Leopard horse: Fossils, phenotypes and genotypes

I wish I were talking about some beastly horse-big-cat hybrid, or at least a carnivorous horse. Instead… a ton of anthropology-related papers came out today in PNAS, and possibly the coolest one is a study that compares the DNA of Pleistocene fossil and modern horses with different coat colors/patterns, and then ties this in with Paleolithic cave art. A crazy confluence of four-field anthropology right there.

Modern horses and their depictions in Late Pleistocene French caves (Pruvost et al. 2011)
Melanie Pruvost and colleagues (in press) noted that the depiction of spotted horses at the site of Pech-Merle (they give 24 kya) could mean one of two things: (1) either the early human painters were depicting horses they actually saw on the landscape at the time, or (2) they were just being fanciful and frivolous, creative and carefree with their cavern canvas. Now, some modern horse breeds have a similar spotted, “leopard” phenotype, and a genetic basis for this is understood. So Pruvost and pals examined DNA from fossil horse bones from European sites dating to 20 – 2 kya to see if these mottled mares roamed the lands of the cave-painters. Sure enough, several samples show evidence for the mutation causing leopard spots.

This is pretty cool for evolutionary biology and paleontology. A major question in biology is how an individual’s genes (genotype) relate to overall appearance/behavior (phenotype). To a certain extent, physical variation between organisms arises from genetic variation, so when we see things evolve through the fossil record, this ought to correspond with some genetic changes as well. But linking genes to appearances isn’t so easy (especially for extinct animals). Pruvost and colleagues’ study is a step in this direction, though. Plus, the recent sequencing of the fossil Neandertal (Green et al. 2010) and Denisovan (Reich et al. 2010) genomes makes it possible to try to figure out if/how humans’ unique physical traits reflect our genes. In fact, even before these genomes were fully sequenced, Carles Lalueza-Fox and team (2007) identified a mutation on Neandertals’ MC1R gene, strongly suggesting the Neandertals sampled had light skin and red hair.

But the genetic basis for skeletal phenotypes is harder to discern. For example, Green et al. (2010) identified the unique human version of the RUNX2 gene as having come under strong natural selection since the disappearance of Neandertals. The authors noted that because mutations of RUNX2 in humans are associated with a cleidocranial dysplasia affecting the form of the skull and shoulders, and because humans and Neandertals differ in some aspects of their skulls and shoulders, then RUNX2 variation between humans and Neandertals is likely related to visible differences in their skeletons. But that’s about as much as could be said at the moment – RUNX2 is involved in bony development of the entire skeleton, interacting with other various genes in various places during ontogeny. So while it’s tempting, it’s still a little early to link RUNX2, or pretty much any other development-related gene, with physical differences between humans and our fossil relatives. But one day!

A Neandertal’s ruddy locks have never preserved in the fossil record, but its bones are very well known. In an ironic twist, we may have a better understanding of the genetic basis of variation in a soft-tissue (for which there are no fossils), than we do for the skeleton (for which we have lots of fossils).

And maybe one day I’ll get that leopard horse I was hoping for.

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

Pruvost, M., Bellone, R., Benecke, N., Sandoval-Castellanos, E., Cieslak, M., Kuznetsova, T., Morales-Muniz, A., O’Connor, T., Reissmann, M., Hofreiter, M., & Ludwig, A. (2011). Genotypes of predomestic horses match phenotypes painted in Paleolithic works of cave art Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1108982108

Reich, D., Green, R., Kircher, M., Krause, J., Patterson, N., Durand, E., Viola, B., Briggs, A., Stenzel, U., Johnson, P., Maricic, T., Good, J., Marques-Bonet, T., Alkan, C., Fu, Q., Mallick, S., Li, H., Meyer, M., Eichler, E., Stoneking, M., Richards, M., Talamo, S., Shunkov, M., Derevianko, A., Hublin, J., Kelso, J., Slatkin, M., & Pääbo, S. (2010). Genetic history of an archaic hominin group from Denisova Cave in Siberia Nature, 468 (7327), 1053-1060 DOI: 10.1038/nature09710

Inanimate fossils getting older still

Two reports came out last week in the journal Nature, re-dating some European human fossils to before 40 thousand years ago (kya), a few thousand years older than previous evidence for modern-looking people in the region. The media have been reporting these studies as revealing “the first Europeans,” but of course we all know that the first Europeans were the badass hominids, my favorites, from the 1.8 million year old site of Dmanisi.

