that some amount of interbreeding between regional populations of archaic humans would have occurred. In this context, the importance of introgression is now in the realm of direct quantification rather than analogy. It makes little difference whether hominids were more like baboons or more like some other model. Humans are the one primate species for which adaptive introgression is now most amply documented.
We briefly discuss in this paper several loci that demonstrate introgression in humans, but we have reserved a more extensive review for another forthcoming paper.
There is a lot of action on this front right now, because our knowledge of variation across the genome has become ripe for it. In short, with 25,000 genes to work with, there are unquestionably many that have drawn their adaptive nature in modern humans from some archaic population. It remains to be discovered just how many there are, and what proportion of them come from different archaic populations.
We think that this is one of the two major forces underlying the emergence of modern humans, and one that underlines the enormous evolutionary potential of our species. As we conclude:
The notion that a single small population of incipient modern humans had the perfect genetic combination for ultimate success seems quite improbable. Instead, the long coevolution of modern anatomy and behavior in contact with archaic humans, even as those archaic populations appeared to diminish, provided a rich source of adaptations for the expanding modern population. With current genomic techniques, we are beginning to find these archaic genes. We expect that they will prove central to the story of modern human origins.
Hawks J, Cochran G. 2006. Dynamics of adaptive introgression from archaic to modern humans. PaleoAnthropology 2006:101-115. Free full text