Dietary divergence of robust australopithecines

I’m writing a review of the “robust” australopithecines, and I’m reminded of how drastically our understanding of these hominins has changed in just the past decade. Functional interpretations of the skull initially led to the common wisdom that these animals ate lots of hard foods, and had the jaws and teeth to cash the checks written by their diets.

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Comparison of a “gracile” (left) and “robust” (right) Australopithecus face, from Robinson (1954).

While anatomy provides evidence of what an animal could have been eating, there is more direct evidence of what animals actually did eat. Microscopic wear on teeth reflects what kinds of things made their way into an animal’s mouth, presumably as food, and so provide a rough idea of what kinds of foods an animal ate in the days before it died. Microwear studies of A. robustus from South Africa had confirmed previous wisdom: larger pits and more wear complexity in A. robustus than in the earlier, “gracile” A. africanus suggested more hard objects in the robust diet (e.g., Scott et al., 2005). A big shock came a mere 8 years ago with microwear data for the East African “hyper robust” A. boisei: molars had many parallel scratches and practically no pitting, suggesting of a highly vegetative diet (Ungar et al. 2008).

robust microwear

Microwear in A. boisei (blue) and A. robustus (red). Although they overlap mostly for anisotropy (y-axis), they are completely distinct for complexity (x-axis). Data from Grine et al. (2012) and skull diagrams from Kimbel et al. (2004).

Stable carbon isotope analysis, which assesses what kinds of plant-stuffs were prominent in the diet when skeletal tissues (e.g. teeth) formed, further showed that the two classically “robust” hominins (and the older, less known A. aethiopicus) ate different foods. Whereas A. robustus had the carbon isotope signature of an ecological generalist, A. boisei had values very similar to gelada monkeys who eat a ton of grass/sedge. GRASS!

robust isotopes

Stable carbon isotope data for robust australopithecines. Data from Cerling et al. (2013) and skull diagrams from Kimbel et al. (2004). Note again the complete distinction between A. robustus (red) and A. boisei (blue).

ResearchBlogging.orgWhile microwear and isotopes don’t tell us exactly what extinct animals ate, they nevertheless are much more precise than functional anatomy and help narrow down what these animals ate and how they used their environments. This highlights the importance of using multiple lines of evidence (anatomical, microscopic, chemical) to understand life and ecology of our ancient relatives.


Cerling TE, Manthi FK, Mbua EN, Leakey LN, Leakey MG, Leakey RE, Brown FH, Grine FE, Hart JA, Kaleme P, Roche H, Uno KT, & Wood BA (2013). Stable isotope-based diet reconstructions of Turkana Basin hominins. Proceedings of the National Academy of Sciences, 110 (26), 10501-6 PMID: 23733966

Grine FE, Sponheimer M, Ungar PS, Lee-Thorp J, & Teaford MF (2012). Dental microwear and stable isotopes inform the paleoecology of extinct hominins. American Journal of Physical Anthropology, 148 (2), 285-317 PMID: 22610903

Kimbel WH, Rak Y, & Johanson DC (2004). The Skull of Australopithecus afarensis. Oxford University Press.

Robinson, J. (1954). Prehominid Dentition and Hominid Evolution Evolution, 8 (4) DOI: 10.2307/2405779

Ungar PS, Grine FE, & Teaford MF (2008). Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PloS One, 3 (4) PMID: 18446200

eFfing Fossil Friday: Feces

As we saw in last week’s FFF, Spain has some of the best human fossils. Now it also has some of the shittiest. I mean this literally, not figuratively: archaeologists working at at the ~50 thousand year old site of El Salt have found the oldest known human poop:

Neandertal coprolite

Party pooper. Left is a picture of the coprolite, right is the inset blown up. Top is regular color, bottom is under polarized light (Fig. 1D from Sistiaga et al. 2014).

