Hello Dr. Hawks, I understand your a busy man so my question will be brief. I learned in my biology class that two different species can not interbreed and produce fertile offspring. If this is the case, how can we carry 4% Neanderthal genes? If they were a different species we should have not been able to crossbreed. Could you please explain this if you have time?
They weren't a different species.
Within paleoanthropology, we often witness taxonomic clashes. Species that were named on the basis of a single fossil are later discarded. Now with genomics, we can see that the fossil "species" we named for Late Pleistocene humans in fact extensively interbred with each other. I have found it interesting over the last year to talk with artist reconstructors about the way they incorporate this information into their works.
I was pointed to an essay by James Prosek, a biological artist best known for his books illustrating fish (James Prosek's Amazon page). As he matured as an artist, he discovered that the lines in nature are sometimes blurry, and science sometimes changes much more than nature. The essay was originally printed in the March 2008 issue of Orion ("The failure of names").
As I painted trout through my late teens, major shifts in trout taxonomy were taking place. Through genetic analysis, which was fairly new in the early ’90s, it was discovered that rainbow trout (from the Pacific coast) and brown trout (introduced from Europe) were not as closely related as once thought. The genes showed that the rainbow trout was more closely related to Pacific salmon, fishes that die when they spawn, of the genus Oncorhynchus. The brown trout was more closely related to the Atlantic salmon, and remained in the genus Salmo. The native trout of my home state, Connecticut, the brook trout, was actually a whole separate genus, Salvelinus, more closely related to the Arctic char than to the rainbow or brown trout. Technically, it was no longer correct even to call the book I was working on Trout. I found myself wanting to ignore the namers because they were getting in the way of my own personal vision.
The essay recounts how Prosek surpassed this clash with taxonomy. He travelled extensively during the research for his second book, Trout of the World, and explored the variability within (and continuities among) taxonomic groups. His artistic process led him to experiment with visual forms that could communicate both the natural variation and science's
After drawing curvilinear lines, first emanating from the points on the body of a seahorse, I realized the lines were helpful as visual aids to point out particular parts of a creature that I wanted to bring attention to. The lines activated the space around the animal in a satisfactory way, erasing the need for the name to be written beneath. In this way, the lines became a very personal visual taxonomy, replacing the lingual one.
(via Karen James)
Last week, Science ran a couple of items by Ann Gibbons that give further perspective on the discoveries last year that Neandertals and Denisovans both contributed to the ancestry of recent human populations. The sidebar piece, titled, "The species problem," raises the taxonomic question:
Our ancestors had sex with at least two kinds of archaic humans at two different times and places—and those liaisons produced surviving children, according to the latest ancient DNA research (see main text, p. 392). But were the participants in these prehistoric encounters members of separate species? Doesn't a species, by definition, breed only with others of that species?
I get the most awesome quote in the short article, because I get to defend the Biological Species Concept!
Gibbons describes this as a "minority view among paleoanthropologists." I can't disagree: Get a dozen paleoanthropologists in a room, and I bet only 1 or 2 will seriously propose that we could apply BSC to hominins.
This would be sort of understandable, if we were limited to the evidence of 15 years ago, with no genetics. It just wasn't really possible to test the hypothesis of interbreeding among populations, not at the scale at which we can today. There was always skeletal evidence that suggested Neandertals had contributed to later populations, as many of us pointed out repeatedly. But it was hard to quantify the phenomenon, and without quantification, it was possible for people to argue that interbreeding had been "evolutionarily insignificant".
Paleoanthropologists have instead held species concepts that did not use interbreeding as a primary criterion. Many adopted Cracraft's Phylogenetic Species Concept, or Wiley's treatment of Simpson's Evolutionary Species Concept. Both of these define species in terms of morphological characters visible to the systematist, although they differ with respect to the pattern that justifies recognizing a species.
Much of this is just ridiculous now. Genetic evidence shows a substantial amount of interbreeding between these Pleistocene groups. Lots of living humans trace more than a couple of percent of their genomes from some ancient non-African population; some may derive more than 8 percent of their ancestry from such populations. That's not rare hybridization. With this kind of evidence, we can apply the BSC.
