A species by any other name…would leave us with the same problem


This is a great big week for anthropology coverage. The sequencing of the orangutan (Pongo species) genome made the cover of Nature. It’s grant-writing-dissertation-formulating-prelim-studying time for me so I haven’t had a chance to read this one yet. Science has a couple paleoanthropology-related stories, including two by Ann Gibbons. The first is about recent research on ancient DNA, and how this informs the debate about ‘modern human’ origins. But there’s also a short blurb on what the eff “species” means.

This is a great effing question! The textbook species definition is that proffered by Ernst Mayr: populations of actually or potentially interbreeding individuals, capable of producing viable (and fertile) offspring. Cool, so a dog and a cat are different species because if they mated (ew) no ungodly animal would come from this monstrous union. Expensive high-tech multivariate Scientific reconstruction simulations show the abomination would probably look like this:
But there are many “good” plant and animal species that do mate and reproduce successfully (‘hybridize’). Very often these hybrids are sterile, but then very often they’re not. This has led researchers to come up with scores of other ways to define species (Holliday (2003) has a great discussion on the matter).
Worse, there’s no way to measure, genetically or morphologically, just how different things should be before they can be called different species. The late Morris Goodman and others (Wildman et al. 2003) argued that humans and chimpanzees are so genetically similar that chimps, now in the genus Pan, should be moved to our genus Homo to denote how similar we are. But any other, non-genetic comparison would put our chimp cousins in a very different group from us. Moreover, the effects of hybridization seem, to me at least, to be fairly unpredictable, at least superficially. That is, the outcome of hybridization is highly contingent on what animals are hybridizing, and on these lineages’ own evolutionary histories (this is the intractable problem that made me abandon doing hybrid work for my dissertation. Some day though…).
A major issue relates to what I blogged about yesterday: both ‘species’ and ‘hybrid’ are terms we’ve found ourselves with, but they have no inherent meaning in themselves, other than whatever we give them. So it’s funny to read this from Gibbons’ story:

In the real world, [Jean-Jacques Hublin] says, Mayr’s concept doesn’t hold up: “There are about 330 closely related species of mammals that interbreed, and at least a third of them can produce fertile hybrids.”

But is it Mayr’s species concept that’s flawed, or was it misguided to have put these hybridizers into different species in the first place? Should we delineate species based on our a priori conception about whether two things are different, or should a definition of ‘species’ determine what we call them? Or does it even matter?
To this end, Gibbons’s other story describes the morphologically-unremarkable Denisova fossils as belonging to “a new type of human.” Well, now what the eff does that mean? We’re back to “The Species Problem” (the title of Gibbons’s article), but with a new term. And pretend for a moment that the Denisovan fossils didn’t yield DNA: the pinky and tooth probably would not have made headlines. Pretend they did have diagnostic cranial remains – would we have recognized them as being so distinct as their genes indicate?
For that matter, I wonder how many arguably ‘modern’ human fossils would still retain the modern moniker if we could analyze their genes…
Gibbons, A. (2011). The Species Problem Science, 331 (6016), 394-394 DOI: 10.1126/science.331.6016.394
Gibbons, A. (2011). A New View Of the Birth of Homo sapiens Science, 331 (6016), 392-394 DOI: 10.1126/science.331.6016.392
Holliday, T. (2003). Species Concepts, Reticulation, and Human Evolution Current Anthropology, 44 (5), 653-673 DOI: 10.1086/377663
Wildman, D. (2003). Implications of natural selection in shaping 99.4% nonsynonymous DNA identity between humans and chimpanzees: Enlarging genus Homo Proceedings of the National Academy of Sciences, 100 (12), 7181-7188 DOI: 10.1073/pnas.1232172100

Dobzhanksy on Posh Hybrids

Long-time readers may recall that one thing I wish I did active research on is hybridization: the crossing of divergent species or lineages, the developmental abnormalities arising from hybridization, and the potential role of hybridization in human evolution. One such developmental abnormality is “heterosis,” a.k.a. ‘hybrid vigor.’ In general, heterosis refers to any trait in hybrids that is larger than the average of the two parents’ (or the parents’ species) values for that trait. The phenomenon was recognized in plant domestication as far back as the 19th century – crosses between different plant (namely corn) strains produced hybrid strains with much greater yield than their parent species.