Any nerd worth their el salt has surely seen/read Jurassic Park, and will recall that there’s a lot to be learned from poop. Paleontologists even have a technical term for fossilized feces – “coprolite.”  The coprolite from El Salt was excavated from a hearth (if I’m reading “combustion layer” correctly), meaning that 50,000 years ago some jerk Neandertal ruined the campfire and subsequently the whole camping trip. Analysis of the stool’s sterols and (copro-) stanols (the chemical residuals of digesting plant and animal food) adds to previous findings that Neandertals ate plants and not only meat. However, the stanol profile suggests that the majority of the diet came from meat rather than plants. Because coprostanol is created by gut microbes, this study potentially paves the way to reconstructing Neandertals’ gut microbiome. Like I said, there’s a lot to be learned from poop.

The article, by Sistiaga and colleagues and published in PLoS One, contains lots of interesting information about the digestive process that I for one didn’t know. It’s totally open access, so it’s completely free for all. Go read it now!

Historical contingency and an herbivorous calamity

This post was chosen as an Editor's Selection for

A while ago I asked, “What the hell was Australopithecus boisei doing?” To recap: there’s this weird side branch of human evolution that was dubbed “Australopithecus boisei” and lived in Eastern Africa from around 2.3 – 1.4 million years ago. They lived right alongside our ancestors, early Homo. If you think human diversity is remarkable today, you’d be totally blown away by the diversity of the early Pleistocene. Since 1959 when A. boisei (then Zinjanthropus boisei) was first discovered, people noticed its massive molar and premolar teeth, thick and powerful jaws, and muscle markings indicative of diabolical chewing power. ‘Probably subsisted on a diet of low-quality, hard to chew foods,’ people reasoned.

But a few years ago, this picture changed: evidence from toothwear and the chemical composition of teeth suggested A. boisei was actually eating grass or sedges (see the referred post or a nice recent review by Julia Lee-Thorp for more info). Such a diet is totally at odds with what people had hypothesized based on the size of the chewing muscles and teeth.

Colobus molars, good for shearing apart leaves. (image:

I was discussing this last point with a colleague the other day, who could not believe A. boisei ate grasses or the like: Many animals known to eat grass or leaves tend have molars with high crowns with slicing edges for shearing apart a mouthful of vegetation (above), but A. boisei molars are large and low-cusped, becoming fairly flat with wear (below).

Australopithecus boisei specimen KNM-ER 15930 (Leakey & Walker 1988, Figure 8)
But, it occurred to me, maybe high-crowned, shearing molars simply were not an ‘option’ in the evolution of Australopithecus boisei. Natural selection is a powerful force of evolution, but it is limited because it can work only with existing variation: it does the best it can with what it’s got. The earliest surefire hominins, Australopithecus anamensis and afarensis, certainly did not have ‘cresty’ molars with pointy cusps, and neither did many late Miocene apes, for that matter. Rather, the ancestors of A. boisei had fairly low bulbous molar cusps, and that’s some serious evolutionary baggage for a hominid hoping to corner the grass and sedge market.
So we can draw up the following hypothesis for the evolution of A. boisei: as the early members of the species moved into a niche of eating grass/sedges, rather than evolve cresty teeth, they increased the size and enamel thickness of their ancestors’ molars to better-withstand their diet. Perhaps this was the ‘easiest’ solution to adapting teeth to a crappy diet (maybe some developmental constraint?). Or perhaps there’s another, yet unidentified food responsible for the species’ curiously high-C4 diet … who knows? Nota bene: this isn’t necessarily what I think happened, it’s just a hypothesis consistent with current evidence about A. boisei‘s anatomy and diet.
If Life on Earth has taught us anything, it’s that there are many ways to do the same thing. What’s more, evolution is highly constrained by pre-existing biology and historical circumstance. Australopithecus boisei may have been ‘a victim of its times,’ forced into an herbivorous niche for which it was ill-equipped.
Leakey RE, & Walker A (1988). New Australopithecus boisei specimens from east and west Lake Turkana, Kenya. American Journal of Physical Anthropology, 76 (1), 1-24 PMID: 3136654
Lee-Thorp, J. (2011). The demise of “Nutcracker Man” Proceedings of the National Academy of Sciences, 108 (23), 9319-9320 DOI: 10.1073/pnas.1105808108
*Edited 07 Nov 2015

Dmanisi Homo erectus: I’ll have what she’s having

Speaking of diet in fossil humans … Herman Pontzer and buddies just published a brief analysis of fine-scale tooth wear in the Dmanisi Homo erectus specimens.


