Did GDF6 “gene tweak” allow humans to become upright?

The short answer is, “Not really.” But as is often the case, the real story behind so many headlines last week is a bit more complicated.

smh.

smh. Links to the first, second, third, and fourth stories.

What are they talking about, Willis?

These headlines, each saying something slightly different, are referring to a study by Indjeian and colleagues published in Cell.  Researchers identified a stretch of DNA that is highly conserved across mammals, or in other words, it is very similar between very different organisms. In humans, however, this conserved region is actually missing (“hCONDEL.306”):

Fig. 4A from Indjeian et al. 2016. A stretch of DNA, "hCONDEL.306" is completely missing in humans (as is another stretch, hCONDEL.305) but otherwise very similar between chimpanzees, monkeys and mice.

Fig. 4A from Indjeian et al. 2016. A stretch of DNA on Chromosome 8, “hCONDEL.306,” is very similar between chimpanzees, macaque monkeys, and mice, but is completely missing in humans (as is another stretch, hCONDEL.305).

That a stretch of DNA should be highly conserved across diverse animal groups suggests purifying natural selection has prevented any mutations from occurring here – alterations to this stretch of DNA negatively affected fitness. But that humans should be missing such a highly conserved region suggests that this deletion came under positive natural selection at some point in human evolution. This strategy, of seeking stretches of DNA that are similar between many animals but very different in humans, has led to the identification of hundreds of genetic underpinnings of human uniqueness. Some of these, such as the case in question, involve deleted sequences and have been termed “hCONDELs,” for “regions with high sequence conservation that are surprisingly deleted in humans” (McLean et al., 2011: 216). Others involve the accumulation of mutations where other animals show few or none (e.g., HACNS1; Prabhakar et al. 2008). In many (most?) cases these are “non-coding” sequences of DNA.

How can “non-coding” DNA help make humans upright?

As was predicted 30 years ago (King and Wilson, 1975), what makes humans different from other animals isn’t so much in the protein-coding DNA (the classical understanding of the term, “genes”), but rather in the control of these protein-coding genes. “Non-coding” means that a stretch of DNA may get transcribed into RNA but is not then translated into proteins. But even though these sequences themselves don’t become anything tangible, many are nevertheless critical in regulating gene expression – when, where and how much a gene gets used. It’s wild stuff. Indeed, “Many human accelerated regions are developmental [gene] enhancers” (Capra et al., 2013).

In the present case, hCONDEL.306 refers to the human-specific deletion of a developmental enhancer located near the GDF6 gene, which is a bone morphogenetic protein. The major finding of the paper, as stated succinctly in the Highlights title page, is that “Humans have lost a conserved regulatory element [hCONDEL.306] controlling GDF6 expression…. Mouse phenotypes suggest that [this] deletion is related to digit shortening in human feet.”

How do they link this “gene tweak” to digit shortening?

Since humans have lost this gene enhancer that is highly conserved in other mammals, Indjeian and team reasoned that the chimpanzee DNA sequence associated with this deletion, retaining the enhancer sequence, is likely the ancestral condition from which the human version evolved. They inserted the chimpanzee version into mouse embryos and watched what happened as they developed. The enhancer was only active in the mice’s back legs, specifically in the cartilage that would later become the lateral toe bones and cells that would become a muscle of the big toe (abductor hallucis). These are areas where humans and chimpanzees differ: our lateral toes are shorter than chimps’, and we only have one abductor hallucis muscle whereas chimpanzees have an additional, longer abductor hallucis  (Aiello and Dean, 2002). So, we’re on our way to seeing how hCONDEL.306 might relate to our big toe or upright walking, as the headlines say.

But this still doesn’t explain how this deletion affects GDF6 gene expression, and therefore what this does for our feet. Pressing onward, the scientists compared the size of certain bones in mice with a normal Gdf6 gene, and those in which the Gdf6 gene was completely turned off (or “knocked out”).  The Gdf6 knock-out mice had shorter lateral toe bones than regular mice, but they also had shorter big toes as well – the previous experiment staining mouse embryos showed the ancestral enhancer was expressed more in the latter toes, not so much the big toe.