Implicit in the term is that heterosis, or larger size, is a more adaptive condition than found in the parents. Here’s what the late, brilliant Theodosius Dobzhansky (1950: on hybrids: 557) had to say on the matter.

The advisability of applying the term “heterosis” to cases in which heterozygotes are larger in body size, or show “increases” in any “traits,” but no evidence of higher adaptive value compared to the corresponding homozygotes, is open to question. Perhaps the word “luxuriance” would be a better designation for such cases, the word “heterosis” or “euheterosis” to be used for adaptive superiority of heterozygotes to homozygotes. . . . it is clear that the mechanisms underlying euheterosis and luxuriance are quite different.

I wonder if these luxuriant (not heterotic) hybrids also love diamonds, yoga and kopi luwak coffee?
DOBZHANSKY T (1950). Genetics of natural populations. XIX. Origin of heterosis through natural selection in populations of Drosophila pseudoobscura. Genetics, 35 (3), 288-302 PMID: 15414931

Denisova the Menace II: Nuclear story

Earlier this year, I discussed the publication of a mitochondrial DNA study from a 50,000 year old pinky bone from Denisova in Siberia. The big story there was that the mtDNA of this specimen was twice as divergent (different) from modern humans as Neandertal mtDNA. This suggested to researchers that there was this rogue human group (some [not I] might say ‘species’) running around Eurasia around the time of the Upper Paleolithic.

Well now they’ve sequenced the nuclear genome of one of a Denisova denizen. The picture painted is that a Denisova-Neandertal ‘lineage’ split off from that of modern humans some time in the distant past, then the Denisovans split from Neandertals some time later. Most interesting, modern-day Melanesians seem to derive about 4% of their genes from this ‘archaic’ Denisovan lineage, whereas this archaic genetic baggage isn’t present in other modern human populations.

AMAZING! Think back to the draft of the Neandertal nuclear genome, also published earlier this year. Green and colleagues (2010) reported that the Neandertal nuclear genome revealed that Neandertals contributed up to 4% of the genomes of modern-day non-Africans. Now, the Denisova genome shows that a different and more specific group of modern humans (Melanesians) appears to uniquely share a different set of nuclear genes from an ‘extinct’ human group.

But if they contributed their genes to modern people, are they really extinct? Of course not! I’m admittedly not a geneticist, but I think what we’re seeing here are the genetic signatures of a single, ancient structured population of modern humans. That is to say, all modern humans derive different amounts of their genes from various ancient subpopulations of ‘archaic’ humans (for ‘archaic,’ think ‘people that lived a long time ago’). There was just little enough contact between these populations for them to have diverged slightly from one another, but still enough contact for them all to have contributed different parts and amounts of genes to people today.

It is weird, then, to see the ancient DNA geneticist Svante Pääbo (out of whose lab this ancient genetic work is done) say this to BBC News:

“It is fascinating to see direct evidence that these archaic species did exist (alongside us) and it’s only for the last few tens of thousands of years that is unique in our history that we are alone on this planet and we have no close relatives with us anymore.”

Why are these ‘archaic species…alongside us”? The fact that these groups were mixing means that they are a single species – the ability (and propensity) to interbreed is the standard definition of ‘species’ used in modern biology.

So contrary to Pääbo’s quote, I’d say we do have close relatives with us, it’s just that modern humans are much more closely to one another related than ancient human populations were to one another. Probably there is more contact between modern human populations, beginning a few tens of thousands of years ago, because population sizes explode to the some 7 billion people we have on earth today. This greater contact means less chance for populations to diverge from one another.