Teeth are useful as hell in life. Humans’ teeth are critical not only for eating, sporting a sexy smile, and biting people (right), but also for speech and song (“f,” “th” and “v” sounds). Some parents even harvest their childrens’ exfoliated baby teeth. The things we do with teeth.

Teeth are also really useful for studying long-dead people and animals – teeth may preserve pretty well for millions of years, they can be used to estimate an individual’s age-at-death, and their shape and composition can be used to learn about diet. In a vile act of revenge, the food that sustains us also scrawls its Nom Hancock into the surfaces of our teeth. So, scientists can study the microscopic marks (= “microwear”) on tooth surfaces to see what kinds of foods were eaten shortly before death. Peter Ungar, an author of the current paper, has done a lot of work here, and his website is worth checking out if you’re interested in learning more. Microwear can’t really tell you exactly what an animal was eating, but can tell you whether the animal mostly ate grasses, leaves, hard objects like nuts, and so forth.

So Pontzer and colleagues (in press) examined the microwear on some of the lower molars of the youngest members of the nearly 1.8 million year old (Ferring et al. 2011) Homo erectus group from Dmanisi in the Republic of Georgia. To the left is a picture of the jaws, from the paper (from another paper. How meta of me). The microwear patterns of these badass early humans fit cozily within the variation exhibited by other Homo erectus specimens.

Microwear in Homo erectus is pretty variable, but still rather distinct from other fossil groups like robust Australopithecus, and a little less distinct from their putative ancestor H. habilis. This suggests that something special about Homo erectus was the species’ great dietary breadth – Homo erectus‘ key to colonial and evolutionary success might not have been the adoption of a key dietary resource, but rather the ability to utilize a wide range of food resources. Atkins diet be damned. What’s neat is that the Dmanisi hominids, though kind of primitive (Australopithecus-like) in terms of brain size and some aspects of skull shape, nevertheless demonstrated key behaviors of H. erectus, namely colonization (Dmanisi is the oldest reliably-dated hominid site outside Africa), and dietary flexibility. This really suggests the success of our ancestors was due to some behavioral innovation, aside from advances in stone tool technology.


Now, these Dmanisi H. erectus kids’ teeth wore like other H. erectus, and it would be reasonable to infer that this is because they ate similar foods. This makes it all the more mysterious that the other Dmanisi jaws, from older adults, have teeth completely worn to shit (sorry to swear). D3444/3900 (left) are the cranium/mandible of an individual who was missing all their teeth, except maybe a lower canine – the earliest example of edentulism in the human fossil record (Lordkipanidze et al. 2005). D2600 (below) is a very large mandible with teeth so worn that the pearly-white first-molar crowns were gone and the internal pulp cavity (and nerve) were exposed. (Interestingly, D2600 is so large that some researchers initially argued it represented a different species from the other jaws – yet Adam Van Arsdale presented evidence that this extreme tooth wear may actually be responsible for making jaws relatively taller in early humans).

So what’s curious is why the older Dmanisi hominids should show such an extreme amount of tooth wear compared to other H. erectus, but microwear on the young suggests their diet was the same (that is, just as diverse in texture) as others in the species. Was Dmanisi-level tooth wear (and tooth loss) comparable to other H. erectus, and we just happen not to have found them at other sites? (KNM-ER 730 from Kenya is the next-most worn early Homo that next comes to mind) Is there another aspect of diet we don’t know about, that caused the Dmanisi teeth to wear especially quickly? Or were these early Homo from Dmanisi actually living longer than other H. erectus? I suspect the second is more likely, but that’s a hypothesis that remains to be tested.
Read more, dammit!
Ferring, R., Oms, O., Agusti, J., Berna, F., Nioradze, M., Shelia, T., Tappen, M., Vekua, A., Zhvania, D., & Lordkipanidze, D. (2011). From the Cover: Earliest human occupations at Dmanisi (Georgian Caucasus) dated to 1.85-1.78 Ma Proceedings of the National Academy of Sciences, 108 (26), 10432-10436 DOI: 10.1073/pnas.1106638108
Lordkipanidze, D., Vekua, A., Ferring, R., Rightmire, G., Agusti, J., Kiladze, G., Mouskhelishvili, A., Nioradze, M., de León, M., Tappen, M., & Zollikofer, C. (2005). Anthropology:  The earliest toothless hominin skull Nature, 434 (7034), 717-718 DOI: 10.1038/434717b
Pontzer H, Scott JR, Lordkipanidze D, Ungar PS. In press. Dental microwear texture analysis and diet in the Dmanisi hominins, Journal of Human Evolution (2011). DOI:10.1016/j.jhevol.2011.08.006