Figures 5-6 from Indjeian et al. (2016) sum up the findings. Figure 5 (left) shows that the ancestral version of the GDF6 enhancer (blue staining) is most strongly expressed in the lower limb, especially the fifth toe bone. Figure 6 (right) shows that a lack of GDF6 expression (black bars) results in shorter skull and toe bones. Combining these findings, humans lack a gene enhancer associated with the development of long lateral toes.

Figures 5-6 from Indjeian et al. (2016) sum up the findings. Figure 5 (left) shows that the ancestral version of the GDF6 enhancer (blue staining) is most strongly expressed in the lower half of the body, especially the fifth toe bone. Figure 6 (right) shows that a lack of Gdf6 expression (black bars) results in shorter skull and toe bones. Combining these findings, humans lack a gene enhancer associated with the development of long lateral toes.

hCONDEL.306 doesn’t completely turn off GDF6, so this second experiment doesn’t really tell us exactly what the hCONDEL does. But the results are highly suggestive. Indjeian and team showed that Gdf6 affects toe length, among other skeletal traits, in mice. The ancestral enhancer that humans are missing seems to affect GDF6 activity in the leg/foot only. This illustrates a mechanism of modularity – as the authors state, “Loss of this enhancer would thus preserve normal GDF6 functions in the skull and forelimbs, while confining any … changes to the posterior digits of the hindlimb.” In other words, developmental enhancers allow different parts of the body to evolve independently despite being made by some of the same genes (such as GDF6).

As with any good study, results are intriguing but they raise more questions for future studies. The researchers conducted two experiments to investigate the function of hCONDEL.306: first putting the chimp version in mouse embryos to see where the ancestral enhancer is expressed, and then turning off Gdf6 completely in mice to see what happens. A more direct way to see what hCONDEL.306 does might be to put a longer stretch of the human sequence surrounding GDF6 containing (or rather missing) the ancestral enhancer into mouse embryos. I’m not a molecular biologist so maybe this isn’t possible. But this is important because the ancestral (chimpanzee) enhancer appeared to be most strongly expressed in the little toe, but of course this isn’t our only toe that is short compared to chimps. Similarly, how hCONDEL.306 relates to the abductor hallucis muscle remains in question – does it reduce the size of the intrinsic muscle present in both humans and chimps, or does it prevent development of the longer muscle that chimps have but we lack? We can expect to find hCONDEL.306 in the genomes of Neandertals (and Denisovans?), since they also have short toes, but what would it mean if they retained the ancestral enhancer?

So how does this gene tweak help with upright walking?

This is a really cool paper with important implications for human evolution, but something seems to have been lost in translation between the paper and the headlines (the news pieces themselves are good, though). The upshot of the study is that humans lack a stretch of non-coding DNA, which in chimpanzees (or chimp-ified mice) promotes embryonic development of the lateral toes and a big toe muscle. This may be a genetic basis for at least some aspects of our unique feet that have evolved under natural selection for walking on two legs.

But the headlines misrepresent this result, with words like “led to,” “allowed,” and “caused,” especially when these are followed by “big toe” or “upright walking.” hCONDEL.306 doesn’t really have anything to the big toe bone itself, although it might relate to a muscle affecting our big toe. The only sense in which the “Gene tweak led to humans’ big toe” (first title above) is that hCONDEL.306 might be responsible for our short lateral toes, which make our first toe look big by comparison. The other headlines are misleading since we know from fossil evidence that hominins walked upright long before we have evidence for short toes:

These little piggies get none. Fourth toe bones of living apes and humans (left) and possible hominins from 3-5 million years ago (right).

These little piggies get none. Fourth toe bones of living apes and humans (left) and (probable) hominins from 3-5 million years ago (right). I did my best to get all images to scale.

“Epigenetic,” from the fourth article headline, is simply wrong. Modern day epigenetics is a field concerned with the chemical alterations to the structure of DNA. Even the broad concept of epigenetic as originally devised by Conrad Waddington was about how environments (cellular or outside the body) influence development.

