teeth

Writing about the Sarmiento-White exchange [1] [2] a couple of weeks ago, I mentioned that I had three areas of comment. The molecular clock argument was the first, the pelvis the second. My trip to Europe got in the way of finishing up these notes, but after the molecular clock and the pelvis, I've come to the third area -- the canine-promolar complex.

Here is Sarmiento's exposition:

Fourteen of the 26 characters in table 1 in (1) common to Ardipithecus and Australopithecus are in the canine/premolar complex. However, reliance on the canine/premolar complex to diagnose hominids (in the classic sense) has misdiagnosed Miocene fossil apes (i.e., Oreopithecus and Ramapithecus) as early human ancestors (12, 13). Character polarity for this complex is not clear-cut, with many early hominoids, especially females, often showing a humanlike condition. The canine/premolar complex shows such a marked grade of character lability (e.g., conspecific males and females show the diagnostic character differences) that reversals in polarity could have occurred repeatedly over the evolutionary periods necessary for these fossil genera to differentiate (12). Approximation to the humanlike canine/premolar complex, therefore, does not indicate that Ardipithecus is a hominid or ancestral to Australopithecus any more than it indicates that Oreopithecus and the orangutan-like females of Sivapithecus, both of which also share a humanlike premolar/canine complex, are hominids or represent a descendant-ancestor continuum.

Sarmiento here accepts that the C/P₃ complex of Ardipithecus "approximates" the hominin condition. I would not go so far as this. I faced a big difficulty in understanding the description of the dentition by Suwa and colleagues [3]. As I pointed out last fall, they did not report standard measurements. Those have been hidden from everyone. Moreover, most of the metric comparisons presented graphically in the paper and its supplement are non-standard ratios.

Such comparisons have many disadvantages. Many lack any clear biological meaning (for example, why take the ratio of lower P₃ height to M₁ length?). Why use the maximum diameter of the P₃ without any reference to the angle of the tooth relative to the mesiodistal axis?

A few things are clear from the description and photos of upper canines and lower third premolars in figure S14 of Suwa et al. [3]. Many of the Ardipithecus upper canines are worn on the tip, and some of them are worn extensively. None of them have "honing" wear, which means wear that enhances the cutting function of their distal edges. The upper canines of Ardipithecus are like male bonobos in their crown diameter and intermediate between male and female bonobos in their labial height. There are some similarly large canines in Australopithecus afarensis, although the average in that species is significantly lower in crown diameter.

Australopithecus afarensis has a range of P₃ forms. Some are more apelike, asymmetrical crowns dominated by a single buccal cusp and angled relative to the mesiodistal axis. Others are more humanlike, with two more or less equal cusps and perpendicular to the mesiodistal axis. In Au. afarensis, the more apelike The Ardipithecus range of variation apparently never included any like these latter, humanlike P₃s from Au. afarensis. The P₃s of Ardipithecus also had substantially greater crown heights than typical of Australopithecus. The Ardipithecus P₃ is hominin-like in only two senses: It is smaller than the chimpanzee equivalent, and never has a facet for honing wear on the upper canine. This may be why Suwa and colleagues (2009) and White and colleagues [2] referred to the "C/P₃ complex" instead of simply the P₃. It may also explain why the research paper by Suwa and colleagues [3] did not illustrate any comparative statistics of the P₃. The fact is that the P₃ of Ardipithecus is by itself apelike.

White and colleagues respond to Sarmiento's points as follows:

The greatly expanded Ar. ramidus dental sample now further obviates Sarmiento’s assertions by establishing a metrically and morphologically refined Ar. kadabba-Ar. ramidus-Au. anamensis-Au. afarensis morphocline (5–7). It now seems clear that not all recovered Ar. ramidus canines can be female (7). Feminization of the male Ardipithecus C/P3 complex is robustly documented [detailed in the supporting online material in (7)]...

Wait a minute! "Robustly documented?!" There are no measurements!

...and is incompatible with Sarmiento’s argument that Ar. ramidus represents the stem taxon for both African apes and humans (1). If that were the case, a hominid-like C/P₃ complex with lack of honing would need to have evolved in Ar. ramidus, only to have independently reverted to the honing complexes in each African ape clade.