One hangup: maybe we can't prove that our Neandertal ancestors contributed genes in proportion to their population numbers. Maybe a large fraction of their genes had a fitness disadvantage in the later population. But this is a hypothesis, not a fact. Any estimate of the fitness of Neandertals in mating with their non-Neandertal contemporaries has to take account of the demographic growth of later populations, including selection on new gene variants. We know for a fact that some Neandertal genes are today very common -- for example, one 100-kilobase region occurs at a frequency of 28 percent outside of Africa. Any assignment to a species is a hypothesis, provisional on finding new facts to refute it. For the moment the facts point to them being the same species as us.
What do we do with a population like the Neandertals, or the Denisovans? Each was more genetically distant from the average living human than members of living populations are from each other. Each evolved during a long period of isolation or strongly restricted gene flow from each other and from sub-Saharan Africans. Still, the level of genetic difference among these populations was comparable or less than that separating populations of great apes that historically have been recognized as subspecies. So that's what I would call them. Subspecies of Homo sapiens.
As a postscript, I think that whoever came up with the idea of "Denisovans" as a population name has done us a tremendous favor. The great benefit of the name, "Neandertals", is that we could talk about them without trotting out a taxonomic name. Now we have something similar in eastern Eurasia.
Also Jerry Coyne, coauthor of Speciation, discusses the issue.
John Wilkins is an expert on species concepts in biology; he has written a short piece for wide circulation on the topic which is archived at his blog: "How many species concepts are there?" I just lectured on that topic in my introductory course, and it's good to have such an accessible introduction to the topic. In this case, Wilkins focuses on the philosophy -- why are there different concepts, and what do we mean when we say that?
In a new paper, Yohannes Haile-Selassie and colleagues describe new hominin fossils from Woranso-Mille, Ethiopia. A good thing: It gives somebody like me a rationale for describing early hominins from the point of view of Hadar. You see, Hadar is the first sample to include a really complete skeletal representation. You can present earlier sites as a series of "firsts", but that's kind of misleading. Now, the simple Ardi-Lucy comparison carries a lot of water for teaching early hominins, and if we can assume that the samples intermediate in time are mostly A. afarensis-like, so much simpler.
Oh, and one more really good thing: Standard dental measurements are provided in the text of the paper. Thank you, AJPA! We may not get all the specimens, but at least we can check the statistics.
But there's a chance that things are not so simple as they seem, that there are mysteries still waiting to jump out of this sample and scare us at night. I imagine that some people are less than thrilled about this paper, which explicitly rejects the reality of one Leakey-named species and ignores another into obscurity. One might expect me to welcome our new lumping taxonomic overlords. And yet, this little paper doesn't provide some information and comparisons that seem like curious omissions. Which makes me wonder...
The fossils from Woranso-Mille are between 3.6 and 3.9 million years old -- basically older than Laetoli and younger than Kanapoi. Since the Laetoli sample is A. afarensis, and the Kanapoi sample is A. anamensis, we can expect that the Woranso-Mille sample would say something about how these two species were related to each other. The fossils might be one species or the other, they might be intermediate between them, or they might even be something altogether different.
The sample as described is almost exclusively dental, with only a fragment of mandible and another of maxilla tossed in the mix.
Some readers may have been under the impression there's more at this site, and indeed I am as well. I think I've even seen them for 500 milliseconds at a meeting once upon a time. Of course, maybe that was a dream. Much in paleoanthropology seems to be fading into a unicorn fairyland these days...
Wait a minute! It's for occasions like this that I have a blog! As it turns out, I took some notes on Woranso-Mille back in 2007.
Now, I have to warn you: These notes were so snarky that I didn't dare hit "publish". But there's no sense shirking responsibility for them now. Next thing I know, some crank will be hacking my server to bring all this snark into the open!
