Aurignacian

So a couple of weeks ago, the Journal of Biogeography published a paper arguing that humans and orangutans are sister taxa.

This week, the journal has published a paper on the biogeography of Sasquatch.

Yes, that's correct. The same journal that published the updated "red ape" paper has now published a Bigfoot paper.

OK, Journal of Biogeography, I'll be your straight man. I mean, I bow to no one in my ability to snark on human evolution, but this is like some sort of karmic singularity.

Besides, this Bigfoot paper is really good. The authors intend it as a "tongue-in-cheek" example, and it works on that basis, as an illustration of the "garbage in, garbage out" principle. Biogeographers have been using increasingly sophisticated computer algorithms to predict the "ecological niche" of species. The algorithms take information about sightings or recorded incidences of a species, find commonalities among those sightings against maps of other ecological data (rainfall, forest type, presence of other species, etc.), and spit out an ecogeographic distribution for the target species.

Of course, the algorithm will come to some result, regardless of how well each piece of data in the system is known. And the algorithms are complex enough that the creeping effects of errors may be hard to evaluate:

While the value of publicly available sample locality data is not questioned, the consequent introduction of errors in the accuracy of specimen identity and georeferencing could be problematic for developing ENMs [that is, "ecological niche models"] from public data sources (Graham et al., 2004; Soberón & Peterson, 2004). Although georeferencing inaccuracies can be identified in databases from qualitative or quantitative accuracy thresholds (e.g. http://manisnet.org/GeorefGuide.html), poor taxonomy and/or misidentification may be less detectable. This issue may be particularly problematic, for example, with cryptic species or subspecies that are morphologically similar but may have very distinct ecological requirements and geographic distributions, or for those data sources that contain indirect observations rather than references only to physical specimens.

What better way to illustrate the problem, than by applying the analytical methods straight to a "species" whose existence is, shall we say, "questionable."

The authors additionally raise one particular element of confusion that may enter into ecological niche modeling -- sightings of similar species may confound each other. They consider the example of black bears -- another large North American mammal that occurs in many of the areas where Bigfoot sightings are reported. They run the same analysis on black bears as they did on Sasquatch, finding a large overlap in distributions. But interestingly, they have fewer observations for bears than they do for Bigfoot -- leading them to an underestimate of the actual range of black bears. They reflect on the possible interpretations of the overlap:

Thus, the two 'species' do not demonstrate significant niche differentiation with respect to the selected bioclimatic variables. Although it is possible that Sasquatch and U. americanus share such remarkably similar bioclimatic requirements, we nonetheless suspect that many Bigfoot sightings are, in fact, of black bears.

From my perspective, this paper is important for two reasons, neither of them really having to do with large North American primates. First is a social and legal angle. Increasingly, the habitat distributions of endangered or threatened species are evaluated on the basis of similar computer models of ecological niche. In particular, the changes in species distributions under scenarios of climate change are modeled in this way. This computer modeling has the appearance of objectivity, and it certainly allows reams of data to be statistically simplified into human-readable maps. That makes the results of such analyses really valuable to cases where political and legal units need to make decisions about how to comply with threatened species regulations.

But if the data going into the model aren't correct, then the predictions of the models won't reflect reality. The question is, how much will they be wrong?

In this case, the limited black bear dataset leads to a substantial underestimation of the black bear habitat niche. And possible confusion between Sasquatch and black bear sightings raises the possibility that any rare species will be significantly overrepresented in ecological niche modeling when such confusions are possible. Neither of these outcomes tells us how bad such errors are likely to be, but they point to real weaknesses in the maps generated by these computer algorithms.

I expect that smart lawyers will be finding ways to use this Bigfoot paper a lot.

Second, I think the paper is important at this moment in paleoanthropology. Late last year, I wrote about a paper that evaluated ecological niche models for Neandertals and people who made the Aurignacian ("'Competitive exclusion' and the extinction of Neandertals: should we believe it?"). The paper, by William Banks and colleagues, had used the observed distribution of archaeological sites between certain radiocarbon date intervals to estimate an ecological niche model for the two hominid groups.

