More on bison and introgression
Jim Robbins of the NYT has written a long article about genetic introgression of cattle genes into bison populations. The article is mainly concerned about management, and wildlife managers are trying to minimize the proportion of cattle genes in their conserved herds:
Over time, cattle genes have spread into many of the remaining herds of American bison. Since the late 1990s, Dr. Derr and his graduate students have traveled to public and private bison herds around the country, taking blood samples. They have concluded that the vast majority of the 300,000 or so bison in the United States are hybrids, though they look like pure bison. Fewer than 10,000 bison are genetically uncontaminated.
The whole idea of "genetic contamination" implies that there is something bad about this genetic introgression. But we can guess that the cattle genes don't intrinsically reduce fitness, since bison with cattle genes have been greatly increasing in numbers. And these introgressed herds are unlikely to be fixed for any cattle genes, so the original bison alleles still have every chance to compete with the cattle alleles. In other words, the cattle introgression has introduced variation into bison, some of which might be adaptive.
As you can tell, I'm not very sympathetic to the idea that we should prevent "genomic extinction" by insisting on some kind of genetic purity. It seems to me that we want to retain as much variation in our conserved populations as possible, so that they can adapt to changing climatic conditions in the future. We can't predict which alleles will be adaptive.
The geneticists in the article worry that cattle genes will make the bison susceptible to cattle-borne diseases like Texas fever. But making a large herd of genetically uniform bison is hardly the way to prevent disease!
Now, a history of selection for docility on ranches is of more concern:
"Ranchers might get rid of a cantankerous bull, for example," said Curt Freese, a biologist who directs Great Plains bison restoration for the World Wildlife Fund. "Breeding bison to be docile and meaty are the kinds of things that affect the wildness of the bison."
But it's unpredictable what behavioral traits will adapt bison to a conserved herd, which after all must be smaller and occupy a lot less space than many of the ancestral bison herds. They may end up more docile anyway, or just the opposite. I tend to think that selection will sort all this out.
Managers of these herds must also keep a wary eye on hybridized invaders. In Yellowstone, officials found a domestic bison that had wandered into the wild population from a neighboring ranch. And Wind Cave National Park is adjacent to Custer State Park, where the animals are hybridized.
The new approach may change other aspects of management, as agencies move from managing the species to managing the genetics. Dr. Derr is involved in a study, for instance, of whether the hunting of the bison that leave Yellowstone might be selecting certain behaviors from the population because animals that migrate are targeted.
This kind of selection is unavoidable in conserved populations, and might even be desirable -- they do, after all, want to stop the bison roaming out of the park. Roaming out of the park is one of the more noticeable bison phenotypes. I'm more worried about all the selection that is happening but doesn't have obvious effects.
This seems like a good doctoral project for somebody: how do the introgressed bison compare behaviorally with "genetically pure" bison? And the all-important question: how does mean fertility compare between these herds? They've both historically grown very rapidly, but does one maintain higher mean fitness than the other? Are there more animals in the Custer herd that fail to reproduce?
Anyway, there was no way to quantify the introgression until recent molecular techniques made it possible, and Ted Turner and others were happy to breed large bison herds that contained introgressed cattle genes. The only difference now is that wildlife managers know that some herds are "more pure" than others. But making conservation decisions on "purity" seems less relevant than fitness, which they still don't know much about because it's harder to measure. There is a presumption that the originally bison alleles will be more fit, but today's conserved situations are very different from those faced by ancient bison. And the historic bison -- the ones shot up by Buffalo Bill -- were facing a very novel environment compared with their ancestors.
The best we can hope for is a capacity for adaptation, which will maximize the chance of survival. In that context "genetic purity" is less important than genetic variability.
Aurochsen genes in today's cattle
Cattle are my favorite comparative model for Pleistocene human evolution, not because I think we necessarily share the same pattern of species and subspecies interactions, but because interbreeding and introgression are so evident among populations that are separated by strong local adaptations. Greg Cochran and I went into some detail about recent cattle phylogeny in our 2006 PaleoAnthropology paper. So I try to follow current research into cattle phylogeography, to see what other interesting things turn up.