Data, development and diets

As mentioned briefly but repeatedly on this blog, my dissertation is about growth of the lower jaw in Australopithecus robustus (right), comparing it with jaw growth in recent humans. This is important because we don’t really know exactly how skeletal-dental (especially skeletal) maturation of our fossil relatives compares with us today. From a developmental perspective, it is also important to know how and when adult form arises during growth, and how these processes vary within and between species.

It’s not easy to examine ontogeny in fossil samples. In a post a few weeks ago I included a drawing of some of the A. robustus juvenile jaws. At the time, I was pointing out variation in dental maturity (which is a nice thing when studying growth), but the picture also reveals a bigger bugbear – variable preservation of features (which is a terrible thing if you’re trying to study growth).

For example, the youngest individual in the fossil sample (right, viewed from above, front is at the top of the picture) includes only the second baby molar tooth, a bit of the bone surrounding the sides and back of the tooth, and a small portion of the ascending ramus. The oldest subadult in the sample (SKW 5), on the other hand, is almost entirely complete. In between these ages, jaws variously preserve different parts. Under these circumstances (i.e. lots of missing data), growth cannot be studied by traditional (namely, multivariate) methods (how I will deal with this is a topic for another day).

So while studying the fossils in South Africa, in order to maximize the number of comparisons I could possibly make, I measured just about every single linear dimension conceivable on these jaws. I thus have a spreadsheet with 300 columns of measurements I could take on each specimen. Most of the cells are empty : (

What’s a boy to do?! In order to compare A. robustus with humans, I need to take the same measurements on a growth series of human jaws, too. But life is short, and if I want to finish this project before I succumb to some sinister signature of senescence, I really can’t take hundreds of measurements on a human sample which is much larger than the fossils. Plus, a lot of the individual measurements are a bit redundant: some of the distances overlap, many of the variables can be taken on the right and the left sides, etc.

If I am to finish collecting data in a reasonable time frame, I need to cull my variables from 300 to however many (a) maximizes the comparisons I can make within the less-complete A. robustus sample, and (b) are not too repetitive. Boo. Plus I have to get these spreadsheets ready to be read and analyzed in the program R, which for whatever reason is always a pain in the ass.

Again, the statistics of the overall comparisons is a topic for another day, and I haven’t had the opportunity yet to write the analytical program(s). But I have looked at some individual traits in A. robustus compared with a subsample of humans. For example, at the left is a plot of changes in height of the jaw at the baby second molar or adult second premolar (which replaces the baby molar). Obviously my human sample is way to small at the moment to make any really meaningful statements about how growth compares between the two species. Note also that these are absolute measures and not size-corrected, and that these are stages of dental eruption rather than chronological ages. But from this preliminary view, the two species are very similar up to around when the first adult molar comes in (“stage 4” here). Thereafter, the A. robustus individuals dramatically increase in size rather fast, whereas humans only slowly increase in size.

Again, this is a very preliminary result, and only for a single measurement. But it is interesting in light of a recent study by Megan Holmes and Christopher Ruff (2011). These researchers compared jaw growth recent humans who differed in the consistency of their diets. They found that kids in the two populations were not too different, but the samples became more different with age to become fairly different as adults. Now, A. robustus seems to have eaten a diet with lots of hard objects (see recent review by Peter Ungar and Matt Spohneimer), but humans’ diet (and technology) really obviates the need for chewing as powerful as seen in A. robustus. So this dietary divergence may well be reflected in the growth difference suggested above, but it may not be the sole factor. PLUS I NEED TO INCREASE MY HUMAN SAMPLE.