I think that paper was very good work, but it obviously is subject to uncertainties in the initial observations -- just as the Sasquatch data are. The archaeological observations add even more uncertainties of dating and certainty of association between biology and archaeology. And the Sasquatch data set is much, much larger in terms of sighting numbers; meaning that the archaeological cases ought to have more error, when it comes to evaluating niche flexibility.

For the purposes of the Banks et al. (2008) paper, I think their conclusions are pretty secure. They tested the hypothesis that the reduction of Neandertal occurrences over time could be explained by climate change; they were able to reject that hypothesis by showing the ecological niche breadth of earlier Neandertals included paleoenvironments that were very widespread across Europe throughout the period when they were declining. It's a nice demonstration.

But the Sasquatch example shows that we have to evaluate the ability of ecological niche modeling to test each hypothesis, on the basis of the data that are likely to be available. Can the model show that the spread of Aurignacian people caused the Neandertals to decline? That depends on our confidence about the dating and biological associations at early Aurignacian sites. The computer algorithm gives a structured way to reduce information that is already manifest in the data.

References:

Lozier JD, Aniello P, Hickerson MJ. 2009. Predicting the distribution of Sasquatch in western North America: anything goes with ecological niche modelling. J Biogeogr (early online) doi:10.1111/j.1365-2699.2009.02152.x

Banks WE, d’Errico F, Peterson AT, Kageyama M, Sima A, et al. (2008) Neanderthal Extinction by Competitive Exclusion. PLoS ONE 3(12): e3972. doi:10.1371/journal.pone.0003972

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 don't have much value to add to the "figurative art" angle to the Hohle Fels Venus figurine. It seems very interesting that there is a concentration of carved iconic figures in the Swabian Aurignacian. That has two elements -- first, the concentration itself; second, the focus on carved ivory. Other regional Upper Paleolithic variants have their own concentrations of unique artifacts, sometimes tools (like the Solutrean leaf point) other times found objects (like the fossil shells in the Belgian and German Magdalenian. And we know that other times and places in the Upper Paleolithic have carved objects, so here we have the combination of both, in a very early Upper Paleolithic culture.

I do think it's worth discussing the date of the figurine a little more closely. Conard's paper includes a nice short discussion of the difficulties of establishing an accurate chronology -- a bunch of dates are available spanning much of the sequence, and there is substantial mixing of older and younger dates across the sequence.

There is no simple explanation for the variable radiocarbon dates from Hohle Fels and Geienklösterle. The noisy signals result from a combination of factors including variable sample preparation, variable levels of atmospheric carbon, taphonomic mixing and excavation error. Given the lack of reproducibility within and between radiocarbon laboratories, I prefer to emphasize the stratigraphic context of the finds, and to use the highly variable radiometric dates as rough indicators of age8. Although there is no generally accepted calibration for radiocarbon dates over 30 kyr bp, preliminary calibrations suggest that dates of 32 kyr bp correspond to roughly 36 kyr bp in calendar years. If the early dates are correct, the Venus would be even older. The fact that the Venus is overlain by five Aurignacian horizons, containing a dozen stratigraphically intact anthropogenic features with a total thickness of 1 m, suggests that the figurine is of an age corresponding to the start of the Aurignacian, around 40,000 calendar years ago.

The paper also includes a very nice picture showing the stratigraphy profile of the site in terms of artifact positions, color-coded by level. The Venus does lie beneath a well-stratified Aurignacian, with a depth of in this area of more than a half meter, although I am also impressed by the overlying meter of "Gravettian-Aurignacian transition." Conard's text is slightly more definitive than the figure, since two of the five "overlying" Aurignacian layers are not represented directly above the artifact, and one appears mostly to underlie it.

The research report is accompanied by a perspective piece by Paul Mellars. He frames the importance of the site by referring to its early date:

Fragments of the figure were excavated from archaeological deposits in the Hohle Fels cave in south Germany, dated by a range of more than 30 radiocarbon measurements to at least 35,000 years in age (in terms of the newly 'calibrated' radiocarbon timescale) (Mellars 2009:176).