KC4 maxilla (Higham et al. 2011)

From Kent’s Cavern (United Kingdom) is a partial maxilla, now dated to 44 – 41 kya* (Higham et al. 2011; but see below). The jaw fragment with highly worn teeth was found just above some Aurignacian-like (Upper Paleolithic) blades in 1927. [NB below these 2 blades were 2 other blades of a tool “complex…tentatively associated with Neandertals] The laughable amount of bone makes it rather impossible to say whether the fossil represents a Neandertal or more modern-looking human. The authors examined what little of the morphology was left and concluded that the fossil shared the most similarities with recent humans but only a few with Neandertals. A more rigorous analysis of what this mix of traits means would have been nice (i.e. why would an individual have derived traits of both ‘modern’ humans and Neandertals?). The researchers tried to extract DNA for analysis, but apparently organic remains were too poorly preserved for a good analysis. Bummer.

Cavallo B and C (Benazzi et al. 2011)

A similar older-than-we-thought story is reported by Stefano Benazzi and buddies, who reanalyzed teeth from the Italian site of Grotta del Cavallo (left). After the site was excavated in 1967, the teeth were attributed to Neandertals and the lithics classified as “Uluzzian.” I would be a dirty liar if I said knew anything about the “Uluzzian” industry (try this other site which may be more informative), but apparently it’s seen as transitional between the Neandertal-associated Mousterian and ‘more advanced’ Upper Paleolithic toolkits. So this assemblage could be used to argue that Neandertals were smart enough to upgrade to a sexier stone tool industry shortly before their anatomy (but not their genes!) disappeared. BUT! also like in Kent’s Cavern paper, Benazzi and colleagues examined what little morphology is preserved in the fossil teeth, and (re)assigned them to modern-looking humans. The authors provided nice qualitative and quantitative arguments for the human status of the teeth, though again I have to raise caution that these are only teeth and we have no idea what the rest of the skeleton would have looked like. Researchers also analyzed shells associated with the now-human teeth and dated the site to around 44 kya, making them the oldest probably-human remains in Europe.

Now, according to conventional wisdom, the Neandertals were dullards who made and used the Mousterian stone tool industry. The Mousterian was nice and all, but not nearly as wicked-pisser as the smart and sassy modern-looking humans’ Aurignacian toolkit. The thing is, though, there really hasn’t been really a lot of evidence unequivocally linking modern-looking fossils with Aurignacian artifacts. So both of the recent studies in Nature lend support to the idea that maybe modern humans were the sole makers (and users) of an advanced stone tool industry. But it’s important to remember [1] that the blades ‘associated’ with the Kent’s Cavern jaw can’t really be definitively attributed to a stone tool industry; [2] the blades were deeper in the cave than the jaw, and so may actually be appreciably older than the jaw; and [3] while the teeth from Kent’s Cavern and Cavallo do look most comparable to those belonging to ‘anatomically’ modern humans, we don’t know what the skulls or skeletons containing the teeth looked like. All that said, it’s neat to see the possible appearance of certain anatomy and technology in Europe thousands of years earlier than previously thought. It also re-raises the issue of the degree to which modern-looking humans and Neandertals overlapped in space and time, and what these interactions would have been like (I’d guess terrifying, hilarious and/or sexy).

KC4 originally
(Higham et al. 2011)

A fun lesson also comes from the Kent’s Cavern study. Higham and colleagues report that the KC4 human maxilla was excavated in 1927 and analyzed by Sir Arthur Keith, a well-trained anatomist and paleoanthropologist famous in his day. Keith described the fossil as containing a canine, second premolar and first molar (right, compare with above). Higham and colleagues, however, noticed that what Keith described as a second premolar was in fact a first premolar. The teeth are so worn they mostly lack information about their form and features, so this mistake probably didn’t really mislead anatomists in any way. Still, it goes to show that even experts like Keith can make mistakes or overlook the things they know best, and this is not the first time I’ve seen this happen with fossils. So always (politely) question those giants whose shoulders you’re standing upon.

*Update (07 Nov): John Hawks points out that the KC4 maxilla itself was not used to obtain the older radiocarbon age estimate. In 1989 the maxilla was directly dated to around 30 kya, over 10 ky younger than the new estimates. Higham and friends thought this date was too young, based on methodological grounds. An attempt to redate the KC4 maxilla based on one of the teeth yielded too little collagen (organic material) to produce a date. Bummer again! The new estimate is instead based on radiocarbon dates obtained from animal bones that were excavated from above and below the human jaw. So this ‘redating’ of the Kent’s Cavern maxilla is very interesting, but should be taken with a grain of salt.

