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.

REFERENCES

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

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Bioanthro lab activity: What species is it?

We’re learning about the divergence between robust Australopithecus and early Homo 2.5-ish million years ago in my Human Evolution class this week. Because of this multiplicity of contemporaneous species, when scientists find new hominin fossils in Early Pleistocene sites, a preliminary question is, “What species is it?”

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Scrutinizing the fossil record, asking the difficult questions. (Science credit)

To help my students learn how we know whether certain fossils belong to the same species, and to which group new fossils might belong, in this week’s lab we compared tooth sizes of Australopithecus boisei and early Homo. After seeing how tooth sizes differed between these groups, students then tested whether they could determine whether two “mystery” fossils (KNM-ER 60000 and 62000; Leakey et al. 2012) belonged either group.

Early Pleistocene hominin fossils from Kenya. Left to right: KNM-ER 406, ER 62000 and ER 1470.

Early Pleistocene hominin fossils from Kenya. Left to right: KNM-ER 406, ER 62000 and ER 1470. At the center is one f the lab’s “mystery jaws.”

Students downloaded 3D scans of hominin fossils from AfricanFossils.org, and measured buccolingual/labiolingual tooth crown diameters using MeshLab.

Early Pleistocene hominin mandibles. Left to right: KNM-ER 3230, ER 60000 ("mystery" jaw) and ER 1802.

Early Pleistocene hominin mandibles. Left to right: KNM-ER 3230, ER 60000 (“mystery” jaw) and ER 1802.

The first purpose of this lab was to help familiarize students with skull and tooth anatomy of early Pleistocene humans. Although lectures and readings are full of images, a lab activity forces students to spend time visually examining fossils. Plus, they’re in 3D which is a whole D greater than 2D – the visual equivalent of going to eleven! The second goal of the lab was to help prepare students for their term projects, in which they must pose a research question about human evolution, generate predictions, and find and use data to test hypotheses.

If you’re interested in using or adapting this activity for your class, here are the handout and data sheet into which students enter their measurements. The data sheet specifies the fossils that can be downloaded from africanfossils.org.  Some relevant fossils (i.e., KNM WT 15000 and ER 992) were not included because the 3D scans yield larger measurements than in reality.

Lab 3-Mystery Jaws (instructions and questions)

Lab 3-Mystery jaws data sheet

ResearchBlogging.orgReference
Leakey MG, Spoor F, Dean MC, Feibel CS, Antón SC, Kiarie C, & Leakey LN (2012). New fossils from Koobi Fora in northern Kenya confirm taxonomic diversity in early Homo. Nature, 488 (7410), 201-4 PMID: 22874966

Gracile & robust Australopithecus

Last week, I introduced my Human Evolution students to the “robust” australopithecines. It was a very delicate time, when we had to have a grown up, mature conversation about adult things. I reminded the students that they’re only human, but they must resist urges that seem only natural. No matter how much they want to, even if their friends are doing it, they must not act on the deep, dark desire to say that “robust” vs. “gracile” Australopithecus differ in their body build.

Don't do it, Homo naledi. Don't talk about body size when you mean to talk about jaw and tooth size. Illustration by Flos Vingerhoets.

Don’t do it, Homo naledi. Don’t talk about body size when you mean to talk about jaw and tooth size. Illustration by Flos Vingerhoets.

Every semester, students (who don’t read and/or pay attention to lecture) think that the difference between these two groups has to do with the species’ body sizes. This is a misconception that has reached the highest echelons of reference:

At least one person is not citing their source here. F-.

Apple and Google, at least one person here is not citing their source: F-. Also, is no one else surprised that this term is allegedly specific to anthropology?

No. In the case of australopiths, “gracile” and “robust” refer to the relative size of the jaws, teeth and chewing muscles (all contributing to the “masticatory apparatus”). Traditionally,  graciles include the ≥2 million year old Australopithecus afarensis and africanus, and robusts include the later A. boisei and robustus. The discovery of an A. aethiopicus cranium (Walker et al. 1986) somewhat blurred the lines between the two groups but it is usually included with the robusts (who are often collectively called Paranthropus). John Fleagle’s classic textbook (1999) illustrates the gracile-robust dichotomy very nicely:

Comparison of gracile (left) and robust (right) craniodental traits. From Fleagle, 1999.

So to recap: Jaws and teeth, people! To the best of my knowledge, there’s little or no evidence that the various australopithecines differed appreciably in body size (McHenry and Coffing, 2000), stoutness, or muscularity. Although the OH 80 partial skeleton, attributed to Australopithecus boisei  based on tooth size and proportions, includes a humerus with very thick cortical bone and a radius with a crazy big insertion for the biceps muscle – it was a very large and muscular A. boisei (Domínguez-Rodrigo et al., 2013). Nevertheless, gracile and robust australopithecine species differ most notably in their jaws and teeth, not bodies. Maybe this is why Liz Lemon was so confused about the term “robust”?