The current Current Biology has a brief paper by Alessandro Achilli and colleagues, who sampled complete mtDNA genomes from recent European and Near Eastern cattle:
Archaeological and genetic evidence suggest that modern cattle might result from two domestication events of aurochs (Bos primigenius) in southwest Asia, which gave rise to taurine (Bos taurus) and zebuine (Bos indicus) cattle, respectively [1], [2] and [3]. However, independent domestication in Africa [4] and [5] and East Asia [6] has also been postulated and ancient DNA data raise the possibility of local introgression from wild aurochs [7], [8] and [9]. Here, we show by sequencing entire mitochondrial genomes from modern cattle that extinct wild aurochsen from Europe occasionally transmitted their mitochondrial DNA (mtDNA) to domesticated taurine breeds. However, the vast majority of mtDNAs belong either to haplogroup I (B. indicus) or T (B. taurus). The sequence divergence within haplogroup T is extremely low (eight-fold less than in the human mtDNA phylogeny [10]), indicating a narrow bottleneck in the recent evolutionary history of B. taurus. MtDNAs of haplotype T fall into subclades whose ages support a single Neolithic domestication event for B. taurus in the Near East, 9-11 thousand years ago (kya).
It is somewhat hard to believe that the mtDNA would be selectively neutral in newly-domesticated cattle, considering their growth and metabolic requirements had radically changed. So I would hold out the possibility that the strong standardization on a single T haplogroup in West Asian cattle may be a direct consequence rather than a side effect of domestication.
The current locations of the introgressive mtDNAs were interesting:
However, the tree also reveals exceptions that radiate much earlier than the T node. MtDNAs #98 and #99 harbour identical sequences (both from the Cabannina - an endangered breed from Liguria, northern Italy) belonging to a novel haplogroup (Q) whose ML time estimate from the QT node is 52.2 ±Â 8.0 kya. Sequence #100 radiates even earlier from the PQT node (74.4 ±Â 9.7 kya) and was detected in one animal from Korea, generically classified as 'beef cattle'. Strikingly, the control region of this mtDNA harbours the mutational motif of haplogroup P -- the marker of the extinct aurochs of Northern and Central Europe [8].
Those "introgressive" haplotypes really are not very divergent from the main mtDNA variation of B. taurus -- for instance, European aurochsen would appear to have been relatively genetically homogeneous compared to human mtDNA.
References:
Hawks J, Cochran G. 2006. Dynamics of adaptive introgression from archaic to modern humans. PaleoAnthropology 2006:101-115. Open Access (PDF)
Achilli A and 21 others. 2008. Mitochondrial genomes of extinct aurochs survive in domestic cattle. Curr Biol 18:R157-R158. doi:10.1016/j.cub.2008.01.019
Breeding nutritional Neanderwheat
On the topic of introgression, this article by Reuters' Will Dunham is a good illustration:
A team led by University of California at Davis researcher Jorge Dubcovsky identified a gene in wild wheat that raises the grain's nutritional content. The gene became nonfunctional for unknown reasons during humankind's domestication of wheat.
Writing in the journal Science on Thursday, the researchers said they used conventional breeding methods to bring the gene into cultivated wheat varieties, enhancing the protein, zinc and iron value in the grain. The wild plant involved is known as wild emmer wheat, an ancestor of some cultivated wheat.
Introgression between domesticated crops and their wild relatives is one of the most common ways to introduce desirable traits into agricultural production. For the most part -- even when they are classified as different species -- domesticated crops can be crossed with wild progenitors.
Emmer wheat is itself a tetraploid, presumed to be a hybrid of two wild diploid grasses. Tetraploidy (and other -ploidies) come to mind when talking about plant hybrids, because it often happens that new plant species originate from such crosses. There's nothing so exotic about emmer-domesticated wheat introgression, since wheat is also tetraploid. The ability to breed in characteristics is simple Mendelism:
"We didn't do it by genetic modification. The normal wheat crosses perfectly well with the wild wheat. So we just crossed it after normal breeding," Dubcovsky said.