See for yourself
Benazzi, S., Douka, K., Fornai, C., Bauer, C., Kullmer, O., Svoboda, J., Pap, I., Mallegni, F., Bayle, P., Coquerelle, M., Condemi, S., Ronchitelli, A., Harvati, K., & Weber, G. (2011). Early dispersal of modern humans in Europe and implications for Neanderthal behaviour Nature DOI: 10.1038/nature10617

Higham, T., Compton, T., Stringer, C., Jacobi, R., Shapiro, B., Trinkaus, E., Chandler, B., Gröning, F., Collins, C., Hillson, S., O’Higgins, P., FitzGerald, C., & Fagan, M. (2011). The earliest evidence for anatomically modern humans in northwestern Europe Nature DOI: 10.1038/nature10484

Neandertal terminal biogeography

How late did Neandertals persist in the Late Pleistocene? Two papers out this week discuss the dates of the latest Neandertals in western Asia.

Pinhasi and colleagues (2011) stress the importance of directly dating Late Pleistocene human-ish fossils. There are numerous techniques used to estimate the ages of the fun stuff we find underground. For fairly old fossils like australopithecines, perhaps the most reliable radiometric method is Argon-Argon, though this requires the fossils to be relatable to volcanic sediments whose argon levels can be measured. The point is that dates of burial are often not estimated from the fossil materials themselves, but rather the sediments and such surrounding the fossil of interest. But younger fossils (than say 50,000) preserve some of the bone’s original carbon -allowing age estimates of the fossils themselves by radiocarbon dating.

Pinhasi and colleagues note that while seven separate Neandertal specimens from across Europe and western Asia have been directly dated to be younger than 36 thousand years, these dates may be underestimates. In other words, Neandertals may not have lived after 40 thousand years. To this end, these researchers directly re-dated the infant Neandertal from Mezmaiskaya Cave in Russia, and estimate the poor lad to have died around 42-44 thousand years ago. The authors predict that future direct redating of other Neandertals will show Neandertals to have disappeared by 40 thousand years ago, and that they would have overlapped in time with more modern-looking humans either minimally or not at all. If only there were more information on the latest dates for Middle Paleolithic people!

Lucky me, in tomorrow’s Science, Ludovic Slimak and colleagues report on Mousterian tools dating to 32-34 thousand years ago, from the site of Byzovaya Cave “in the western foothills of the Polar Urals” (Slimak et al. 2011: 841). “POLAR!” The site is way further north than any site with Neandertal bones like Mezmaiskaya and Okladnikov, which is pretty impressive. But, there are no human remains associated with the tools, so we don’t know who made them. To what extent do these finds address Pinhasi’s and others’ contention of no Neandertals after 40 thousand years ago?

Slimak and colleagues carbon-dated animal bones that were butchered with the Mousterian tools, which were allegedly made only by Neandertals. There is a major problem with the wide-held assumption that Mousterian (Middle Paleolithic) tools were made only by Neandertals, whereas Upper Paleolithic industries beginning with the Aurignacian were made only by humans. This goes along with people’s wont to make a connection between stone tool ‘culture’ and biologically determined, phylogenetically significant behavioral capacities. But of course, we know biology doesn’t determine behavior, and so there’s no reason to assume [Mousterian:Neandertal::Aurignacian:’Modern’ Human]. Where Mousterian remains have been associated with diagnostic skeletal remains, they are Neandertal. But the Aurignacian, so far as I know, is not associated with diagnostic fossils – we can’t say for certain who made it. Plus we know Neandertals were doing something kooky, yet logical in some sort of cognitively complex way, with bird feathers in Italy 44 thousand years ago (Peresani et al. 2011). So the Byzovaya stone tools may demonstrate a late, northern holdout of Neandertals, but then they could simply mean that the new technology either hadn’t arrived or hadn’t been successful in the far reaches of sub-Artic Pleistocene humanity.

If the latter is the case and Pinhasi & team’s hypothesis that Neandertals didn’t coexist in time and space (or did only minimally) holds, then the old assumption of Mousterian = Neandertal becomes dubious for other sites with Mousterian tools but no diagnostic fossils. This would also beg the question of the role of modern humans in the Neandertal demise – did the Neandertals disappear and open a niche for other groups of people (‘moderns’)?