ResearchBlogging.orgIt’s hard to fit all the important and interesting information from scientific papers into news headlines. Still, it would be good if headlines more accurately portrayed scientific findings, especially avoiding such definitive verbs as “caused.” Especially in the realm of biology, people should know that there’s a lot that we still don’t know, that there’s lots more important work left to be done.

References

Aiello and Dean, 2002. Human Evolutionary Anatomy. Academic Press.

Capra et al., 2013. Many human accelerated regions are developmental enhancers. Philosophical Transactions of the Royal Society B 368: 20130025.

Indjeian et al. 2016. Evolving new skeletal traits by cis-regulatory changes in bone morphogenetic proteins. Cell http://dx.doi.org/10.1016/j.cell.2015.12.007

King and Wilson, 1975. Evolution at two levels in humans and chimpanzees. Science 188: 107-116 DOI: 10.1126/science.1090005

McLean et al., 2011. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471: 216-219.

Prabhakar et al., 2008. Human-specific gain of function in a developmental enhancer. Science 321: 1346-1350.

#FossilFriday: 2015 Retrospecticus

summerof4ft26_thumb

Holy crap 2015 was a big year for fossils. And how fortuitous that 2016 begins on a Fossil Friday – let’s recap some of last year’s major discoveries.

Homo naledi

Homo naledi mandibles in order from least to most worn teeth.

Some Homo naledi mandibles in order from least to most worn teeth.

The Homo naledi sample is a paleoanthropologist’s dream – a new member of the genus Homo with a unique combination of traits, countless remains belonging to at least a dozen individuals from infant to old adult, representation of pretty much the entire skeleton, and a remarkable geological context indicative of intentional disposal of the dead (but certainly not homicide, grumble grumble grumble…).  The end of 2015 saw the announcement and uproar (often quite sexist) over this amazing sample. You can expect to see more, positive things about this amazing animal in 2016.

We’ll be presenting a bunch about Homo naledi at this year’s AAPA meeting in Hotlanta. I for one will be discussing dental development at Dinaledi- here’s a teaser:

377

As long as we’re talking about the AAPA meetings, my colleague David Pappano and I are organizing a workshop, “Using the R Programming Language for Biological Anthropology.” Details to come!

Lemur graveyard

Homo naledi wasn’t the only miraculously copious primate sample announced in 2015. Early last year scientists also reported the discovery of an “Enormous underwater fossil graveyard,” containing fairly complete remains of probably hundreds of extinct lemurs and other animals. As with Homo naledi, such a large sample will reveal lots of critical information about the biology of these extinct species.

Australopithecus deyiremeda

Extended Figure 1h from the paper, with a Demirjian developmental stages, modifed from Table 2 from Kuykendall et al., 1996. Compare the M2 roots with completed roots of the M1 (to the left).

Extended Figure 1h from Haile-Selassie et al. (2015), compared with Demirjian developmental stages 6-8 . While the M1 roots look like stage 8 (complete), M2 looks like stage 7 (incomplete).

We also got a new species of australopithecus last year. Australopithecus deyiremeda had fat mandibles, a relatively short face (possibly…), and smaller teeth than in contemporaneous A. afarensis. One tantalizing thing about this discovery is that we may finally be able to put a face to the mysterious foot from Burtele, since these fossils come from nearby sites of about the same geological age. Also intriguing is the possible evidence, based on published CT images (above), that A. deyiremeda had relatively advanced canine and delayed molar development, a pattern generally attributed to Homo and not other australopithecines (if this turns out to be the case, you heard it here first!).

Lomekwian stone tool industry

3D scan and geographical location of Lomekwian tools. From africanfossils.org

3D scan and geographical location of Lomekwian tools. From africanfossils.org.

Roughly contemporaneous with A. deyiremeda, Harmand et al. (2015) report the earliest known stone tools from the 3.3 million year old site of Lomekwi 3 in Kenya. These tools are a bit cruder and much older than the erstwhile oldest tools, the Oldowan from 2.6 million years ago. These Lomekwian tools, and possible evidence for animal butchery at the 3.4 million year old Dikika site in Ethiopia (McPherron et al. 2010;  Thompson et al. 2015), point to an earlier origin of lithic technology. Fossils attributed to Kenyanthropus platyops are also found at other sites at Lomekwi. With hints at hominin diversity but no direct associations between fossils and tools at this time, a lingering question is who exactly was making and using the first stone tools.