White and colleagues here link two assertions. First, they assert that the C/P₃ complex in Ardipithecus is actually like later hominins. On that assertion, the facts listed above are the pertinent ones. There are dental similarities, many of which are also shared with one or more lineages of Miocene apes. As Sarmiento claims, these similarities are arguably "shallow" -- mostly they reflect the fact that Ardipithecus has smaller canines than chimpanzees.

Second, White and colleagues assert that the canine morphology of chimpanzees and gorillas is unlikely to represent an evolutionary reversal. This second assertion is taken up later in the comment:

The character distributions we noted in the pelvis, C/P₃ complex, and basicranium are consistently indicative of a sister relationship of Ar. ramidus with Australopithecus (and later hominids). For Ar. ramidus to be a stem species of the African ape and human clade as Sarmiento advocates, its highly derived C/P₃ complex morphology, basicranial shortening, and iliac structure must have first emerged in some yet-unidentified Miocene ancestor before then reverting to an African ape–like condition. Such multiple, nonparsimonious character reversals are highly unlikely.

Shouldn't a sympathetic editor would have stopped them from including this passage? Lovejoy and colleagues' "Great Divides" paper [4], in the special issue of Science, was completely devoted to the argument that chimpanzees and gorillas derived most of their locomotor adaptations in parallel to each other. That includes a series of postcranial derived features ranging from the lumbar spine, wrist, hand and foot, limb proportions and the pelvis. No matter what we may think of Ardipithecus, the dentitions of chimpanzees and gorillas also evince substantial parallelism in enamel and crown morphology.

True or not, none of that is parsimonious.

I don't see any reason why the C/P₃ complex should be special evidence of relationship. Lovejoy and colleagues [4] had given some attention to the idea that morphological characters might be genetically correlated through changes to toolkit genes. For no system is such genetic correlation as likely as for the dentition. The serial homology among neighboring teeth reflects the action of precisely the same genes in different segments established early in dental development. Moreover, unlike the case of digits and limbs, the teeth may mechanically affect each other's development because they are adjacent to each other. That means that neither morphological reduction of the canines nor any change in their eruption schedule can be isolated from changes in the premolars.

Is it any surprise that the reduction of upper canines should result in a lack of honing wear on lower premolars? Honing is a consequence of a direct mechanical connection that becomes impossible with sufficient reduction of the canine.

Can we isolate a slight reduction in the lower third premolars from the significant reduction in the lower canines? As Suwa and colleagues (2009:95) point out, this lower canine evolution is not limited to hominins but also occurred in parallel in bonobos and some Miocene lineages:

A hominid-like incisiform LC morphology (high mesial shoulder, developed distal crest terminating at a distinct distal tubercle) is seen in some female apes (e.g., Ouranopithecus and P. paniscus), whereas the LCs of Ar. kadabba and Ar. ramidus tend to be conservative, exhibiting a strong distolingual ridge and faint distal crest, typical of the interlocking ape C/P₃ complex (4) (Fig. 1 and SOM text S1).

I just don't think that the Miocene ape record can sustain the argument that the C/P₃ "complex" carries much phylogenetic weight. A bonobo-sized canine is never going to be strong evidence linking a fossil to the hominins. That's part of why Ardipithecus remains such a doubtful case.

References

Debbie Guatelli-Steinberg and Donald Reid report on the perikymata spacing of a sample of fourteen anterior teeth from Qafzeh. These are "early modern humans", among the earliest to be located outside of Africa, but their anatomical position relative to Neandertals and other groups has been subject to frequent dispute.

As I've emphasized several times ("Neandertal teeth: the other shoe", "How modern is "modern tooth development"?"), this growth characteristic of teeth is variable among living human populations. What remains totally unclear is why it varies.

Neandertals are at the low end of the human range of variation for perikymata counts on their anterior teeth, and the patterning of packing across the tooth is somewhat different. In particular, Neandertals have fewer perikymata nearer the roots of these teeth (for details, I suggest Guatelli-Steinberg's 2009 review article).