The take-home: We all have multiple ancestors, from various times and places. For more comprehensive and better-informed coverage, check out John Hawks’s post on the topic.
Green, R., Krause, J., Briggs, A., Maricic, T., Stenzel, U., Kircher, M., Patterson, N., Li, H., Zhai, W., Fritz, M., Hansen, N., Durand, E., Malaspinas, A., Jensen, J., Marques-Bonet, T., Alkan, C., Prufer, K., Meyer, M., Burbano, H., Good, J., Schultz, R., Aximu-Petri, A., Butthof, A., Hober, B., Hoffner, B., Siegemund, M., Weihmann, A., Nusbaum, C., Lander, E., Russ, C., Novod, N., Affourtit, J., Egholm, M., Verna, C., Rudan, P., Brajkovic, D., Kucan, Z., Gusic, I., Doronichev, V., Golovanova, L., Lalueza-Fox, C., de la Rasilla, M., Fortea, J., Rosas, A., Schmitz, R., Johnson, P., Eichler, E., Falush, D., Birney, E., Mullikin, J., Slatkin, M., Nielsen, R., Kelso, J., Lachmann, M., Reich, D., & Paabo, S. (2010). A Draft Sequence of the Neandertal Genome Science, 328 (5979), 710-722 DOI: 10.1126/science.1188021

Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PL, Maricic T, Good JM, Marques-Bonet T, Alkan C, Fu Q, Mallick S, Li H, Meyer M, Eichler EE, Stoneking M, Richards M, Talamo S, Shunkov MV, Derevianko AP, Hublin JJ, Kelso J, Slatkin M, & Pääbo S (2010). Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature, 468 (7327), 1053-60 PMID: 21179161

Hybrids, hominoids and hominins

Is the Eastern lowland gorilla (Gorilla beringei graueri) a hybrid (sub)species? A recent study by RR Ackermann and JM Bishop suggests this scenario.

Their study used morphological, genetic and geographic information to analyze variation in extant gorilla species and subspecies. A previous study by Ackermann and colleagues (2006) on baboons found that non-metric traits–namely pairs of extra teeth and unusual sutures between some facial bones–have freakishly high frequencies in known hybrids compared to their parents of different species. Well wouldn’t you know it: G. b. graueri had a significantly higher frequency of such traits than the other gorilla species/subspecies (the putative ‘parental’ species, the Eastern mountain gorilla G. b. beringei and the Western lowland gorilla G. gorilla gorilla).

Additionally, for a number of cranial metric traits, graueri had significantly higher values than the other gorilla species’ sample averages. “Heterosis” refers to a condition wherein a hybrid phenotype exceeds the combined parental mean–it appears that if this is truly a hybrid population, graueri displays heterosis for a number of cranial features. Finally, it is notable that graueri has been described as more like Western gorillas in some respects, but more like Eastern mountain gorillas in others, and then totally unique in some aspects. This is arguably a result of graueri possessing genes from two other distinct species.

Oh, and the mtDNA evidence suggests fairly recent gene flow from Western lowland gorillas eastward. Because mtDNA is maternally inherited, this implies that females have been involved in this west-to-east gene flow. However, it is unclear the extent to which there was east-to-west gene flow, or the potential involvement of male gorillas here.

Why is graueri likely a largely hybrid sample, and not just part of a morphological and genetic cline conecting Western and Eastern gorilla populations (i.e. making gorillas a single, polymorphic, geographically broad species)? The hybrid morphologies above are believed to indicate complications that arise in development, due to the union of two species’ distinct sets of genes. Such signatures of hybridizaiton would not be expected to appear in a regularly panmictic species. It also seems that the separation of Western and Eastern gorilla species occurred during the Pleistocene, which means that the two sides have been diverging for quite a long time and have recently come back into contact.