Along with many other people, I got to see the hominids from Woronso-Mille this spring. Then again, see is probably an overstatement. I mean, when you see something, generally light waves from the objects actually have time to strike your retinas. I couldn't swear that anyone actually had that experience during Yohannes Haile-Selassie's talk to the Paleoanthropology Society. Sure, there was a subliminal impression that the pictures were there. And yet, Powerpoint and automatic timing can do magical things.I experimented a bit later, to try to estimate just how long the pictures had been up there. The 500 millisecond setting seemed about right. Definitely automated. Too short for microsaccades to bring in the edges of the fossils properly. And many of them were in situ photos, with a lot of brown-on-brown. Hard to pick out edges at all, and some edges were still in the ground.
I mean, really, work out the time that Santa Claus has to spend in each kid's house on Christmas Eve to make it to all the world's children in one night. That's the kind of time we're talking about.
See what I mean. I mean, that's over-the-top snark. Still, it's better material than I usually work with, so I can't for the life of me figure out why I didn't publish it. It goes on:
Don't get me wrong. I think it's entirely appropriate to hide the images, dim them, heck, don't even show them if they don't want to. Think of all the yokels like me who could tell immediately from a decent picture whether the fossils were A. afarensis or not, and go shooting off their servers to the rest of the world. Hard work in the field, with the high risk of failure, deserves every possible reward -- certainly the right to take the necessary time to make a careful analysis. I hardly ever make any comments after I hear a public talk, unless the material is already well-known or described elsewhere. And there are other practical reasons not to talk about it -- for one thing, people sometimes change their minds!
But why should I feel any compunction about prognosticating on fossils that are announced in the press? Hey, if they didn't want the attention, they wouldn't have a press conference, right? I'll bet they didn't make the press sit through the half-second slide show!
Haile-Selassie announced several of the Mille fossils in 2005, notably the partial skeleton -- of which they are still trying to find more parts. At the time, I wrote about it, Rex Dalton wrote about it, Ann Gibbons wrote about it, twice, the AP wrote about it. Good times were had. Oh, those good times. Sure, no descriptions. Granted, in situ brown-on-brown photographs with buried edges. But good, good times.
How could I have forgotten those good times?
Now, there is a second press offensive underway. The best stories are at National Geographic News and The Cleveland Plain Dealer (Haile-Selassie's in Cleveland). It's an important site, with dozens of specimens.
Hey, maybe they're like the Laetoli footprints and they rebury them when they're done looking at them. Kind of like catch-and-release.
All this was nearly three years ago. Which is a bit strange, considering that the current paper still doesn't include all the specimens. Assuming the 2007 illustrations were correct, the current paper doesn't even include all the Woranso-Mille dental specimens, as at least one mandibular dentition appears to have been omitted. It is, of course, possible that the news reports had the wrong picture.
Here are my 2007 thoughts on the matter:
We can probably answer this already: the National Geographic story includes a picture of the most complete mandible, and it looks an awful lot like LH 4, maybe with a more sloping symphysis. It's a rotten view - artistic, sure, but a lousy angle for comparison.
This mandible is not included in the current paper. It is pretty obviously the most diagnostic of the mandibular/dental specimens, if it's from Woronso-Mille. I wonder if National Geographic really may have credited the wrong photo to Haile-Selassie? Very strange. In any event, it's an important question since the sample of other postcanine teeth in the paper is generally 2-3 specimens. A missing postcanine dentition would make a lot of difference to our picture of the variation.
OK, continuing on:
But still, the teeth appear to fall into the Laetoli-Maka-Hadar sample, the postcanine rows diverge from each other, and the symphyseal morphology in A. afarensis is certainly variable enough to encompass this mandible. Really the only missing feature that would be helpful is the P3, but unless other specimens turn out to be outside the Hadar range, I would assume this is going to be assigned to A. afarensis.
Which does make me wonder how much the hidden mandible has driven the paper's conclusion. On the basis of the specimens they published, the majority of dental features seem to argue in favor of A. anamensis, as they explicitly write. They mention only a few "derived features" also present in later sites. Given the date, one might just as easily argue that these "derived" features were actually low-frequency variants heretofore unrecognized in the small A. anamensis sample, so that Woranso-Mille extends the range in that species while maintaining its overall anatomical pattern. The stealth mandible, if indeed it exists, looks more persuasive fitting in the pattern of A. afarensis.