Breeders can take the selection coefficient all the way up to 100 percent if they want, and so ensure the fixation of a desirable allele like this one. Natural popluations usually don't have this privilege -- and advantageous alleles are often lost, despite being favored by selection. A process carried out methodically by breeders reduces to a scattershot in nature. But it is an orderly scattershot in one way: the most strongly selected alleles have the highest chance of making it.
The inevitability of introgression
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.
References:
Hawks J, Cochran G. 2006. Dynamics of adaptive introgression from archaic to modern humans. PaleoAnthropology 2006:101-115. Free full text
Howler hybrid hunting
Alouatta palliata and Alouatta pigra are sympatric in parts of their ranges, and they give rise to visibly obvious hybrids. Liliana Cortés-Ortiz and colleagues sampled some DNA to figure out how permeable this hybrid zone really is.These patterns imply that the direction of hybridization and subsequent backcrosses is strongly biased. Only crosses between A. pigra females or hybrid females carrying the mitochondrial haplotype of A. pigra and A. palliata males or hybrid males with the Sry gene of A. palliata occur and give rise to female offspring (Figure 3). However, no male hybrids with the Sry gene of A. palliata were observed and so, in accordance with Haldane's rule (HALDANE 1922), the data strongly suggest that the aforementioned crosses fail to produce viable males. Furthermore, on the basis of the low probability of detecting only the mtDNA haplotype of A. palliata in 12 adult hybrid individuals, A. palliata females and A. pigra males or hybrid males either mate infrequently or typically fail to produce viable offspring. Nonetheless, the genotypes of the hybrid infant and its suspected parents imply that this infant (S157, Table 2) was produced from a backcross between a male hybrid (S154, Table 2) and a female A. palliata. This demonstrates that such matings occur and that female offspring are produced. However, because no adult females were observed with the mitochondrial haplotype of A. palliata, we suspect that such crosses are uncommon or this infant is either infertile or will not survive to reproductive age.
Yes, while J. B. S. Haldane was otherwise occupied formulating the mathematical account of genic selection, he took time off to generalize about interspecific hybridization.
These authors have previously estimated a divergence date between A. palliata and A. pigra of 3 million years. The two species are almost entirely allopatric, with small areas of overlap at the edges of their ranges. A. pigra lives in the Yucatan and adjacent areas of Mexico, Belize, and Guatemala; A. palliata lives in surrounding areas of Mexico, Honduras, and further south all the way to Ecuador. So, the range of A. pigra (black howlers) makes a sort of wedge in between two areas inhabited by A. palliata (mantled howlers). And A. palliata is exceptionally cosmopolitan compared to the endemic A. pigra.
How is it that they came to be split up this way? Amrei Baumgarten (2006) notes that the two species have similar vegetational preferences, despite earlier reports that the more cosmopolitan A. palliata more readily invaded disturbed habitat such as banana and mango plantations. Instead, he finds that the primary difference between the two species is cold tolerance: A. pigra can and does live at higher altitudes than A. palliata, ranging high enough that it must tolerate freezing temperatures:
My study identified an important geographic barrier separating the two species: the highland massif of northern Central America, including Sierra Madre de Chiapas, Mexico, central highlands of Guatemala and Honduras (Fig. 3.1). The region is characterized by montane coniferous forests, subalpine forests and semiarid inland valleys, all unsuitable habitats for Alouatta. Therefore, the continuous highland belt in Mexico and Guatemala seems to be a barrier between the species and it defines the southern limit of the range of Alouatta pigra. A. palliata borders these mountains in Mexico at lower elevations in Tabasco, Veracruz and the Isthmus of Tehuantepec (Fig. 3.1). It probably bordered the same massif along its Pacific side as indicated by historical records in Mexico (Estrada and Coates-Estrada 1984), Guatemala (Handley 1950) and El Salvador (Daugherty 1972; USNM specimens # 282795, # 282850). (Baumgarten 2006:18).