I think the authors make a very good case for the importance of hybridization in the evoluton of gorillas, at least as we know them today. I like their use of both morphological and genetic data, which complement one another nicely in support of a hybrid-type nature of Gorilla beringei graueri. In addition, the implicaitons of the study are fantastic! Even though the authors did not know for sure whether individual specimens were hybrids, they were able to use the results of previous work to make a convicning case that a number of their specimens were very likely to be hybrids. This is a good sign for persons like myself who are interested in the detection of hybrids in skeletal/fossil samples. Another great implication is that hybridization indeed has a place in hominoid evolution–it awaits to be seen what role hybridization may have played in the course of human evolution.

Ackermann RR, Rogers J and Cheverud JM. 2006. Identifying the morphological signatures of hybridization in primate and human evolution. Journal of Human Evolution 51: 621-645.

Ackermann RR and JM Bishop. Morphological and molecular evidence reveals recent hybridization between gorilla taxa. Evolution: in press.

Long-term effects of hybridization in primates

One of my research interests is hybridization in primates, and the possible role it played in hominin evolution. It’s a sticky subject, so it’s always fun to find good papers on real-life examples of hybridization between different primate ‘species.’ In this vein, Burrell et al. <!–[if supportFields]> ADDIN EN.CITE Burrell200975375317Burrell, Andrew S.Jolly, Clifford J.Tosi, Anthony J.Disotell, Todd R.Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini)Molecular Phylogenetics and EvolutionMolecular Phylogenetics and Evolution340-348512KipunjiBaboonRungwecebusLophocebusPapioHybrid speciationMangabey2009http://www.sciencedirect.com/science/article/B6WNH-4VNKGV7-4/2/1fc25562a43afdf7c3fafda3bcfaceb7 <![endif]–>(2009)<!–[if supportFields]><![endif]–> report that the kipunji—a highly endangered papionin monkey from a small area in Tanzania—has an mtDNA haplotype from its yellow baboon (Papio cynocephalus) neighbors. Morphologically, the (living) monkey looks more like mangabeys (Lophocebus), though it has some baboon-like affinities, too.The authors posit that the most likely reason for this is inter-generic hybridization in the past, between Papio cynocephalus (yellow baboons) and Lophocebus sp. (mangabey monkeys).

The authors suggest a scenario in which in a marginal environment, Lophocebus (or Cercocebus?) males mated with some P. cynocephalus females. The hybrids, then, back-crossed into the respective parent species—thus baboon mtDNA was brought into a mangabey population. From here, the habitat favored nuclear genes of mangabeys, hence the overall mangabey appearance. Even though mtDNA is often (by necessity) assumed to be selectively neutral for phylogenetic studies such as these, it is not inconceivable that the baboon mtDNA persisted in the population because of selection, too.

The authors note that the test of the hybrid-origin hypothesis will come from nuclear DNA. If the kipunji truly represents the meshing of two genera’s genomes, then it should have a large amount of mangabey nuclear DNA. However, if the nuclear genome is all Papio that would mean that the kipunji’s ancestors were baboons whose morphology (and niche?) converged on that of mangabeys. Even this outcome would be a bit incredible, given the apparent pervasiveness of homoplasy within the papionins. In fact, the few nuclear genes known for the specimen either cluster in Papio, or are phylogenetically ambiguous. But for the moment, mtDNA and morphology support hybrid-origins. This is especially remarkable, since hybridization between genera, above the species level, leading to a stable taxon has not been documented before.

It is unclear whether the kipunji represents an instance of hybrid (or “secondary”) speciation, in which hybrids thrive in an environment while individuals of the parental species don’t, or just an intense case of gene transfer between species (I suppose if you’re getting a whole mitochondrial genome, it’s not really introgression). Nevertheless, the paper provides an amazing example of the potential evolutionary significance of hybridization in primates. Nice.