Stay tuned for more analyses and results!

ResearchBlogging.orgReferences to make you smarter and stronger
Holmes, M., & Ruff, C. (2011). Dietary effects on development of the human mandibular corpus American Journal of Physical Anthropology, 145 (4), 615-628 DOI: 10.1002/ajpa.21554

Ungar, P., & Sponheimer, M. (2011) The Diets of Early Hominins. Science 334(6053), 190-193. DOI: 10.1126/science.1207701  

Culinary trends in an extinct hominid

A few weeks ago I discussed a recent paper that analyzed the carbon and oxygen isotope ratios from Australopithecus boisei molars (Cerling et al. 2011). The major finding here was that an enlarged sample (n=24 more) corroborated earlier isotopic (van der Merwe et al. 2008) and tooth wear evidence (Ungar et al. 2008) that A. boisei probably did not subsist on as much hard foods as previously thought. Although this strange hominid probably ate mostly grass/aquatic tubers, some researchers think it may have looked something like this:
Left, A. boisei reconstructed skull, from McCollum (1999, Fig. 1). Right, artist’s reconstruction of what the individual on the left may have looked like during life.
But looking at the numbers I’m wondering if the carbon isotopes reveal anything more about this curious hominid. If we plot boisei‘s carbon 13 values against the fossils’ estimated ages, there’s a small hint of a temporal trend, of increasing carbon 13 levels over time (more C4 plant consumption). Fitting a line to these data does indicate an increasing C4 component over time, but the slope of the line is not significantly different from zero. The early, high value could be an outlier (not eating the same stuff as his/her peers?), although the lowest carbon 13 value of all that would support this trend is also much lower than the other values; it could be a more anomalous one. So while it’s tempting to hypothesize dietary change over time in A. boisei, at the moment it looks like you can’t reject the hypothesis that diet is consistent throughout the Pleistocene until the A. boisei’s demise.  Supporting dietary stasis, Ungar and colleagues (2008) reported similar molar tooth wear in specimens from 2.27-1.4 million years ago.
In addition, Cerling and colleagues sampled at least one of each of the cheek teeth. Because teeth form in the jaws in a sequence (not all at the exact same time), the isotopic signatures from given teeth represent the dietary intake of carbon at various different points in an individual’s childhood. In the figure below I lumped upper and lower teeth together; the un-numbered “M” indicates molars unassigned to a specific position.

The first molar crown starts to form right around birth, and note here that it’s carbon 13 values are slightly higher than the other molars. The premolars and second molar start to form around the same time, so it is curious that each of these teeth show distinctly different ranges of carbon 13 levels. The sole P3 is also the lowest value (eating fewer C4 plants) in the entire sample, but the P4 has less negative values (eating more C4 plants). Not sure what’s going on here, but maybe later analyses of more specimens will clarify the situation.
Our australopithecine ancestors and cousins have proven to be a rag-tag bunch of funny bipeds, and A. boisei has proven to be one of the weirder ones, in my opinion. Of course descriptions of Ardipithecus ramidus and Australopithecus sediba skeletons have been recent reminders that we have lots left to learn about Pleistocene hominids. For my part, I’m interested in working out the deal with the group of “robust” Australopithecus.
Cerling, T., Mbua, E., Kirera, F., Manthi, F., Grine, F., Leakey, M., Sponheimer, M., & Uno, K. (2011). Diet of Paranthropus boisei in the early Pleistocene of East Africa Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1104627108
McCollum, M. (1999). The Robust Australopithecine Face: A Morphogenetic Perspective Science, 284 (5412), 301-305 DOI: 10.1126/science.284.5412.301
Ungar PS, Grine FE, & Teaford MF (2008). Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PloS one, 3 (4) PMID: 18446200
van der Merwe NJ, Masao FT and Bamford MK. 2008. Isotopic evidence for contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania. South African Journal of Science 104: 153-155

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