This is a tricky statement to parse. Conard provides eight radiocarbon dates for objects in the lowest Aurignacian level (Vb) at Hohle Fels, only two of these are older than 35,000 radiocarbon years. Mellars refers to calibrated dates, not radiocarbon dates. On that basis, the statement is likely correct but a little misleading in comparison with later, Gravettian-associated figurines, whose dates are reported in uncalibrated years.

For those not familiar with the arcana of radiocarbon dating, the atmospheric proportion of carbon-14 varied during the last 40,000 years, so that there was actually more or less of it at some times than others. For the oldest radiocarbon dates, up above 25,000 BP, the age reported in half-lifes is systematically younger than the real age of an object in calendar years (given in "years ago" or some such). Over the span above 30,000 years ago, the difference is up to 5000 years or more -- so that a radiocarbon date of 30,000 BP might correspond to a calendar date older than 35,000 years ago.

This creates the potential for much confusion when describing dates. In this case, what does it mean to see that a Venus figurine from the Aurignacian is "more than 35,000 years old" when other figurines from the Gravettian date to "25,000 BP"? There's a 5000-year gap between those two timescales -- one that amounts to a sixth of the total age of an artifact. And when we read that an object is "more than 35,000 years old" and remember that Neandertals lived up to "29,000 BP" it is very easy to forget that these dates may well be synchronous. So we have to continually remind ourselves to use comparable timescales when talking about objects in the Upper Paleolithic.

I've discussed the problems with radiocarbon calibration at some length, in association with some earlier work by Mellars. Sometimes I find that reading and learning more about a subject actually clarifies matters a bit. In the case of radiocarbon chronology, it seems that the more I learn, the more confused things really are.

Given the error associated with calibration and atmospheric variation, it is no surprise (as Conard reports in the paper) that the radiocarbon dates in a site over around 30,000 BP should be somewhat mixed and confused. The problem is not so much that ten objects from the same moment will have different proportions of carbon-14, it is that ten objects from different times may have the same proportion. So it is especially important to understand the stratigraphy of a site completely. This appears to be a good, conservative example, and it will be interesting to see what happens if the excavation progresses further into the deeper underlying Mousterian.

But meanwhile there are other sites, excavated in a range of circumstances, in which the stratigraphy was not so carefully documented, or may have been more mixed. I suspect we'll be hearing more confusion before we get a lot more clarification.

References:

Mellars P. 2009. Origins of the female image. Nature 459:176-177. doi:10.1038/459176a

Conard NJ. 2009. A female figurine from the basal Aurignacian of Hohle Fels Cave in southwestern Germany. Nature 459:248-252. doi:10.1038/nature07995

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.

I've been out of e-mail range for the past week. In the meantime several people e-mailed me this new paper:

Neanderthal Extinction by Competitive Exclusion

Background: Despite a long history of investigation, considerable debate revolves around whether Neanderthals became extinct because of climate change or competition with anatomically modern humans (AMH).

Methodology/Principal Findings: We apply a new methodology integrating archaeological and chronological data with high-resolution paleoclimatic simulations to define eco-cultural niches associated with Neanderthal and AMH adaptive systems during alternating cold and mild phases of Marine Isotope Stage 3. Our results indicate that Neanderthals and AMH exploited similar niches, and may have continued to do so in the absence of contact.

Conclusions/Significance: The southerly contraction of Neanderthal range in southwestern Europe during Greenland Interstadial 8 was not due to climate change or a change in adaptation, but rather concurrent AMH geographic expansion appears to have produced competition that led to Neanderthal extinction.

OK, so should we believe it?

The authors are out to test the idea that climate killed the Neandertals (also covered by me in 2007, not to mention "The unbearable hotness" from last week).

The authors confine their analysis to a simple question: Were the European ecologies of the later times of Neandertal existence compatible with those that existed slightly earlier? If the climate deterioration is insufficient to explain the range reduction of late Neandertal sites, then we need some other factor. Competition with the non-Neandertal population would be a logical hypothesis, in this event.

Competitive exclusion is not a new concept applied to Neandertals. The novel element in the paper is its inclusion of paleoclimate models to support the hypothesis that Neandertals and modern humans actually would have competed in the same niche.