To explain further, most of the Yucatan is relatively low in elevation. But the A. pigra-A. palliata barrier is primarily in the highlands to the south of the peninsula. No howlers live at the highest elevations, and the species' ranges are not contiguous in this area. Baumgarten (2006) proposes an interesting historical scenario to explain the current ranges. In his proposal, global cooling cycles that began around 2.7 million years ago may have retracted the howlers' rain forest habitat further south, leaving a relatively cold-adapted population ancestral to A. pigra in the Yucatan. Recurrent isolation and expansion of the two species may have occurred during intervening glacial and interglacial cycles.
Keeping this biogeographic hypothesis in mind, the comparative anatomy of the two species is very interesting. James Dale Smith (1970) reviewed the osteological differences between mantled and black howlers. Both species are considerably dimorphic in body size, and also have the distinctive dimorphism in the throat apparatus (including the hyoid bone) that distinguishes all howler monkeys. A. pigra is substantially larger than A. palliata -- around 30 percent larger in mass (Ford and Davis 1992), with the difference more evident in males. This size difference is also reflected in the distinctive hyoid apparatus, which is much larger in the larger A. pigra males. The larger monkeys have more parallel tooth rows (contrasted with anteriorly converging rows in the smaller monkeys). Smith (1970) asserted that the most significant difference was in the maxillary molars. Large A. pigra skulls have molars that are roughly equal in size, while smaller A. palliata crania have molars that reduce in size from M1 to M3. The size differences are associated with a number of crown features, mainly related to simplification of the smaller M2 and M3 of the smaller monkeys.
Larger monkeys with larger, more complex molars, differences in throat anatomy, and greater cold tolerance, in contrast to a smaller, more cosmopolitan species, with the opportunity for gene flow during interglacials. They sound like Neanderhowlers.
(via Gene Expression)
References:
Baumgarten A. 2006. Distribution and biogeography of Central American howling monkeys (Alouatta pigra and A. palliata). MA Thesis, Louisiana State University.
Cortés-Ortiz L, Duda TF Jr, Canales-Espinoza D, García-Orduña F, Rodríguez-Luna E, Bermingham E. 2007. Hybridization in large-bodied New World primates. Genetics 176:2421-2425. doi:10.1534/genetics.107.074278
Cortés-Ortiz L, Bermingham E, Rico C, Rodríguez-Luna E, Sampaio I, Ruiz-García M. 2003. Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Biol Evol 26:64-81. doi:10.1016/S1055-7903(02)00308-1
Ford SM, Davis LC. 1992. Systematics and body size: Implications for feeding adaptations in New World monkeys. Am J Phys Anthropol 88:415-468. doi:10.1002/ajpa.1330880403
Smith JD. 1970. The systematic status of the black howler monkey, Alouatta pigra Lawrence. J Mammal 51:358-369.
Introgression encore
Although I've had a number of papers come out this year, there are two in particular that I've been working on for quite a long time. Both papers began their gestation in the summer and fall of 2005. Each of the two papers explicates a major pattern for the action of natural selection in human evolution -- to my mind, at least, the most important two. Each was a long project, requiring the integration of mathematical, theoretical and informatic resources, and researchers scattered across the country.
Both papers were submitted earlier this year to different journals, and in several instances revisions and decisions about them were made within a week of each other.
Now, the two papers are being published online, both within a week of each other.
The first to appear is our review of genetic introgression and modern human origins, now online in Trends in Genetics.
Gregory Cochran and I published a number of theoretical considerations about introgression last year (Hawks and Cochran 2006, described in this post). That paper included a very comprehensive review of adaptive introgression among natural populations, focused on mammals, citing more than 170 references. But we had relatively little to say about the genetic evidence for introgression in human evolution, because the key paper from Bruce Lahn's lab (Evans et al. 2006) had not yet been published.
We have included some of that evidence in our current review. It is a shorter, more compact paper than last year's. That means that it leaves out a number of details, but it allows us to bring the molecular evidence and population genetic theory together.