<!–[if supportFields]> ADDIN EN.REFLIST <![endif]–>Burrell AS, Jolly CJ, Tosi AJ, and Disotell TR. 2009. Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini). Molecular Phylogenetics and Evolution 51(2):340-348.

A Tale of Two Lineages

[Hey, I’ll bet I’m the first person to make that allusion…]
In a paper published in JHE today, M. Schillaci posits that human facial anatomy suggests the existence of two human lineages in the late Pleistocene. Schillaci’s analysis reveals that faces of early Australasian crania (40-8 ka) are very similar to those of Levantine specimens Skhul 5, Qafzeh 6 and Qafzeh (100-90 ka). The overall results of the study suggest that the Australasian and Levantine populations share an earlier common ancestor than modern humans, including Upper Paleolithic Europeans. Schillaci interprets this to mean that modern humans first dispersed from Africa around 100 ka, long before the supposed “revolution” of Paleolithic Europe, and made it as far as Australia; second dispersal then occurred some 50 ka later.

The article brings up the issue of Out-of-Africa (Replacement) vs. Multiregional models, but does not clearly come out directly in favor of either one. But by setting up a scenario in which two human lineages are present throughout the Old World in the last 100 ka, the possibility is opened up for these lineages to accrue genetic differences simply by drift or even by selection, then to come into contact again and admix, and for the “archaic” genes to be incorporated into the newer (and modern) genome (introgressive hybridization; cf Evans et al. 2006, Garrigan and Kingan 2007, Hawks and Cochran 2006).

Schillaci does note that the Levantine sample

exhibits a slightly closer genetic relationship to Neandertals (d=0.7318) than to Upper Paleolithic Europeans (d=0.7483). . . . This observed relationship is probably not the result of phenotypic convergence, and likely reflects a slightly more recent common ancestry and/or perhaps hybridization between early modern humans and Neandertals (Trinkaus, 2007). (p. 6)

However, he later notes,

In the present study, the relationship between early modern humans from the Levant and early Australasians (d=0.348) is more than 2.1 times closer than between early modern humans and Neandertals (d=0.7318), and Neandertals do not show a close relationship with early Australasians (d=1.2615). If the observed relationship between Neandertals and early modern humans is the product of hybridization, there is no craniometric evidence indicating that there was substantial introgression of Neandertal alleles into the dispersing modern human population… (p. 7)

Can Schillaci make these claims about “genetic relationship[s]” based on his data? Let’s look at the opening line of the abstract: “This study examines the genetic affinities of various modern human groupings using a multivariate analysis of morphometric data.” A rewording might be: This study examines the craniofacial affinities of various modern human groupings, and to thereby infer genetic relationships. Basically, Schillaci assumes that genetic relationships between populations are accurately reflected in facial anatomy, a bold statement to make. Indeed, he acknowledges the problems with this assumption, but also cites studies (which I haven’t yet read) suggest that craniometric variation in humans throughout the world fits a neutral model of genetic variation. So, Schillaci talks about genetic relationships throughout the paper, but these aren’t based on actual genetic data, but rather inferences from craniometric data–quite confusing. His aforementioned lack of evidence for introgression between neandertals and early modern humans does not preclude real genetic evidence for introgression (cf. what I cf-ed above.)

What I care about: the study allows for, and possibly corroborates, a Multiregional model of human evolution (of course, what I really care about is the possibility of such a model prior to, and in the early stages of, the genus Homo). Hey, I guess old-school craniometrics hasn’t outlived its usefulness in physical anthropology.

Evans PD et al. 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(48): 18178-18183.

Garrigan D and SB Kingan. 2007. Archaic Human Admixture. Curr Anthropol 48(6): 895-902.

Hawks J and GM Cochran. 2006. Dynamics of adaptive introgression from archaic to modern humans. Paleoanthropol 4: 101-115.

Schillaci M, in press. Human cranial diversity and evidence for an ancient lineage of modern humans. J Hum Evol xx: 1-13.