The current paper follows up on earlier work by Janet Monge and colleagues (2006). They emphasized that the Qafzeh anterior teeth fit within the overall human range of variation, but observed that two individuals were very close to Neandertals in their packing patterns. Here, Guatelli-Steinberg and Reid include more specimens in the sample, confirming this similarity.

From their conclusion:

The purpose of this study was to investigate whether Qafzeh teeth are different from those of modern humans in the percentage of perikymata present in their cervical [sic] appear to fall in the lower 50% of the modern human distribution, and a few fall within the lowest 5% of the distribution. Thus, this sample of Qafzeh teeth appears to differ from those of modern humans in the same direction that Neandertals do: with generally lower percentages of perikymata in their cervical regions. As can be seen in the SEM montages in Figure 2, perikymata become much more closely spaced in the cervical relative to incisal halves of the Inupiaq LI2 than they do in either the Neandertal or Qafzeh LI2s. Although sample sizes precluded a similar test between the Qafzeh and Neandertal teeth, plots of the averages for these teeth (Fig. 1a,b) reveal the similarity of the Qafzeh and Neandertal teeth, particularly for the UI2, LC, LI2, and LC. Values for two of the Qafzeh UI1s and a single UC are closer to the modern human than Neandertal means for these tooth types, revealing overlap in the ranges of values, as is also true for Neandertals and modern humans (Guatelli-Steinberg et al., 2007).

It may be worth pointing out that the perikymata packing pattern was a key part of Ramirez-Rossi and colleagues' conclusion that the Les Rois B mandible as well as several other Les Rois dental specimens show affinities to Neandertals.

I think Monge and colleagues are correct in asserting that this packing pattern is not a taxonomic diagnosis. Notwithstanding that the precise Neandertal-like pattern, present at Qafzeh, does not occur in the known human samples, we still don't know why human patterns differ from each other. In their discussion, Guatelli-Steinberg and Reid suggest alternatives for the mechanism forming the straiae, but I'd like to have some kind of genetic answer -- what developmental processes changed, carrying this feature along with them?

Anyway, another contrary observation to the idea of "modern human dental development", I guess.

References:

Guatelli-Steinberg D, Reid DJ. 2010. Distribution of Perikymata
on Qafzeh Anterior Teeth. Am J Phys Anthropol (in press). doi:10.1002/ajpa.21158

Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Nat Acad Sci USA 102:14197-14202. doi:10.1073/pnas.0503108102

Guatelli-Steinberg D. 2009. Recent studies of dental development in Neandertals: Implications for Neandertal life histories. Evol Anthropol 18:9-20. doi:10.1002/evan.20190

Monge JM, Tillier A-M, Mann AE. 2006. Perikymata number and spacing on early modern human teeth : Evidence from Qafzeh cave, Israel. Bull Mem Soc Anthropol Paris 18:25-33.

Ramirez Rozzi FV, d'Errico F, Vanhaeren M, Grootes PM, Kerautret B, Dujardin V. 2009. Cutmarked human remains bearing Neandertal features and modern human remains associated with the Aurignacian at Les Rois. J Anthropol Sci 87:153-185.

I pointed a couple of weeks ago to the Les Rois Neandertal paper by Ramirez Rozzi and colleagues.

In the new article section of Journal of Human Evolution, Shara Bailey, Tim Weaver and Jean-Jacques Hublin have a paper that examines the Les Rois sample (among many others) in terms of dental discrete traits. Basically, they set up a discriminant function that can tell Mousterian Neandertals from later Upper Paleolithic people with around 89 percent classification accuracy, and then they applied it to Aurignacian and Châtelperronian dental remains. Here's what they concluded about Les Rois (p. 13):

The analysis of the entire Les Rois sample (n = 15) showed that they have an overwhelmingly ‘modern’ signal. Fourteen of the fifteen individuals had high posterior probabilities of belonging to the Upper Paleolithic modern human group (>80%). This is not unexpected considering the teeth are associated with an Aurignacian industry (Dujardin, 2000) and most come from unit B, which has been dated to 28,715 ± 145 BP using AMS C14. One individual (Mandible B), however, was classified as Neandertal with a low posterior probability (54%) based on 13 traits.