Earliest Homo

The reconstructed Ledi Geraru mandible (top left), compared with Homo naledi (top right), Australopithecus deyiremeda (bottom left), and the Uraha early Homo mandible from Malawi (bottom right).

The reconstructed Ledi Geraru mandible (top left), compared with Homo naledi (top right), A. deyiremeda (bottom left), and the Uraha early Homo mandible from Malawi (bottom right). Jaws are scaled to roughly the same length from the front to back teeth; the Uraha mandible does not have an erupted third molar whereas the others do and are fully adult.

Just as Sonia Harmand and colleagues pushed back the origins of technology, Brian Villmoare et al. pushed back the origins of the genus Homo, with a 2.7 million year old mandible from Ledi Geraru in Ethiopia. This fossil is only a few hundred thousand years younger than Australopithecus afarensis fossils from the nearby site of Hadar. But the overall anatomy of the Ledi Geraru jaw is quite distinct from A. afarensis, and is much more similar to later Homo fossils (see image above).  Hopefully 2016 will reveal other parts of the skeleton of whatever species this jaw belongs to, which will be critical in helping explain how and why our ancestors diverged from the australopithecines. (note that we don’t yet have a date for Homo naledi – maybe these will turn out to be older?)

Early and later Homo

Modified figures X from Maddux et al. (2015) and 13 from Ward et al. (2015).

Left: modified figures 2-3 from Maddux et al. (2015). Right: modified figures 7 & 13 from Ward et al. (2015). Note that in the right plot, ER 5881 femur head diameter is smaller than all other Homo except BSN 49/P27.

The earlier hominin fossil record wasn’t the only part to be shaken up. A small molar (KNM-ER 51261) and a set of associated hip bones (KNM-ER 5881) extended the lower range of size variation in Middle and Early (respectively) Pleistocene Homo. It remains to be seen whether this is due to intraspecific variation, for example sex differences, or taxonomic diversity; my money would be on the former.

Left: Penghu hemi-mandible (Chang et al. 2015: Fig. 3), viewed from the outside (top) and inside (bottom). Right: Manot 1 partial cranium (Hershkovitz et al. 2015: Fig. 2), viewed from the left (top) and back (bottom).

Left: Penghu 1 hemi-mandible (Chang et al. 2015: Fig. 3), viewed from the outside (top) and inside (bottom). Right: Manot 1 partial cranium (Hershkovitz et al. 2015: Fig. 2), viewed from the left (top) and back (bottom).

At the later end of the fossil human spectrum, researchers also announced an archaic looking mandible dredged up from the Taiwan Straits, and a more modern-looking brain case from Israel. The Penghu 1 mandible is likely under 200,000 years old, and suggests a late survival of archaic-looking humans in East Asia. Maybe this is a fossil Denisovan, who knows? What other human fossils are waiting to be discovered from murky depths?

The Manot 1 calvaria looks very similar to Upper Paleolithic European remains, but is about 20,000 years older. At the ESHE meetings, Israel Hershkovitz actually said the brain case compares well with the Shanidar Neandertals. So wait, is it modern or archaic? As is usually the case, with more fossils come more questions.

Crazy dinosaurs

YiQiSkeksis

Yi qi was bringing Skeksi back, and its upper limb had a wing-like shape not seen in any other dinosaur, bird or pterosaur. There were a number of other interesting non-human fossil announcements in 2015 (see here and here), proving yet again that evolution is far more creative than your favorite monster movie makers.

ResearchBlogging.orgWhat a year – new species, new tool industries, new ranges of variation! 2015 was a great year to be a paleoanthropologist, and I’ll bet 2016 has just as much excitement in store.