Today, these are somewhat antiquated terms. Back when the only hominins known to science were the species listed above, it was easy to make a distinction. However, as the fossil record has expanded of late, the gracile-robust dichotomy becomes blurry. Australopithecus garhi (Asfaw et al., 1999) has overall tooth proportions comparable to graciles, but absolute tooth sizes and sagittal cresting like robusts. The recently described Australopithecus deyiremeda has tooth sizes and proportions like graciles but lower jaws that are very thick, like those of robust australopithecines (Haile-Selassie et al., 2015).

So in light of all the confusion and blurring distinctions, maybe it’s time to scrap “gracile” vs. “robust”?

Further reading:  The “robust” australopiths (Constantino, 2013).

ResearchBlogging.org

References
Asfaw B, White T, Lovejoy O, Latimer B, Simpson S, & Suwa G (1999). Australopithecus garhi: a new species of early hominid from Ethiopia. Science (New York, N.Y.), 284 (5414), 629-35 PMID: 10213683

Domínguez-Rodrigo, M., Pickering, T., Baquedano, E., Mabulla, A., Mark, D., Musiba, C., Bunn, H., Uribelarrea, D., Smith, V., Diez-Martin, F., Pérez-González, A., Sánchez, P., Santonja, M., Barboni, D., Gidna, A., Ashley, G., Yravedra, J., Heaton, J., & Arriaza, M. (2013). First Partial Skeleton of a 1.34-Million-Year-Old Paranthropus boisei from Bed II, Olduvai Gorge, Tanzania PLoS ONE, 8 (12) DOI: 10.1371/journal.pone.0080347

Haile-Selassie Y, Gibert L, Melillo SM, Ryan TM, Alene M, Deino A, Levin NE, Scott G, & Saylor BZ (2015). New species from Ethiopia further expands Middle Pliocene hominin diversity. Nature, 521 (7553), 483-8 PMID: 26017448

Walker, A., Leakey, R., Harris, J., & Brown, F. (1986). 2.5-Myr Australopithecus boisei from west of Lake Turkana, Kenya Nature, 322 (6079), 517-522 DOI: 10.1038/322517a0

New beef with boisei – maybe the dingo ate their babies?

ResearchBlogging.orgUnfortunately, the title is not in reference to a study demonstrating that early hominids fell prey to wild dogs. But Elaine Benes would have appreciated it.

As part of my Latitudes Tour, I’m in Nairobi for a couple of days, hoping to spend some quality time with the young Australopithecus boisei kids at the Nairobi National Museum. Recall (that is, if I’ve mentioned it here?) that my dissertation research is on growth of the lower jaw, in Australopithecus robustus as compared to modern humans. The study of growth obviously requires analyzing individuals across different age groups (an “ontogenetic series” is the fancy term). Admittedly, then, the focus on A. robustus is chiefly because this species has the largest ontogenetic sample of any early hominid (tho at nearly 15 subadults, it’s still not as large as one could hope). Also because A. robustus was totally badass.

Australopithecus boisei makes an important comparison for A. robustus, because the two species are allegedly evolutionary ‘sisters’ – the “robust” australopithecines (though I’m personally not convinced that these two are each other’s closest relative). So their growth should be pretty similar. At the same time, though, A. boisei shows much greater adaptations to heavy chewing – they’ve been referred to as “hyper-robust.” So comparing growth in these species should elucidate how their differences arise.
Problem is, there just aren’t enough kids! It’s like that song by Arcade Fire. Wood and Constantino (2007) published a pretty comprehensive review of A. boisei, including a 1.5-page table of the skulls and teeth attributed to the species. So far as I know, only 4 specimens in this table are subadult mandibles, and so far as I can tell, they’re all about the same age (right around the age that the first permanent molar comes in). There are so many jaws of adult A. boisei (although many of these are abraded mandibular bodies lacking teeth) – so how can there be fewer subadults?!?!