In that form, it is possible to discuss some of the interesting predictions we might make about Neandertal-human population dynamics. For instance, why are two of the candidate introgressive alleles related to the brain? Our final section, "What did archaics have to offer?" takes on this question:
Adaptive alleles from archaic humans present a paradox. We recognize archaic humans by their morphology, and their morphology has mostly disappeared. Therefore, if moderns still retain adaptive alleles from archaic humans, those alleles almost certainly were not correlated with traits that we recognize as archaic. Instead, they must be related to phenotypes that we cannot recognize easily in archaic human fossils.
This is a crucial fact. We already know that Neandertal anatomies disappeared. But what makes a "Neandertal" anatomical feature? Clearly, we recognize it precisely because it is rare today.
If we are going to look for introgressive alleles, we have to look outside of this acquisition bias. The brain is a promising area on this score -- we know little about its variation in fossil humans.
In the final section, we allowed ourselves some speculation about the dynamics of modern human origins and dispersal:
Cosmopolitan populations like modern humans are generally a threat to endemics, but this threat intensifies during range expansions and population growth. In endemic species, alleles that promote outbreeding can be selected merely because the cosmopolitan species is expanding, aiding the collapse of former reproductive boundaries. Certainly, the distinctive morphological adaptations of archaic humans lost some of their selective advantage with the increasing technical sophistication of the early Upper Paleolithic (35 000 - 15 000 years ago). This must especially have been true of populations like the Neanderthals, whose skeletal and muscular specializations required a high energy budget. In an adaptive context, Neanderthals and other archaic humans were like endangered endemics, suffering from relatively high mortality and high energetic costs. Possibly, the only remaining adaptive strategy for them was mixture with the more cosmopolitan modern humans.
This is of course speculative, but I think it is valuable because it attempts to place ancient human populations in the context of modern conservation biology.
We often read that various human groups were "endangered" at one time or another, including the Neanderthals. But I have not seen anyone take the next logical step, which is to discuss the ways that endangered species actually interact with their congeneric competitors. When the interaction between populations includes interbreeding, interesting dynamics may emerge.
Does this mean that humans and Neandertals were distinct species who intermixed by hybridization?
I wrote about that question last year, concluding:
There will never be any tidy solution to the species problem, because all species have unique evolutionary histories and constraints. Given these difficulties, the species status of archaic Homo populations is basically an intractable problem. That is, I am happy to suggest that archaic Homo populations correspond to classical subspecies, and as far as I know, no evidence strongly contradicts that position. But I can recognize that some people will never agree with this assignment. And from the perspective of their evolution, it just doesn't matter. Evolutionarily important gene flow occurs between mammal species, subspecies, and populations.
The last sentence is the most important point. Those who want to put Neandertals into a distinct species (Homo neanderthalensis) generally believe that there was no evolutionarily significant gene flow between them and modern humans. But the opportunity for evolutionarily significant gene flow is always there, irrespective of whether the populations are species, subspecies, or even genera. Remember Bos-Bison introgression.
You can't simply define the problem of Neandertal-modern interactions away by giving them different names. And in reference to the "paradox" pointed out above, there is no defining the problem away by pointing to morphological differences. If we recognize that Neandertals are hominids, that is quite enough to suggest that gene flow was possible between them and their contemporaries.
The only thing left is to quantify the amount. The genetic observations thus far suggest that a predominant fraction of the gene pool of living humans descends from a relatively homogeneous ancient population. Since Late Pleistocene humans were geographically differentiated, this means that one ancient population disproportionately expanded at the expense of others. Genetic comparisons allow us to infer that the expanding population was initially African. This expanding population received introgressive alleles, both from other African populations and from Eurasian ones.
But that was not the end of the story. Introgressive alleles succeeded or failed on the basis of selection on them. The expanding population continued to grow in numbers. And the stage may have been set for something even more interesting...
More reading
"Why introgression?" discusses why introgression is a useful concept, compared to the simpler "gene flow."
"Introgression and microcephalin FAQ" addressed the MCPH1 genealogy.