References (in order of appearance)

Haile-Selassie, Y., Gibert, L., Melillo, S., Ryan, T., Alene, M., Deino, A., Levin, N., Scott, G., & Saylor, B. (2015). New species from Ethiopia further expands Middle Pliocene hominin diversity Nature, 521 (7553), 483-488 DOI: 10.1038/nature14448

Harmand, S., Lewis, J., Feibel, C., Lepre, C., Prat, S., Lenoble, A., Boës, X., Quinn, R., Brenet, M., Arroyo, A., Taylor, N., Clément, S., Daver, G., Brugal, J., Leakey, L., Mortlock, R., Wright, J., Lokorodi, S., Kirwa, C., Kent, D., & Roche, H. (2015). 3.3-million-year-old stone tools from Lomekwi 3, West Turkana, Kenya. Nature, 521 (7552), 310-315. DOI: 10.1038/nature14464

McPherron, S., Alemseged, Z., Marean, C., Wynn, J., Reed, D., Geraads, D., Bobe, R., & Béarat, H. (2010). Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature, 466 (7308), 857-860. DOI: 10.1038/nature09248

Thompson, J., McPherron, S., Bobe, R., Reed, D., Barr, W., Wynn, J., Marean, C., Geraads, D., & Alemseged, Z. (2015). Taphonomy of fossils from the hominin-bearing deposits at Dikika, Ethiopia Journal of Human Evolution, 86, 112-135 DOI: 10.1016/j.jhevol.2015.06.013

Villmoare, B., Kimbel, W., Seyoum, C., Campisano, C., DiMaggio, E., Rowan, J., Braun, D., Arrowsmith, J., & Reed, K. (2015). Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia Science, 347 (6228), 1352-1355 DOI: 10.1126/science.aaa1343

Maddux, S., Ward, C., Brown, F., Plavcan, J., & Manthi, F. (2015). A 750,000 year old hominin molar from the site of Nadung’a, West Turkana, Kenya Journal of Human Evolution, 80, 179-183 DOI: 10.1016/j.jhevol.2014.11.004

Ward, C., Feibel, C., Hammond, A., Leakey, L., Moffett, E., Plavcan, J., Skinner, M., Spoor, F., & Leakey, M. (2015). Associated ilium and femur from Koobi Fora, Kenya, and postcranial diversity in early Homo Journal of Human Evolution, 81, 48-67 DOI: 10.1016/j.jhevol.2015.01.005

Chang, C., Kaifu, Y., Takai, M., Kono, R., Grün, R., Matsu’ura, S., Kinsley, L., & Lin, L. (2015). The first archaic Homo from Taiwan Nature Communications, 6 DOI: 10.1038/ncomms7037

Hershkovitz, I., Marder, O., Ayalon, A., Bar-Matthews, M., Yasur, G., Boaretto, E., Caracuta, V., Alex, B., Frumkin, A., Goder-Goldberger, M., Gunz, P., Holloway, R., Latimer, B., Lavi, R., Matthews, A., Slon, V., Mayer, D., Berna, F., Bar-Oz, G., Yeshurun, R., May, H., Hans, M., Weber, G., & Barzilai, O. (2015). Levantine cranium from Manot Cave (Israel) foreshadows the first European modern humans Nature, 520 (7546), 216-219 DOI: 10.1038/nature14134

Blood spattered Easter eggs from Raymond Dart

Some of the more colorful ideas and text in the anthropological literature are courtesy of Raymond Dart.

Dart, hammering away to remove a fossil from some breccia. I hope. Image credit.

Dart, hammering away at some breccia to remove a fossil. I hope. Image credit.

In 1925, Dart identified the Taung fossil as a close relative of humans, and coined the scientific name, Australopithecus africanus. This was a pretty good idea, as Taung was the first in what is now a large collection of fossils attributed to this species.

Taung was such an important discovery, you can now walk across it as you enter the fossil collections at Wits University.

Taung was such an important discovery, you can now walk across it not once, not twice, but thrice! as you enter the fossil collections at the Evolutionary Studies Institute at Wits University.

Some of Dart’s ideas that made it into print, though, were a bit more fanciful. Aside from his description of Taung, he is probably most famous for hypothesizing the “osteodontokeratic” culture, the idea that the myriad broken animal bones in Makapansgat cave were in fact tools used by australopiths for hunting and murder. MURDER! It was a neat idea at the time, but his vision of bloodthirsty, bone-dagger-wielding australopithecines is not accepted today (nor back when he was writing).