A very preliminary observation of infant-child pairs in the two species suggests they both increase in size fairly dramatically between when they only have baby (a.k.a. “deciduous” or “milk”) teeth and when the first permanent molar comes in. But this is just a preliminary observation based on 2 specimens of each species! Take with a grain of salt!
On second thought, maybe I’ll propose the nearly untestable hypothesis that bone-eating hyenas ate the boisei babes, and that’s why we don’t have their jaws. What could have been nicely preserved subadult boisei bones are instead coprolites (fossilized poops). A little spectacular, yes, but it’s also been hypothesized that many of the A. robustus fossils we know and love came to us as carnivores’ scraps.
further reading:
Wood, B., & Constantino, P. (2007). Paranthropus boisei: Fifty years of evidence and analysis American Journal of Physical Anthropology, 134 (S45), 106-132 DOI: 10.1002/ajpa.20732

What the hell was Australopithecus boisei doing?

A little over 2 million years ago there a major divergence of hominids, leading on the one hand to our earliest ancestors in the genus Homo, and on the other hand to a group of ‘robust’ australopithecines, the latter group a failed evolutionary experiment in being human. In our ancestors, parts of the skull associated with chewing began to get smaller and more delicate, while the robust australopithecines increased the sizes of their crushin’-teeth and chewin’-muscle attachments.
A face not even a mother could love, so now they’re extinct (from McCollum 1999 Fig. 1). Note the very tall face, flaring cheeks, and massive lower jaw which would have facilitated wicked-pisser chewing power.
Weirder, there is a South African form (Australopithecus robustus) and an East African form (A. boisei, the figure here looks like it’s based off this species) of robust australopithecine. These two may have inherited their robust adaptations from a common ancestor, or they may be unrelated lineages that evolved these features in parallel. A boisei has been referred to as ‘hyper-robust,’ its face and teeth are generally larger than those of A. robustus.
For a while it’s been supposed that these ‘robust’ chewing adaptations in our weird, extinct evolutionary cousins (every family has those, right?) reflected a diet of hard objects requiring powerful crushing and grinding – things like hard fruits, seeds, Italian bread, etc. But a few years ago Peter Ungar and others (2008) examined the microscopic wear patterns on the surfaces of molar teeth of A. boisei and noted that they lacked the characteristic pits of a hard-object feeder. A. robustus on the other hand does have wear patterns more like an animal that ate hard foods. Why such a difference? Why the hell wasn’t boisei behaving robustly?
Also in 2008 Nikolaas van der Merwe and colleagues analyzed the carbon isotopes preserved in the teeth of A. boisei and some other fossils. Briefly, plants utilize two isotopes of carbon (C12 and C13), but ‘prefer’ the lighter-weight C12. Some groups of plants like grasses have thrived because they’re less picky and can get by just as well with C13. Different kinds of plants, then, incorporate different amounts of these two carbon isotopes into their tissues, then when animals eat it, these isotopes get incorporated into the animal’s developing tissues, including tooth enamel. So by looking at the relative amounts of carbon in teeth, researchers can get a rough idea of whether an animal was eating more of the C13-loving or C13-loathing plants (or the animals eating the plants). van der Merwe and others found A. boisei to have a way higher percentage of the plants that don’t discriminate against C13 as much, possibly things like grass, sedges or terrestrial flowering plants. GRASS?!


Last week, Thure Cerling and colleagues expanded on the earlier study led by van der Merwe, including a larger set of boisei specimens spanning 500 thousand years of the species’ existence. Lo and behold, Cerling and others got similar results: the isotopic signature in A boisei is similar to grass-feeding pigs and horses in its habitat – was the badass “hyper robust” A boisei just a hominid version of a horse? Now, the silica in grass make it extremely wearing on tooth enamel, and while A. boisei had crazy thick molar enamel, I would be a little surprised if the boisei dentition could withstand a lifetime of a grassy diet. Nevertheless, boisei‘s diet clearly differed from robustus, based on both dental wear and carbon isotopes.
This raises interesting questions about the evolution of the robust group. Does their shared ‘robust’ morphology reflect common ancestry, with the subtle differences the result of their divergent diets? Or do the subtle differences indicate that they evolved separately but their diets for whatever reasons resulted in similar mechanical loading on their jaws and faces? It should also be noted that while the dates for South African cave sites are always a bit uncertain, it is possible that A. robustus persisted alongside genus Homo until around 1 million years ago, whereas the fossil record for A. boisei craps out around 1.4 million years ago – was A. boisei too specialized on crappy grass, resulting in its evolutionary demise?
ResearchBlogging.org
A horse-ish, human-ish hominid? Australopithecus boisei, rest in peace. 2.1 – 1.4 mya.
References
Cerling TE, Mbua E, Kirera FM, Manthi FK, Grine FE, Leakey MG, Sponheimer M, & Uno KT (2011). Diet of Paranthropus boisei in the early Pleistocene of East Africa. Proceedings of the National Academy of Sciences of the United States of America PMID: 21536914
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, & 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