Ramirez Rozzi (pers. comm.) has recently suggested that Mandible B represents a Neandertal, based largely on the asym-
metrical P4 together with some aspects of the corpus. Trinkaus (2007) has also argued that the specimens from Les Rois are mixed in morphology. While the P4 is asymmetrical, a large sagittal crack in the crown exaggerates this feature and the remaining aspects of the tooth are distinctively not Neandertal-like (it lacks a transverse crest and multiple lingual cusps: Fig. 6). In the end, we do not consider the posterior probability of 54% to be compelling enough to conclude, based on dental traits, that there were Neandertals present at Les Rois.

Ramirez Rozzi et al. (2009) made their conclusions about the Les Rois specimens mainly based upon perikymata packing patterns, secondarily supported by tooth sizes and the dental nonmetrics used here. So they are really concluding the same thing about mandible B. What's interesting is that Ramirez Rozzi and colleagues find several other dental individuals from the earlier unit with similar enamel formation patterns, and which they claim are also Neandertals.

In some senses, Les Rois is a good case study for how more complete specimens come to dominate the discussion to the exclusion of other fragmentary remains. Mandible B is itself a tiny piece of a skeleton, but because it has several different anatomical elements on that little piece, the two papers can conduct this kind of in-depth analysis. But the status of the other isolated teeth are equally important -- if Ramirez Rozzi and colleagues are right, they might be enough to establish the earlier Les Rois sample as standing apart from other early Aurignacian-associated samples. If we're talking about a single specimen, however well documented, the situation is somewhat different.

As everybody knows, my null hypothesis is that the samples are mixed in their morphological pattern. On that topic, the more interesting implication of the study by Bailey and colleagues (2009) is that when they applied their discriminant function to Châtelperronian samples, they got a similar classification frequency to Neandertals as for earlier Neandertal samples. And when they applied their function to Aurigacian samples, they got a similar classification frequency to modern humans as for later Upper Paleolithic samples. Under the hypothesis of a mixed transition from earlier Neandertals through later Châtelperronian Neandertals into early Aurignacian and into the Upper Paleolithic, you'd expect the intermediate time steps to give a lower classification frequency -- more Neandertal-like in Aurignacian than later; more modern-like in Châtelperronian than earlier. Bailey and colleagues found that their function classified 85 percent of Aurignacian dental individuals as modern (29/35) compared to 89 percent of later Upper Paleolithic individuals (56/63). Those numbers aren't significantly different, and given the variability in completeness of assigned specimens, I wouldn't go farther.

One possible criticism of the paper is that the morphological pattern that makes up the discriminant mostly consists of traits that are shared by both groups but differ in frequencies. It is still quite possible to use the traits to discriminate individual specimens, but somewhat harder to interpret what a change in trait frequencies means in genetic terms. Bailey and colleagues recognize this issue, and raise it in their discussion of the Oase 2 specimen, for example (p. 12):

Given that the cranium of Oase 2 is clearly not that of a Neandertal (Rougier et al., 2007), the assignment of this individual to the Neandertal group was unexpected. Trinkaus (2007) has suggested that, while essentially ‘modern,’ both Oase 1 and 2 exhibit a mosaic of cranio-dental features, some of which are archaic (e.g., dental proportions, long and flat frontal bone), and others apparently derived towards anatomically modern humans (parietal curvature, absence of supraorbital torus) or towards Neandertals (unilateral lingual bridging of the mandibular canal).

It is important to note that the dental traits aligning Oase 2 with Neandertals are archaic in nature, as they are observed in other fossil hominins as well (Bailey, 2002b, 2006; Martínon-Torres et al., 2007). It is unfortunate that incisor morphology could not be assessed (teeth are missing), and that the upper M1s are too worn to ascertain occlusal polygon shape and occlusal polygon area, since these are features that are likely derived for the Neandertals/Neandertal lineage (Bailey, 2004; Gómez-Robles et al., 2007). Considering that some of the most diagnostic features of the upper dentition could not be assessed and that our approach is not 100% accurate, we caution against over-interpreting the classification of Oase 2.