So how were Neandertal populations distributed through space and time in their latest days? I dunno! But for the moment I suppose I’d be surprised if no fossils with Neandertal morphology turn out to be younger than 40 thousand years as suggested by Pinhasi and co. But then I could be wrong.

Hoffmann, A., Hublin, J., Hüls, M., & Terberger, T. (2011). The Homo aurignaciensis hauseri from Combe-Capelle – A Mesolithic burial Journal of Human Evolution DOI:10.1016/j.jhevol.2011.03.001

Peresani, M., Fiore, I., Gala, M., Romandini, M., & Tagliacozzo, A. (2011). Late Neandertals and the intentional removal of feathers as evidenced from bird bone taphonomy at Fumane Cave 44 ky B.P., Italy Proceedings of the National Academy of Sciences, 108 (10), 3888-3893 DOI:10.1073/pnas.1016212108

Pinhasi R, Higham TF, Golovanova LV, & Doronichev VB (2011). Revised age of late Neanderthal occupation and the end of the Middle Paleolithic in the northern Caucasus.Proceedings of the National Academy of Sciences of the United States of America PMID:21555570

Slimak, L., Svendsen, J., Mangerud, J., Plisson, H., Heggen, H., Brugere, A., & Pavlov, P. (2011). Late Mousterian Persistence near the Arctic Circle Science, 332 (6031), 841-845 DOI:10.1126/science.1203866

Speciation and reticulation

ResearchBlogging.org Hey, “all you lovers out there,” which is how Marvin Berry introduced “Earth Angel” at the Enchantment Under the Sea dance back in good-olde 1955. And by “lovers” I mean “geneticists.”

Poring over the recent Neandertal nuclear genome paper (Green et al. 2010) for seminars, we’re struck by two contradictory ideas. On the one hand, the authors demonstrate pretty convincingly that Neandertals and the more ‘anatomically modern’ humans of Europe and Asia interbred. This doesn’t come from genetic comparisons of Neandertal and contemporaneous human fossils, but of Neandertals with living humans traipsing modern soil. But on the other hand, the authors estimate the time of the divergence of Neandertal and living human populations.
Herein lies the rub:

“Population divergence [is] defined as the point in time when two populations last exchanged genes.” (Green et al. 2010: 717)

Which they estimate, based on genome sequence divergence and some other assumptions, to be anywhere from ~270,000 – 440,000 years ago. But then this:

“[The Out-of-Africa] model for modern human origins suggests that all present-day humans trace all their ancestry back to a small African population that expanded and replaced [Neandertals] without admixture. Our analysis of the Neandertal genome may not be compatible with this view because Neanertals are on average closer to individuals in Eurasia…” (Green et al. 2010: 721)

Though they say “may not” they probably should’ve just said “isn’t.” Either way, they estimate an ancient date at which the groups in question “last exchanged genes,” but also demonstrate that these populations last exchanged genes much more recently.
So what is “population divergence,” then? As a wise man asked, “what does divergence mean when there is reticulation?” (I’m assuming he would prefer to go nameless) Reticulation referring not to pythons or chipmunks, but to mating between individuals in different populations. Is “divergence” not so much the last time genes were exchanged, but rather the time when the genomes began to become different?
Now that I bring it up, wouldn’t it also be neat to see a fight between the reticulated python and northern reticulated chipmunk?
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

Iron Chef: Middle Paleolithic

New evidence suggests Neandertals ate cooked foods, and plants at that.
Amanda Henry and colleagues (in press) extracted phytoliths – small mineralized parts from plants – and starch grains from dental calculus found on 2 Belgian (Spy) and 1 Iraqi (Shanidar) Neandertal fossils. I’ve never seen a study look at this kind of evidence before, I have to say it’s pretty neat. Calculus, not just a badass type of mathematics, is mineralized plaque that can build up on teeth. As the Neandertals chewed their foods, the small food particles got trapped in their plaque and this gross matrix hardened onto their teeth. So, if you want to obliterate traces of your diet, and otherwise conform to Western norms of dental hygiene, one thing you can do is be sure always to brush. And floss.