The unanswered phylogenetic questions are chiefly about what other lineages there may have been at the time. Mille might answer that question if substantial hominid diversity were found there, or at least something really different from the other sites. But no apparent evidence of such diversity was apparent in the public lecture. Maybe there are surprises waiting, but this team in the past has argued pretty strongly for taxonomic conservatism.
On the other hand, this is what Haile-Selassie told the Cleveland Plain Dealer:
"The current hypothesis, which so many people seem to accept, is that they were ancestral descendents [sic, I'm assuming that's a misquote]- that anamensis gave rise to afarensis," Yohannes Haile-Selassie, expedition co-leader and anthropology curator at the Cleveland museum, said in a phone interview from Addis Ababa. "To test that, we need fossils. That's why we think these specimens are really, really important."
In their current paper, Haile-Selassie and colleagues conclude the following:
The Woranso-Mille hominids are significant for understanding the evolutionary history of early Australopithecus, particularly due to critical placement within a previously poorly known time period, 3.5 and 3.8 Myr. They are of paramount importance in testing hypotheses about the ancestor–descendant relationship between Au. anamensis and Au. afarensis. The Woranso-Mille hominids shed some light on whether Au. anamensis and Au. afarensis are two distinct species, or parts of a single evolving lineage undergoing morphological change through time. Dentally they are more similar to Au. anamensis from Allia Bay than to Au. afarensis from Laetoli. However, they also share some derived characters with Au. afarensis from Hadar and Laetoli. Based on the currently available evidence, the Woranso-Mille hominids are temporally and morphologically intermediate between the more primitive Au. anamensis from Allia Bay and the slightly derived Au. afarensis sample from Laetoli (Ward et al., 2001; Kimbel et al., 2006). They appear to potentially represent a transitional population within an anagenetically evolving Au. anamensis-Au. afarensis chronospecies (White et al., 2006; Kimbel et al., 2006) providing further support to the well-established hypothesis of ancestor–descendant relationship between the two species. To test this and other alternative hypotheses rigorously, and elucidate the evolutionary history of early Australopithecus, more complete fossil specimens are needed from the critical time period between 3.6 and 3.8 Myr. However, what appears to be evident with the discovery of new fossils spanning the 4- to 3.5-Myr interval is that morphological differences between Au. anamensis and Au. afarensis do not warrant a species level distinction (emphasis added).
Buh-zaaaaaaam! All your species are belong to us! Kenyanthropus? We won't even dignify it by using the word. A. anamensis? Sunk like the Bismarck.
The fundamental debate here is semantic. Everyone seems to agree that anagenesis (that is, gradual evolution over time) is a likely hypothesis for this lineage. Where they disagree is how to handle the taxonomy.
1. Strict cladists want to name species based on the appearance of unique features (that is, phylogenetic species), in which case A. anamensis is a species, A. afarensis is a later species with new characters, and very possibly we need to resurrect Praeanthropus africanus for the Hadar sample, even if it mostly overlaps, since it has a few characters never found earlier and represents a broader sample of postcranial anatomy, which is entirely unknown at earlier sites.
2. Strict users of a Wiley-like Evolutionary Species concept always place anagenetic lineages into one species. So, the single lineage hypothesis lumps A. afarensis and A. anamensis together. And as Haile-Selassie and crew go on to point out, we might even lump Ardipithecus, if it's the lineal ancestor of the later hominins.
3. Not-so-stickly people, which is most everybody, pretty much recognize species along with the crowd. A. anamensis has a history now. It's not just early A. afarensis, because, well, lots of people said so. And after all, you can tell the difference between them if you look carefully.
What's interesting (at least to me) is to read Kimbel and colleagues' 2006 paper, keeping in mind the "following the crowd" scenario 3. In this light, much of that paper is boundary defense. A. anamensis had already elbowed its way into the textbooks, and the paper recognizes the existing taxonomy without attempting any revision. But the demonstration of anagenesis within A. afarensis would be sure to provoke some strict cladists to name some more species -- a species for Hadar, for example. Kimbel and colleagues reiterated that anagenesis within A. afarensis is expected -- it's part of the species' literature, now. So the paper tried to draw two lines in the sand: on the one hand, A. anamensis is real; and on the other hand, no further distinction within A. afarensis is warranted. Taxonomic containment.