That's the basic problem of comparing Neandertals with humans, which we encounter genetically as well as morphologically. The groups differ in the frequencies of traits, but not often in the exclusive presence of distinctive ones. Sometimes, what once looked like a distinctive trait is then found in the other group -- so it's not distinctive anymore! Some researchers focus on "distinctive combinations" of traits, which tend to include a mixture of primitive and derived morphologies. But differences in trait frequencies automatically lead to differences in the combination of traits. Sometimes combinations are disproportionately represented (that is, putting traits together separates the samples more than considering them individually), but it is unclear how much of a trait combination may be explained by a history of inbreeding (in isolated populations) and how much may be explained by pleiotropy (of a few genes that differ in frequency).

You'd think this problem would be easier than it is. But look at Les Rois -- a fragmentary but interesting sample, with a blend of morphologies in different specimens. How do we interpret the similarity of Les Rois mandible B to Neandertals? Is it a Neandertal? If we considered the dental nonmetric features alone, as Bailey and colleagues suggest, the specimen looks like a Neandertal but with really rather weak evidence. If we add the perikymata and size data, the similarities with Neandertals are increased, and other teeth from the site also tend to look more Neandertal-like. But we know that perikymata patterns vary in recent human populations. How should we consider this variation as we compare the Les Rois teeth -- should we consider Europeans only, or modern humans more broadly? How did those traits change within the last 30,000 years, and is that relevant to the 10,000 years before?

Well, it's certainly enough to keep things interesting. I'm raising a lot more questions than offering answers. I like the approach Bailey and colleagues have taken because it includes much of the available sample in a way that can be considered as a unit. But then when we return the the issue of particular specimens and the possible patterns of genetic causation of the traits, we are left with the same problems as before.

References:

Bailey SE, Weaver TD, Hublin J-J. 2009. Who made the Aurignacian and other early Upper Paleolithic industries. J Hum Evol (in press) doi:10.1016/j.jhevol.2009.02.003

I said I was going to do my best to scoop the press this week. How about this piece of undernews: at one of the few early Aurignacian sites to preserve skeletal remains, Les Rois, France, one of the Aurignacian-associated mandibles looks like it may have been a Neandertal.

Before I tell the whole story, let me telegraph the bottom line: Do I think this specimen was really an Aurignacian Neandertal?

My opinion has always been that Europeans in the time span from 40,000 to 25,000 radiocarbon years presented a varying mixture of "Neandertal" and "modern" morphological features. From that standpoint, it is not surprising to find a mandible that has the combination of features reported here. In this case, the most significant mandible (which is really quite a small fragment) shows one very interesting characteristic: a perikymata count and packing pattern similar to Neandertals and different from other Upper Paleolithic European teeth. But as I'll point out below, living humans are variable in their enamel formation in ways that reduce the significance of the differences between Neandertals and later Europeans.

But the story is significant -- not only do these remains extend the biological variability of known Aurignacian-associated people to include Neandertal-like developmental patterns, but also they help to inform us about the potential of cultural associations at other sites, including Vindija.

Joel Garreau (Radical Evolution) covers the future genetics beat for the Washington Post. In today's edition, he has an interesting article about tooth regeneration from stem cells:

As long as there are hockey players, there will be niche markets for false teeth. But the real news about the future of dentures is that there isn't much of one. Toothlessness has declined 60 percent in the United States since 1960. Baby boomers will be the first generation in human history typically to go to their graves with most of their teeth.

And now comes tooth regeneration: growing teeth in adults, on demand, to replace missing ones. Soon.

Naturally, as a paleoanthropologist, this topic is near to my heart. The teeth are one of the better-understood developmental systems, at least in mice. Being a couple hundred million years old, the genetic program that builds the teeth is admirably modularized.

The story traipses through the cultural meaning of tooth loss and its relation to senescence and health risks like smoking and diet. Best line:

If you are one of those obedient doobies who listened to your dentist and had your wisdom teeth removed for no particularly urgent reason, you are hosed.

Well, my twin daughters are losing their teeth now, but I feel no urge to save their baby teeth in liquid nitrogen like some of the subjects of the article. That's just crazy talk.