Microscopic barley grains. Top row are examples of grains from Shanidar calculus, and beneath each are examples of modern barley to which they are probably related. Fig. 1 from Henry et al. (in press)

Types of plants eaten by the Shanidar individual include relatives of modern wheat, barley (see figure), and rye, and what looked like beans and date palm, too. In addition, some of the starch grains bear strong resemblance to plant remains after cooking, probably either by boiling or baking. The Belgian samples provided less broad evidence, indicating presence mainly of some type of underground storage organ (like a tuber) and grass seeds. Many phytoliths and grains were unable to be identified, leaving open the chance that future research on these will uncover utilization of a greater breadth of plants.
This is pretty neat, since studies of the isotopes in Neandertal teeth indicated a strong meat component to the diet. In fact, Neandertals have often been referred to as ‘top carnivores.’ This new study supports other evidence of a large plant component as well. After all, isotope studies are only one form of evidence of diet. Neandertals weren’t just big game hunters, they were hunter-gatherers. What’s more, they improved the edibility and nutritive value of their plant (and probably also animal) foods by cooking them. So, this study presents another way in which Neandertals were probably no different from contemporaneous humans.
One has to wonder what these paleolithic meals would have been like. Especially what with claims of cannibalism in some Neandertal sites – perhaps “liver with some fava beans and a nice chiaaanti…fhfhfhfhfhfhfh,” to quote Hannibal Lecter. And who would win Iron Chef – the classic Neandertals, or their more ‘modern’ looking contemporaries?

Henry, A., Brooks, A., & Piperno, D. (2010). Microfossils in calculus demonstrate consumption of plants and cooked foods in Neanderthal diets (Shanidar III, Iraq; Spy I and II, Belgium) Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1016868108

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

Tooth formation rates – what do species comparisons really mean?

A paper just came out in PNAS, by Tanya Smith and others, in which they estimate tooth-crown formation times in a large sample of modern humans (n=>300 individuals), a modest sample of Neandertals (n=8), and a poor sample of ‘fossil Homo sapiens‘ (n=3). Teeth form by the periodic deposition of enamel (the hard, white part visible in teeth in the mouth) and dentin (forms the tooth root and internal part of the crown). These periodicities are fairly regular (though variable), thus allowing researchers to estimate how long it took for teeth to develop. As previous studies have shown, Smith and colleagues find that Neandertals formed most of their teeth faster than modern humans.

Growth and development are part of an organism’s life history strategy, and so the observation that Neandertals (and other fossil human species/lineages) form their teeth faster than modern people suggests that perhaps they ‘lived faster’ and died younger than us. It has also been used as evidence that Neandertals are a different species from modern humans.
But I don’t know how well the latter taxonomic argument works. Along these lines, I wish the authors had discussed the meaning of the estimated crown formation times for their fossil ‘modern’ humans (Qafzeh 10 & 15 from Israel ~100 thousand years ago, and Irhoud 3 from Morocco ~160 thousand years ago). The boxplot summaries of crown extension rates (above) show that Neandertals are, indeed, generally fast relative to the large modern sample. However the fossil-modern humans (asterisks, which I’ve circled in red) show a bizarre, not easily interpretable pattern. For the central upper incisors (I1), fossil-moderns are either within the Neandertal range or an outlier at the high end of the human sample. For the lower second incisor (I2) the two fossil-moderns are either waaaaaay above the human range, or a little below it -either way it’s outside the human range. In addition, the sole fossil-modern lower first molar has a lower rate than the modern sample – suggesting an even slower development time. Only the fossil-modern canine formation time fits comfortably within the range of modern humans. Given this wide range of variation in tooth crown formation times in the very small sample of fossil-modern humans, I don’t think we can use this information to make taxonomic arguments.
I think these dental histology studies are very interesting, but I don’t know how much stock we can put in any taxonomic interpretations of them. That Neandertal teeth form faster than modern humans’ is old news, and the discussion focused solely on the neandertal-modern human comparison. It’s too bad that the really interesting part of the paper – the variation in formation time displayed by the fossil-moderns – got no discussion.
The paper
Smith TM et al. 2010. Dental evidence for ontogenetic differences between modern humans and Neandertals. Proceedings of the National Academy of Sciences, in press.