"Neandertal introgression, anatomically" reviewed the paper by Soficaru et al. (2006) on the Pestera Muierii skull.
"The inevitability of introgression" announced and gave some details from our 2006 paper.
References:
Evans PD, Mekel-Bobrov N, Vallender EJ, Hudson RR, Lahn BT. 2006. Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc Nat Acad Sci 103:18178-18183. doi:10.1073/pnas.0606966103
Hawks J, Cochran G. 2006. Dynamics of adaptive introgression from archaic to modern humans. PaleoAnthropology 2006:101-115. Open access
Hawks J, Cochran G, Harpending HC, Lahn BT. 2007. A genetic legacy from archaic Homo. Trends Genet (early online) doi:10.1016/j.tig.2007.10.003
"Neanderthals in our midst"
SEED is running a good article by Lee Billings combining the Muierii paper and the MCPH1 paper.
What about species?
A key issue (at least for some paleo folks) is whether the term "introgression" gives aid and comfort to the idea that Neandertals were a distinct species from us. To the extent that we rely on hybrid zones to account for the interaction, it sure looks like we are talking about the interaction of different species. If we are really talking about subspecific interactions, then we shouldn't really be using the term "hybrid".
Even Wikipedia describes introgression as the movement of a gene "from one species into the gene pool of another" by backcrossing.
Now, what do we know about whether Neandertals and modern humans were different species?
- Speciation in primates, from commencement of prezygotic isolation to full postzygotic isolation, has taken between 1 and 4 million years to occur, considering pairs of living primate sister taxa (Curnoe et al. 2006).
- Mitochondrial DNA suggests that modern humans and Neandertals derived from a single ancestral population at most 250,000 - 500,000 years ago (the population divergence time consistent with a 350,000 - 700,000 year genetic divergence).
- Craniometrics suggest that Neandertals and modern humans were more different than many primate subspecies pairs (Harvati et al. 2004).
- Nonmetrics suggest that archaic Homo populations were no more genetically differentiated than human races (Hawks and Wolpoff 2001).
- Early Upper Paleolithic Europeans had a relatively high proportion of traits otherwise common in Neandertals.
I could go on with a few more, but you get the point: Despite their morphological idiosyncracy, genes and comparisons with other primates reject the hypothesis that modern humans and Neandertals were reproductively isolated. In that context, the morphological differences among archaic humans are (presumably) largely adaptive, and the reason that modern humans don't look like archaic humans is a matter of their different adaptations.
But if we aren't talking about different species of Homo, at least not in the sense of complete reproductive isolation, then why are we talking about introgression?
The thing is, introgression and species boundaries have emerged as different problems in the literature on genetics and biogeography.
For example, here's a passage from Dowling and Secor's (1997) review of introgression in animals:
Hybridization is defined as "the interbreeding of individuals from two populations, or groups of populations, which are distinguishable on the basis of one or more heritable characters" (Harrison et al. 1993, p. 5), and introgression is "the permanent incorporation of genes from one set of differentiated populations into another, i.e., the incorporation of alien genes into a new, reproductively integrated population system" (Rieseberg and Wendel 1993, p. 71) (Dowling and Secor 1997:595).
It is worth noting that this definition involves populations that could be defined as phylogenetic species -- populations differentiated by at least one morphological character. Of course, phylogenetic species are not evolutionary or biological species, but concerning the definition of fossil taxa like Neandertals, this is precisely the point at issue!
Another passage from Rhymer and Simberloff (1996:84) approaches the question from the standpoint of conservation genetics:
We define "hybridization" as interbreeding of individuals from what are believed to be genetically distinct populations, regardless of the taxonomic status of such populations. "Hybridization" most commonly refers to mating by heterospecific individuals but has been applied to mating by individuals of different subspecies and even of populations that, though not taxonomically distinguished, differ genetically. Arnold et al. (1991) suggest restricting "hybrid" to matings between species and using "intergrade" for matings between subspecies and "cross" or "interbreed" for matings between individuals of geographically distinct populations. Although such distinctions might clarify future discussions, all these terms seem so widely used in the literature for matings at every taxonomic level that they are unlikely to be restricted. Instead one must depend on accurate taxonomic description of the entities between which mating occurs.