But, drawn in this way, both lines in the sand might be washed away by a single discovery. The present pattern of evidence is mostly dental and mandibular. Woranso-Mille may be only one postcranial specimen away from lacking a bunch of derived postcranial characters that are well-evidenced at Hadar.
After Ardi, I think this is a serious possibility because of the scope of postcranial innovations at Hadar that are not evidenced anywhere earlier. It could be that all the postcranial traits of Lucy and her kin are lineage-typical, going back all the way to Kanapoi (and don't forget the A. anamensis from the Middle Awash). But we don't know this. Given Ardi, it appears that the adaptive package appeared rapidly, after 4.2 but before 3.5 million years ago. It seems to me that there's every chance that A. anamensis, and possibly the Woranso-Mille sample, hadn't built the whole package yet.
Ah, now I've gotten down to the end of my notes. I think I'm starting to remember why I didn't put them up at the time:
While the evidence for bipedality in the earlier A. anamensis is not nearly so extensive as that in A. afarensis, nevertheless it is quite compelling, particularly the KNM-KP 29285 tibia. You'd get pretty long odds betting that the Mille pelvic bones looked very different from Lucy's. I have no information about the pelvis at all, certainly no photos, but it would indeed be a surprise for it to be outside the A. afarensis-A. africanus range of variation.
But then, all it would take is one funky-looking pelvis to throw the whole question of pre-4.0-million-year-old hominids wide open. So maybe we should hope that it's strange.
Well, we certainly got one funky-looking pelvis, didn't we? I'm beginning to think I should republish old notes more often. What are the chances that another funky pelvis is waiting to be published?
Could it be that Woranso-Mille could represent an intermediate postcranial form at 3.7 million years? That would be one good reason to nail down the question of anagenesis from the craniodental perspective.
I think we may already have a hint at the answer. It's a little hard to imagine that Haile-Selassie and colleagues would propose sinking A. anamensis if they already knew that their skeleton has a different postcranial anatomy than represented at Hadar.
There's one more thing worth mentioning: this paper doesn't include any discussion, comparison -- it doesn't even breathe the name -- of the other 3.5-million-year-old hominin. It's not just a skull; there is a sample of teeth from that unmentioned site, which of course may or may not represent the same taxon. Like a forgotten stepchild of paleoanthropology. Is it possible that peer reviewers have already forgotten it's existence?
When I wrote about what I'm wondering, well, this isn't the only paper to have recently omitted this obvious comparison. I'll have more on that little problem later on...
Haile-Selassie Y, Saylor BZ, Deino A, Alene M, Latimer BM. 2010. New hominid fossils from Woranso-Mille (Central Afar, Ethiopia) and taxonomy of early Australopithecus. Am J Phys Anthropol (in press) doi:10.1002/ajpa.21159
Kimbel WH, Lockwood CA, Ward CV, Leakey MG, Rak Y, Johanson DC. 2006. Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the hominin fossil record. J Hum Evol 51:134-152. doi:10.1016/j.jhevol.2006.02.003
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?
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.
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.
R. D. Guthrie, from p. 3 of "Bison evolution and zoogeography in North America during the Pleistocene," Q Rev Biol 45:1-15, 1970:
During the early history of Pleistocene paleontology in America it was not uncommon to give any horn core the status of a new species if it was slightly different from any other type that had been described; consequently the literature abounds with forms such as Bison regius, B. angularis, B. oliverhayi, B. rotundus, B. californicus, B. ferox, B. texanus, B. taylori, B. pacificus, B. sylvestris, and B. kansensis, which have since been lost in the sea of synonymy.
A new population that results from a speciation event is called a species. But although species result from a simple process, recognizing species in nature can be complicated. Biologists cannot travel in time to observe the speciations that resulted in today's diversity of life, so they must observe the reproduction of living organisms to determine the makeup of species. Paleontologists can find the fossil evidence of the ancestors of today's species, but they cannot observe whether those fossil organisms could reproduce with each other. Because scientists have different kinds of evidence about organisms, they use different concepts of species when testing hypotheses about their evolution.