Dart was trained as an anatomist, and much of his work was devoted to writing up australopithecine fossils discovered at site of Makapansgat in South Africa. These are probably the best descriptive papers I’ve found in all the literature, as Dart’s whimsical visions of violence and bloodshed occasionally made their way into otherwise dry scientific prose.

In 1948 he very casually put it out there, that the front teeth of the MLD 2 mandible were lost in “fatal combat . . . presumably by a bludgeon” (emphasis added). Of course, the teeth were probably lost long after the poor kid died, rather than being knocked out “at the hands of a kinsman more expert than himself in the accurate application of directed implements” (Dart, 1948: 393-394). But Dart’s version is certainly more interesting than the more likely taphonomic explanation.

MLD 2

The MLD 2 mandible, poor kid, as illustrated in Dart (1948). Note that the incisor tooth sockets are empty, likely the result of taphonomy rather than bloodsport.

Dart (1958) later described the MLD 7 ilium, which he’d presumed to be a female, from the same site as MLD 2. Dart recounted the violent demise of MLD 2, raising the possibility of a similar death for the MLD 7 individual: “The adolescent boy [MLD 2] … was killed by a bone-smashing blow on the chin from a club or fist. Did brother and sister share here in death the same cannibalistic fate?” (emphasis added) Bloodshed, cannibalism, Australopithecus according to Dart had it all. Although these are unlikely characterizations of australopithecines, there is evidence of cannibalism in later fossil humans.

These gruesome Easter Eggs come to mind as I’m reading his 1956 paper about brain evolution. Here, Dart (1956: 28) says that hominins began walking on two legs after a dietary shift: “The forest-loving vegetarian anthropoids clung to their four-handed climbing and fruit while the terrestrial predaceous australopithecines, depending on their speed of foot and deftness of hand, lusted after flesh!” (emphasis added) Today, this idea would simply be written as, monkeys and apes live in trees and eat fruits while australopithecines lived on the ground and ate meat. But Raymond Dart wouldn’t stand for this. Oh no.

My grad school advisor, Milford Wolpoff, used to lament that students today don’t want to read anything older than the past 5-10 years. But Dart is a shining example of some of the rewarding Easter Eggs that await those who dig deeper into the literature. [I’m reminded also of Don Cousins describing “the colossal poundage of the lowland gorilla ‘Phil,’ who lived in the St. Louis Zoo from 1941-1958″ (1972: 269, emphasis added].

ResearchBlogging.org
Some good, older stuff

Cousins D (1972). Body measurements and weights of wild and captive gorillas, Gorilla gorillaZoologische Garten NF Leipzig 41, 261-277.

Dart, RA (1925). Australopithecus africanus: The Man-Ape of South Africa Nature, 115 (2884), 195-199 DOI: 10.1038/115195a0

Dart, RA (1948). The adolescent mandible of Australopithecus prometheus American Journal of Physical Anthropology, 6 (4), 391-412 DOI: 10.1002/ajpa.1330060410

Dart RA (1956). The relationships of brain size and brain pattern to human status. The South African Journal of Medical Sciences, 21 (1-2), 23-45 PMID: 13380551

Dart, RA (1958). A further adolescent australopithecine ilium from Makapansgat American Journal of Physical Anthropology, 16 (4), 473-479 DOI: 10.1002/ajpa.1330160407

Osteology Everywhere: Vertebeer Fest

This past weekend was witness to the Summer Beer Festival, the annual showcase of Michigan’s brewing splendor. Dozens of breweries brought out batches of beer, from classics we know and love, to inspired innovations meriting a MacArthur Fellowship. There was an embeerrassment of boozes. Dark Horse Brewing Company, from Marshall, MI, put on quite the show:

Dark  Horse Brewing Co. pumping out the brews and blasting t-shirts into the crowd.

Dark Horse Brewing Co. pumping out the brews and blasting t-shirts into the crowd.

Besides towering over the bacchanal hordes, the Dark Horse beer fort also offered IPAs infused with pretty much anything that might pair well with hops. They even steeped habañero peppers in one, and it was maximally boss.

Beer still my heart.

Beer still my heart.