New twist from teeth

Peter Ungar, Fred Grine and Mark Teaford recently reported in PLoS ONE on their results of studying the microwear on Australopithecus boisei molars. Their study showed that the microwear differs from that of A. robustus, arguably boisei‘s South African counterpart, and from A. africanus. Here’s the abstract:

The Plio-Pleistocene hominin Paranthropus boisei had enormous, flat, thickly enameled cheek teeth, a robust cranium and mandible, and inferred massive, powerful chewing muscles. This specialized morphology, which earned P. boisei the nickname “Nutcracker Man”, suggests that this hominin could have consumed very mechanically challenging foods. It has been recently argued, however, that specialized hominin morphology may indicate adaptations for the consumption of occasional fallback foods rather than preferred resources. Dental microwear offers a potential means by which to test this hypothesis in that it reflects actual use rather than genetic adaptation. High microwear surface texture complexity and anisotropy in extant primates can be associated with the consumption of exceptionally hard and tough foods respectively. Here we present the first quantitative analysis of dental microwear for P. boisei. Seven specimens examined preserved unobscured antemortem molar microwear. These all show relatively low complexity and anisotropy values. This suggests that none of the individuals consumed especially hard or tough foods in the days before they died. The apparent discrepancy between microwear and functional anatomy is consistent with the idea that P. boisei presents a hominin example of Liem’s Paradox, wherein a highly derived morphology need not reflect a specialized diet.



Note that they refer to boisei and robustus as “Paranthropus,” whereas I (and others) refer to them as Australopithecus. A. boisei and robustus are two “robust” australopithecines, described as such because their skulls and teeth suggest these guys were adapted for prolonged, powerful bouts of mastication (it means chewing, get your mind out of the gutter). Some people argue that these two taxa form a monophyletic group; that is, they share a last common ancestor that is not shared by any other taxon. If this is the case, the generic distinction (Paranthropus) can be made, separating them from the other australopithecines. Though I tend to lump groups, I really think that these taxa do not form a monophyletic group, that they have different ancestors (that their superficially similar masticatory apparati were independently evolved), and that they should stay in the genus Australopithecus. Right now, this issue (wherein I am very interested) has yet to be resolved.


Anywho, what’s important here is that the two robust austrlopithecines differ in their microwear patterns, which suggests that the two subsisted on different diets. Similarly, Wood and Constantino (2007) report that the stable carbon isotope signal from boisei (yet unpublished, but communicated to them personally by Matt Sponheimer) is different from the A. robustus and africanus. Together, these two data indicate that the robust australopitheciens (not to speak about A. aethiopicus…) were quite different in their diets (and possibly lifestyles?). Interestingly, A. robustus‘s molar microwear and stable isotope signals are very similar to that of A. africanus, who was present in the same regions as robustus but a bit earlier in time. This bolsters the scenario in which A. robustus is evolved from A. africanus, or something like it. Could this suggest also that A. boisei is not descendant from A. africanus? Or, is it simply that there were different foods available in the Plio-Pleistocene of South and East Africa?


Another important note that the authors bring up is the fact that of the seven specimens examined, none appeared to have eaten tough or hard foods that might necessitate the use of their (we assume) powerful masticatory muscles. Now why the hell would they have such a derived face, jaws and teeth if they were not eating things that would have required such an apparatus? One proposed scenario about the “hyper-robust” masticatory apparatus of A. boisei is that it is an adaptation for only the toughest of times, when survival might have hinged upon the ability to process and ingest the lowest quality (and hardest to eat) foods. Ungar et al.’s data suggest that this may well be the case, that the powerful masticatory apparatus came in handy only very rarely, and so the dietary signal from microwear reflects what these critters usually ate (and preferred to eat).


If this is really the case, then it might suggest that the robust face of boisei was almost completely genetically acquired, that epigenetic factors did not contribute greatly to produce boisei‘s face. This could be important for teasing out criteria (i.e. skeletal, craniofacial traits) useful in phylogenetic reconstruction. For example, it could be that certain robust features of boisei‘s face indicate a shared genetic ancestry, whereas those of robustus were more epigenetic in nature, acquired over a lifetime of experiencing high chewing forces. Contrariwise, these traits might be the result of these two taxa’s shared ancestry.


Either way, this paper presents interesting new information about the most bizarre hominin evolutionary dead-end, the robust australopithecines.



References


Ungar PS, Grine FE, and Teaford MF. 2008. Dental Microwear and Diet of the Plio-Pleistocene Hominin Paranthropus boisei. PLoS ONE 3(4):e2044.

Wood B, and Constantino P. 2007. Paranthropus boisei: Fifty years of evidence and analysis. American Journal of Physical Anthropology 134(S45):106-132.