Introgression is gene flow between populations whose individuals hybridize, achieved when hybrids backcross to one or both parental populations. Beyond F1 hybrids, the point at which an individual is no longer viewed as a hybrid but rather as a member of one of the parental populations that has undergone introgression is arbitrary. A hybrid swarm is a population of individuals in which introgression has occurred to various degrees by varying numbers of generations of backcrossing to one or both parental taxa, in addition to mating among the hybrid individuals themselves. Hybridization need not be accompanied by introgression; for example, offspring of hybrid matings might all be sterile. Introgression can be unidirectional, with backcrossing to one parental population only (Rhymer and Simberloff 1996:84, citations omitted).
From these passages, it becomes clear why "introgression" is used so broadly: Biologists still don't agree on what constitutes a species! This should be no surprise -- the species problem is one of the fundamental issues in biology. But it is useful to remember that fossil species are not an exceptional case.
The problem is not with defining "hybrid" or "introgression." The problem is with defining species.
The different definitions of the term "hybrid" evident in those passages also carry a lot of baggage. For the conservation geneticist, "hybridization" may mean something more or less undesirable -- something that ought to be avoided. From the point of view of defining species, "hybridization" ought to be unusual -- out of the ordinary. From the point of view of evolutionary genetics, "hybridization" may just mean reticulation -- a process making it possible for genes to move between populations that are more or less isolated. It is not just very common to talk about trans-subspecies matings as "hybridization" -- it is ubiquitous.
And for that matter, the classical genetics definition of "hybrid" has nothing whatever to do with species. Remember hybrid corn? Mendel's peas? Hybridization is about crossing lines maintained by selection. And lest we forget the etymology of "hybrid", the original Latin hybrida was the offspring of a tame sow and a wild boar. In other words, all this disagreement about the relevant taxonomic level for "hybridization" is highly subject-specific, and emerges from the conservation literature rather than from genetic principles.
I would make two observations. First, the threshold for "introgression" is arbitrary. For example, Ellstrand et al. (1999) define "introgression" as the gene flow between taxa (implying species), but discuss it mainly in connection with introgression from domesticated to wild plants, where the "species" distinction is based on the history of domestication. In the conservation literature, "introgression" concerns the detection of "alien genes", largely from invasive or cosmopolitan species (e.g., mallard genes entering American black duck populations). In the last several years of journals like Molecular Ecology there have been one or two papers per issue dealing with introgression between natural populations of animals -- mainly documenting the apparent movement of alleles between classical subspecies and morphospecies.
References to introgression are accelerating in part because of the prominent role of mitochondrial systematics in the 1990's -- people are discovering that mtDNA phylogenies don't tell the whole story of gene flow between wild populations. This is no surprise at all from an evolutionary perspective, but it has pretty clear application to the systematics of Homo, where much (so far) has ridden on the proposition that mtDNA is an accurate guide to population histories.
My second observation is that the movement of adaptive alleles from one population to another is especially likely to take the form of introgression. Genes under selection doesn't respond to population boundaries in the same way as neutral genes. The way that most people have framed the issue of the archaic-modern transition is in terms of neutral genes and population movements. But this is a poor model for the behavior of adaptive genes. This means that most people's notion of ancient population dynamics is different from the expectations of population genetics. Like the problem defining "hybrids", the mismatch of models and theory is deeply rooted in the species problem: If you think Neandertals were a different "species" from moderns, then you probably think it must follow that there was no "important" genetic interaction between the two populations.
Genetics over the past couple of decades has shown that species "boundaries" are permeable, that postzygotic isolation in mammals takes millions of years, that the flow of adaptive alleles across species boundaries in mammals is ubiquitous, and that reticulate evolution between mammalian genera is far from rare.