The most obvious property that helps to define species is reproductive isolation. Biologists studying living animals often use the biological species concept, which envisions a species as a "group of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups" (Mayr 1942). It is the biological species concept that primatologists use to grapple with whether chimpanzees and bonobos are different species, for example, by observing the differences in their reproductive behaviors and the strength of geographic isolation between their populations.
The biological species concept has some important limitations for paleontology. Making use of the concept depends on observing the mating behavior and interbreeding patterns of animals in their natural environments, which is not possible with fossils of organisms that lived in the past. Other kinds of observations that paleontologists might gather, such as morphological differences between fossils, have no necessary value under this concept. Another limitation is that the biological species concept does not incorporate any idea of how species may change over time. Paleontologists study fossils that may be separated by hundreds of thousands of years of time. It is difficult to imagine such widely separated individuals as part of the same reproductive community, even if they were very similar to each other. Over such time periods, evolution can transform populations substantially. The biological species concept recognizes the genetic continuity within a species caused by gene flow, but it does not incorporate a view of species existing over evolutionary time. For these reasons, paleontology requires a different kind of species concept.
The phylogenetic species concept is an attempt to define species by their relationships to other species. Instead of trying to determine the reproductive boundaries of populations, scientists using the phylogenetic species concept attempt to uncover their genealogical relationships. A group of individuals that includes all the descendants of one common ancestor, leaving no descendants out, is called a monophyletic group.
Paleontologists Niles Eldredge and Joel Cracraft devised a species concept called the "Phylogenetic Species Concept," intended to apply to circumstances in which reproduction or isolation among organisms could not be observed. Under this concept, a species is "a diagnosable cluster of individuals within which there is a parental pattern of ancestry and escent, beyond which there is not, and which exhibits a pattern of phylogenetic ancestry and descent among units of like kind" (Eldredge and Cracraft 1980:92).
Key to the phylogenetic species concept is the idea that species must be "diagnosable." In other words, members of the species should share a combination of characteristics that other species lack. To look for the unique features that define a phylogenetic species, paleontologists must perform systematic comparisons with other related fossils or living species. These aspects of the concept make it widely applicable in paleontology.
But the phylogenetic species concept is not without its problems. Because the concept defines species based on morphology, without explicitly referring to populations or reproductive boundaries, it does not apply well to cases where morphologically different populations are connected by gene flow. Morphological variation among populations is not uncommon within living species. Humans today are a species with substantial morphological variation from continent to continent. Humans on different continents are not reproductively isolated, and their variation is largely distributed as clines over large geographic distances. Yet a paleontologist who had only a few fragmentary specimens from each continent would not necessarily know the pattern of variation, and many features of his specimens would appear to be unique. What would the paleontologist make of the high nose of a European specimen, the forward-facing cheeks of an Asian fossil, or the strong browridge above the eye orbits of an Australian, each taken randomly from their variable populations? By applying the phylogenetic species concept, a paleontologist would probably conclude that the different continents were homes to different human species.
Thus, because the phylogenetic species concept does not identify species based on the reproductive boundaries between them, it may have the effect of identifying populations connected by gene flow as different species. For this reason, a phylogenetic species as defined by a paleontologist may not correspond to a real prehistoric population that was the product of a speciation. Some paleontologists do not view this potential conflict as a problem, because identifying species based on unique characteristics will create as full as possible a systematization of the evolution of new features. Assuming that the number of ancient species was very large, and the number of fossils representing each of them is very small, then paleontologists can hardly hope to identify every speciation event in the past. The phylogenetic species concept may therefore provide a better approximation of the number and diversity of species that existed than other alternatives.
On the other hand, identifying populations connected by gene flow as different species can be a significant problem for paleontologists who take a greater interest in the processes of evolution than in the diversity of species in the past. Gene flow is a significant force shaping evolutionary change within populations. Moreover, evolution may cause a single species to change over time, possibly acquiring new unique features without any division of a species into separate reproductively isolated populations. Some paleontologists approach these difficulties by altering their view of the evolutionary process. If speciations can happen as a transformation of a single population in addition to the appearance of reproductive boundaries between populations, then a single evolving population may over time comprise several phylogenetic species. Or if most evolutionary change happened at the time of speciation, as asserted by the concept of punctuated equilibrium, then the phylogenetic species concept might more closely approximate the actual pattern of speciations in the past. But without such assumptions, the phylogenetic species concept's problems sometimes create a stumbling block for some paleontologists in attempting to understand the evolutionary process.