Neandertal Nuclear Genome: Multiregional Evolution is the new Out of Africa

Green and colleagues announced the Neandertal nuclear genome in tomorrow’s issue of the journal Science. Hitherto only complete mitochondrial DNA (mtDNA) genomes had been recovered. These are only inherited maternally, and the genetic differences between the Neandertal mtDNA and that of modern humans seemed to suggest that Neandertals and humans didn’t mix, that is that they were replaced by “anatomically modern humans” (whatever that phrase means). mtDNA is special as far as genetic stuff goes – only inherited maternally, so only tells about one strain out of a slew of ancestors; doesn’t recombine; as a result, selection acting on a part results on selection of the entire mitochondrial genome; oh and it’s certainly not selectively neutral.
So should we have been wary when it was suggested by mtDNA that neandertals and humans were separate species (recall the issue was even crazier with the Denisova mtDNA specimen…)?

This is a big deal, because for the past several decades researchers have debated the nature of modern human origins. On morphological and shaky mtDNA evidence, several researchers have argued that modern humans emerged from a small African population, which then spread throughout the world between 100-200 thousand years ago and replaced all other ‘archaic’ human populations. Intuitively this doesn’t make sense, and today’s neandertal announcement renders the Out of Africa with Replacement model for human origins absolutely untenable.
So, were Neandertals and (even then-modern) humans the same species? Yes! If Neandertals were a different species, we would expect all humans to be equally genetically divergent from neandertals. But this is not what Green and colleagues found. Rather, the genomes of a French person, a Chinese person, and a Papua New Guinean were actually more similar to the Neandertal genomes than the two African human representatives were to the Neandertals. Such disparate divergences mean we’re dealing with genetic variation within a species, rather than between species.
In fact, the authors estimate that about 1-4% of modern, non-African genomes are derived from Neandertals. Plagnol and Wall (2006) estimated around 5% of human genes come from ‘archaic’ humans, so it is good to see corroborating evidence from two sources. It is interesting, however, that earlier candidates for introgression from archaics, such as the microcephalin haplogroup D, do not appear to have come from Neandertals (maybe another archaic population, then?).
The authors were also able to use these neandertal and modern human genomes to estimate regions of the human genome that have been under recent and accelerated evolution, including:
  • SPAG17 is associated with sperm motility – is this evidence for sperm competition and recent sexual selection?
  • Regions in which, among modern humans, mutations are associated with social-cognitive diseases like schizophrenia and autism
  • RUNX2, again where misexpression in humans is associated with dysgenesis of frontal bone (forehead), shoulder and rib-cage shape morphology
I think the only things I would have loved to have seen in this study are simple logistical issues, things that are probably simply not practical at the moment because of technological constraints. First, I’d love to see a much larger set of modern human reference genomes. The study included only 2 human nuclear genomes from sub-Saharan Africa, 1 from Europe, 1 from China and 1 from Papua New Guinea. Yes, this samples variation from all over the world, but it’s 5 out of nearly 7 billion genomes out there today. At the moment, however, it’s just not that easy to acquire and handle genomic data for many individuals.
Second, I’d like to see nuclear genome comparisons using Upper Paleolithic modern humans – ‘modern human’ contemporaries of Neandertals. The Denisova mtDNA was surprising because, at some 40 ka, its genome was about twice as different from modern humans as the neandertal mtDNA sequences were. Just what kind of genetic diversity are we looking at in ancient (anatomically both ‘archaic’ and ‘modern’) humans?
Green and colleagues should be lauded because of how meticulously they went about this project. They took major pains to circumvent issues of contamination, they maximized the DNA they could obtain in spite of preservation issues, they came up with some clever tests. And their results are really interesting.
Green RE et al. 2010. A draft sequence of the Neandertal genome. Science 328: 710 – 722.
Plagnol V and Wall JD. 2006. Possible Ancestral Structure in Human Populations. PLoS Genetics 2(7): e105

Denisova the Menace

Johannes Krause and colleagues reported yesterday in Nature‘s advance online publication, on a new hominin mitochondrial DNA (mtDNA) genome. The genetic material is derived from a finger bone which lacks diagnostic morphology, from a southern Siberian site called Denisova dating to between 30 – 50 thousand years ago. Of note, the authors describe that the mtDNA is about twice as different from humans as any neandertal mtDNA is from modern humans. If the human-neandertal mtDNA divergence is accurately estimated at around 450 thousand years ago, that means this mystery specimen’s mtDNA lineage diverged from the human-neandertal line around 1 million years ago.