We could just conclude (as some of my readers have) that biology just got the species problem "wrong", and that we should be talking about subspecies instead of species. Maybe we should limit species to "really, really" isolated populations, or populations that "diverged at least 4.5 million years ago", or some other metric. There may be a lot of truth in that, but if wolves and coyotes are subspecies, cattle and bison are subspecies, and all baboons are subspecies, then I think we have to abandon the idea that species are a meaningful unit of adaptation! More to the point, most biologists use subspecies to mean "allopatric", or at least "peripatric" populations, yet hybridization and introgression commonly occur among sympatric (yet partially isolated) populations.
(UPDATE: A reader let me know that it sounds like I am actually proposing that wolves and coyotes are subspecies here. Quite the opposite -- wolves and coyotes are good species for reasons of their clear adaptive differences in sympatry. My -- possibly botched -- point is that the problem is not that the species concept is wrongly applied here; the problem is that the correct application of the species concept still gives us species that interbreed a lot! If you try to fix the problem by applying a different species concept, then we end up with a lot of very strange looking "subspecies".)
I take a different tack. There will never be any tidy solution to the species problem, because all species have unique evolutionary histories and constraints. Given these difficulties, the species status of archaic Homo populations is basically an intractable problem. That is, I am happy to suggest that archaic Homo populations correspond to classical subspecies, and as far as I know, no evidence strongly contradicts that position. But I can recognize that some people will never agree with this assignment. And from the perspective of their evolution, it just doesn't matter. Evolutionarily important gene flow occurs between mammal species, subspecies, and populations.
As you can probably tell, I have become greatly disgusted by the species problem. My reasons for this extend beyond the present discussion, but in any event I think it is a hopeless task to build any kind of consensus about the nature of fossil species.
So we have to begin by identifying patterns of interaction and gene flow. Introgressive gene flow is then a category of gene flow between differentiated populations. In particular, introgression is extensive (as opposed to merely local) and permanent (as opposed to ephemeral). Because of this, the pattern of introgression is fairly likely to involve adaptive alleles, but it need not do so. However, a widespread signature of interbreeding in neutral (or even deleterious) alleles is very likely to reflect a higher level of gene flow than would usually be indicated by "introgression". Is this a distinction without a difference? I think it's a pattern, and one that has now been replicated by several genes. It remains to be seen if it is the dominant pattern, or whether a broader pattern of genetic similarities will emerge -- but keep in mind that I think another pattern is also at play that will help to explain much.
Finding evidence for introgression in genes like MCPH1 is basically the operational procedure by which people are now looking for introgression in natural populations -- with one exception: for extant populations, we can test the genes of both populations directly. For extinct archaic populations, we can have evidence of introgression only by inference, which means that we will likely miss many true instances of gene flow from archaic humans. This does raise the risk of valuing "introgression" more substantially than it may "deserve" -- in particular, that adaptive alleles like MCPH1 will get a lot more attention than other genes that may have more ambiguity.
But I think that evidence of introgression reinforces the hypothesis that modern humans emerged in an adaptive context, making use of adaptive variation from a widespread (possibly pan-Old-World) population of archaic Homo. It's one of the two main patterns in the evolution of modern humans.
References:
Harrison RG. 1993. Hybrids and hybrid zones: historical perspective. In: Hybrid zones and the evolutionary process, ed. Harrison RG. pp. 3-12. Oxford University Press, Oxford UK.
Rieseberg LH, Wendel JF. 1993. Introgression and its consequences in plants. In: Hybrid zones and the evolutionary process, ed. Harrison RG. pp. 70-109. Oxford University Press, Oxford UK.
Dowling TE, Secor CL. 1997. The role of hybridization and introgression in the diversification of animals. Ann Rev Ecol Systemat 28:593-619.
Ellstrand NC, Prentice HC, Hancock JF. 1999. Gene flow and introgression from domesticated plants into their wild relatives. Ann Rev Ecol Systemat 30:539-563.
Rhymer JM, Simberloff D. 1996. Extinction by hybridization and introgression. Ann Rev Ecol Systemat 27:83-109.
John Hawks Department of Anthropology
University of Wisconsin—Madison
Copyright © 2007 John Hawks