The evolutionary species concept combines the genealogical basis of the phylogenetic species concept with the genetic basis of the biological species concept. An evolutionary species is a lineage of interbreeding organisms, reproductively isolated from other lineages, that has a beginning, an end, and a distinct evolutionary trajectory (Wiley 1978). The beginning of a species' existence is a speciation, as a population becomes reproductively isolated from a parent population. The end of a species occurs either with extinction or with the branching of the species into one or more descendants.
Central to the evolutionary species concept is the idea of an evolutionary trajectory. The trajectory of a species is the evolutionary pattern of its characteristics over time. For example, one of the earliest species in the story of human evolution, Australopithecus afarensis, is represented by dozens of fossil teeth and mandibles, as well as other remains. Paleontologists hypothesize that these fossils, from several sites in East Africa, are members of a single species because of their many morphological resemblances. No very similar fossils have ever been found before 3.6 million or after 3 million years ago, dates that appear to indicate the beginning and the end of the species.
Nevertheless, the fossils do show some differences that appear over time. Although the molar teeth of the fossils do not change over time, the mandibles are thicker and more massive in more recent fossils than in the most ancient ones. As far as paleontologists can test, the mandibles form a single series evolving over time toward greater size and thickness. The evolutionary species concept infers that the fossils represent a species, beginning 3.6 million years ago and ending 3 million years ago, with an evolutionary trajectory that includes the evolution of greater mandibular thickness, without apparent changes in molar sizes.
The strength of the evolutionary species concept is that it allows paleontologists to focus on the causes of evolutionary change, whether they occur during speciations or at other times. Regarding A. afarensis, the observation that mandibles increased in size during the existence of the species may be explained by different evolutionary forces and conditions than if all the change occurred with the reproductive isolation of a new population. Although the greater mandibular thickness of later mandibles might be a unique feature, attempting to establish a new phylogenetic species for the later fossils might detract from an explanation of the overall evolutionary pattern.
Phylogenetic species vs. evolutionary species concepts
But the evolutionary species concept also has its problems. Because it uses several different criteria, much more information may be necessary to define an evolutionary species. Some scientists do not view this as a drawback, since even if a scientific view of the species that once existed and their boundaries and relationships proves a challenge, it may nevertheless add to our understanding of the evolutionary process.
Yet for many paleontologists, the need to amass great numbers of fossils from different times makes the evolutionary species concept nearly impossible to implement. At the same time, if scientists always hold out the possibility that two different fossils were actually connected by gene flow, it may impede an understanding of evolutionary changes that accompany the appearance of new reproductively isolated species. If we want to have a scientific, meaning falsificationist, view of the species that have existed and their boundaries and relationships to each other, we must accept that the process will in many cases be difficult. Simply making up many species hypotheses cannot add to our knowledgeÑand in many cases it may detract. What is important is that we realize that our record of past species is incomplete, and our failure to substantiate the existence of many species in the past does not constitute evidence that they did not exist.
However species are defined, whenever scientists identify a species, they actually are stating a hypothesis about the relationships among individual organisms. Such a hypothesis may be tested using morphological, genetic, or behavioral evidence. Discovering real species that existed in the past involves predicting the morphological variability of populations, including variation that occurs among populations connected by gene flow. In the relatively small fossil samples available to paleontologists, determining the number of species in a sample is a significant problem. Researchers use a number of techniques to test species hypotheses with limited morphological samples.
Two fossil hominids: different species or not?
Eldredge N, Cracraft J. 1980. Phylogenetic patterns and the evolutionary process: Method and theory in comparative biology. New York: Columbia University Press.
Hawks J, Wolpoff MH. 2001. The accretion model of Neandertal evolution. Evolution 55:1474-1485.
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