This is really interesting, because also around 40 thousand years ago, but from a site some 100 km to the west of Denisova, bones that were morphologically non-diagnostic yielded mtDNA basically identical to Neandertals.
Does this speak to the presence of at least 3 human species running around the Old World around 40 thousand years ago? Not necessarily. Most claims of a speciose recent human fossil record are based on cranial morphology. For example, modern human skulls are fairly different from “classic” neandertal skulls of western Europe (which is why the Skhul and Qafzeh hominins which display characteristics of both groups are so interesting). However, the mtDNA we have of most of these specimens comes from non-diagnostic specimens. The first Neandertal mtDNA studied came from a piece of tibia (shin bone); this bone is basically non-diagnostic morphologically between recent hominins, and the site it came from (Vindija, Croatia) has both human and Neandertal remains. The Denisova finger, similarly, is non-diagnostic in morphology so far as I can tell, and the archaeological layer contains both Middle and Upper Paleolithic cultural materials: we have no idea what these mtDNA bearers looked like.
I think people thinking “new species at Denisova” (NB: Krause and colleagues never make this claim!) would be shocked if it turns out that the Denisova remains, or those from which the Vindija specimens came, were morphologically modern humans, but this is entirely possible.
Humans today are not so diverse genetically as superficial appearances may suggest to many people. I wouldn’t be surprised if humans simply displayed more genetic diversity in the past. It is certainly interesting just how different the Denisova genome is from both humans and Neandertals. What exactly this difference means is just not clear. It is further interesting to note that the coding regions of the Denisova mtDNA show signs of strong purifying selection. Assumptions of neutrality are so important for genetic studies that I think people often forget that mtDNA actually serves functions necessary to survival, and is not actually neutral. Maybe this ancient mtDNA lineage lasted so long because the mitochondria provided some selective advantage, hence the purifying selection? Who knows?!
The authors make a funny deduction that I can’t quite follow, that because the Denisova specimen’s mtDNA diverged from humans-neandertals some 1 million years ago, “it was distinct from the initial radiation of H[omo] erectus that first left Africa 1.9 million years ago, and perhaps also from the taxon H. heidelbergensis,” which is the name given to mainly European but also African fossils between 1 and 0.5 million years ago. I just don’t follow this. We don’t know what mtDNA diversity was like at any of these times, so there is no reason to think that this specimen’s ancestors were from some undocumented dispersal from Africa. The implicit assumption is that mtDNA lineages arise sporadically and discretely from Africa and then spread to different parts of the world, repeatedly over the course of human evolution. If there’s gene flow all around from the get-go, then the Denisova specimen simply represents an especially ancient mtDNA lineage – not necessarily an ancient population (recall that mtDNA is only inherited from mothers).
Oh well, should be interesting to see the nuclear DNA from this specimen, surely to be described in the near future…
Krause J, Fu Q, Good JM, Viola B, Shunkov MV, Derevianko AP, Paabo S. 2010. The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature, in press.

The earliest flute, and malaria resistance in baboons

Yesterday, two articles of interest to anthropologists were published in the the journal Nature‘s advance online publication. First is the announcement of a very complete bone flute, and fragments of other flutes, dating to around 35,000 thousand years ago from Germany. The finds come from the site of Hohle Fels in Southern Germany; a few months ago it was announced that the site produced the earliest Venus figurine. Venus figurines are some of the earliest pieces of carved art produced by humans, and are figures of corpulent women with corpulent lady-parts. This latter fact captures the popular imagination as the earliest ‘porn,’ but in truth no one’s sure what exactly they mean, although many researchers think they’re related to fertility. Anyway, the flutes are found in Aurignacian deposits, which by and large are attributed to ‘anatomically modern’ humans, as opposed to the contemporaneous Neandertals. The final sentences of the paper sum things up nicely:

“…early Upper Paleolithic music could have contributed to the maitenance of larger social networks, and thereby may have helped facilitate the demographic and territorial expansion of modern humans relative to culturally more conservative and demographically more isolated Neanderthal populations.”

I like their use of “culturally more conservative” description of Neandertals, whereas in the past the phrasing probably would have been “culturally primitive” or “…less advanced.” “Conservative” is certainly an interesting way to describe cultural differences between Neandertals and other Upper Paleolithic populations. I wonder if Neandertals were also more God-fearing and homophobic, as I understand ‘conservative’ to mean nowadays…

The second topic will have to wait. I just got invited to have dinner and drinks and watch soccer, which I’d be silly to pass up. Go South Africa!