The authors applied an optimization algorithm to data. The data included:

1. Paleoclimate predictions for small areal units within Europe for three time periods between 43,000 and 35,000 (calibrated) years ago.

2. The locations and dates of archaeological sites dating to these periods, whether Mousterian, Châtelperronian, or Aurignacian. The first two are assumed Neandertal, the third modern human.

The algorithm tries to find shared paleoclimate features among the locations represented by archaeological sites. Once these are found, the algorithm finds other areas that fit the same paleoclimate parameters as those where archaeological sites were found. In other words, it is an attempt to determine the total ecological range of the populations represented by the sites.

For example, here are the results for the earliest of the three time periods, H4. This is a comparison of the maps of Europe for both the Mousterian-Châtelperronian (left) and Aurignacian (right) archaeological samples:

In this map, red areas are those predicted to be suitable for habitation by Mousterian-Châtelperronian (left) and Aurigacian (right) populations, respectively. One thing stands out: they have almost identical ecological tolerances. Modern humans were not using different ecological zones than Neandertals. The analysis of the later periods shows that the modern humans were not exploiting climate changes at the expense of Neandertals.

The key graph of the paper shows that during the latest time period, near 35,000 years ago, the paleoclimate models predict a very large area of Europe would have been suitable for Neandertal habitation -- at least, if their habitation were constrained only by climate. But the Neandertal sites during that time period are restricted to a very small area. So some additional factor is required. The authors promote the hypothesis that the important factor was the population growth of modern humans.

Now, should we doubt the results? I think this is a good test of the hypothesis that climate change killed the Neandertals. It didn't. They survived through an entire glacial cycle before 40,000 years ago. Without some other factor, they would still be here today.

The paper is stronger than many that have tried to make a similar argument -- that climate couldn't have killed various extinct megafauna. In large part, that is because both the American megafaunal disappearances and the entry and growth of human populations coincided with a period of rapid climate change. In the time frame of the last Neandertals, there were important climate changes, but the paleoclimate models indicate that these changes weren't enough to make Europe uninhabitable for either humans or Neandertals.

The paper is not a test of Neandertal genetic extinction. It takes Neandertal population disappearance as a given. Models that involve gene flow or cultural exchanges between Neandertals and other populations are not part of this paper's scheme.

In this sense, the assumption that the archaeological industries can be analyzed with methods developed for species seems questionable. The paper acknowledges this issue:

Our assumption is that human adaptive systems, defined here as the range of technological and settlement systems shared and transmitted by a culturally cohesive population within a specific paleoenvironmental framework, can be considered to operate as a ‘species’ with respect to their interaction with the environment. This does not imply, however, that human adaptive systems necessarily remained stable over time, as might be the case with animal species occupying narrow and stable niches. Humans can change their adaptive systems rapidly through technical and social innovations in response to environmental change. We know, however, that this was not the case during the late Middle and Upper Paleolithic, periods during which specific human adaptive systems spanned a number of climatic events. Thus, the method described in this study is particularly relevant for addressing issues of human adaptive system stability and eco-cultural niche stability (Banks et al. 2008:2).

But Neandertals during the span from 43,000 to 35,000 years ago were adopting various Upper Paleolithic technological elements. That seems to contradict the assumption that the "technological and settlement systems...operate as a 'species'." Instead, it seems to indicate that these systems changed significantly across the time frame modeled in the paper. I don't think that observation weakens the hypothesis that modern and Neandertal populations may have competed in the same ecological niche. If the Neandertals were using the same technical elements, it probably reinforces the hypothesis of competition.

But I think it is important to bear in mind what the paper tested. The analysis rejects the hypothesis that climate was sufficient to drive a range restriction of Mousterian and Châtelperronian. It doesn't provide additional information about the mode of such restrictions. With that in mind, I admire the paper and see some useful additional work that might be tackled with similar methods.

References:

Banks WE, d’Errico F, Peterson AT, Kageyama M, Sima A, et al. (2008) Neanderthal Extinction by Competitive Exclusion. PLoS ONE 3(12): e3972. doi:10.1371/journal.pone.0003972