Having sampled only a small part of rich the smorgasbord on tap, a rest by the river was in order. The Festival was on the banks of the mighty Huron River, an excellent place to sit and sip Arcadia‘s scotch ale, taking in the evening under cloud-peppered, cerulean skies. Such a calm and relaxing setting would surely offer respite for a brain besieged by bones. Right?

Every year for the Festival they replace the river water with beer.

Every year for the Festival they replace the river water with beer.

Wrong! Peering through beer goggles over the shimmer of the river, seeking signs of Bigfoots lurking on the opposite shore, I locked eyes with a large, wooden vertebral body.

No ordinary tree stump

An eyeless frown marks the ventral surface of this centrum.

The human spine is composed of anywhere from 31-34 vertebrae (not counting the coccyx or tail bone). The body or “centrum” is the large, blocky portion of the bone, which is separated from other such bodies by intervertebral discs; it is literally a pile of bodies, stacked one on top of the other. And the intervertebral discs are remnants of the notochord, the embryonic structure that unites you and me and all other humans with all other animals known as chordates. Anyway, kiss my grits if this old tree stump across the mighty Huron River here doesn’t look like a lower thoracic or upper lumbar vertebral body, the metaphoric shark fin of a giant trunkless human waiting to pounce from the placid waters.

a) Our mystery vertebra. b) a lumbar vertebra from White et al. (2012). c) views of the right and front side of the Australopithecus africanus fossil StW H41, from Sanders (1998, Fig. 1).

a) Our mystery river vertebra. b) a lumbar vertebra from White et al. (2012). c) views of the right and front side of the Australopithecus africanus fossil StW H8/H41, modified from Fig. 1 of Sanders (1998).

Thinking on it, our mystery river vertebra doesn’t just look like any old human centrum, it is a ringer for the second lumbar vertebra of StW H8/H41, a series of the 11th thoracic to 4th lumbar vertebrae of Australopithecus africanus from Sterkfontein (see the red arrow in c, above). Sanders (1998) notes that this short segment of an early hominin spine shows clear adaptation to walking upright like we humans do today, although the size of the vertebral bodies is both absolutely and relatively small compared to ours, just as is seen in other Australopithecus fossils.

And what better way to celebrate this monumental discovery than returning to the Beer Festival – hooray beer!

Quick thought on the Australopithecus deyiremeda maxilla

It will be lots of work to prep my Human Evolution course for the Fall. This past year has seen many major fossil discoveries, and adding to the list is the newly described species Australopithecus deyiremeda (Haile-Selassie et al., 2015). The fossils come from newly announced sites in Ethiopia (here it is on a map!), dating to around 3.4 million years ago. These new fossils are contemporaneous with Australopithecus afarensis, fossils attributed to Kenyanthropus platyops, and whatever the hell the Burtele foot belongs to.

The main specimens are a fairly complete half of a maxilla (upper jaw) and two decent mandibles (lower jaw bones). These fossils do not belong to the same individual (despite all the media pictures of the upper and lower jaws together). One of the most distinctive features of these fossils is how thick, both in absolute and relative terms, the mandibles are, especially given how short they are. What sticks out to me though, is that the upper jaw looks like it might have still had some growing to do. Why on earth would I think so? (The following is based off pictures from the publications, so I could be wrong!)

Extended Figure 1a from the paper. The type specimnen BRT-VP-3/1 maxilla. Front is to the left.

Extended Figure 1a from the paper, the type specimnen BRT-VP-3/1 maxilla viewed from the left side. I’ve added the M2 label for your reading pleasure.

The holotype maxilla (BRT-VP-3/1) is described as coming from a “young adult” in the Supplementary Information. However, it looks like the second molar tooth (M2) is not quite fully erupted and in occlusion, although this could be due to the natural arc of the tooth row. There is no visible wear on the tooth in the pictures, and indeed the Supplementary Information says the tooth is unworn. This means that the tooth is only recently emerged, and may not have passed the gum line, and therefore hasn’t seen much/any use yet. Authors note in the Supplementary Information that there is no M3 (a.k.a. “wisdom tooth”) wear facet on the back of M2 , meaning the last tooth hadn’t yet emerged yet either. So, this all points to a non-adult age by tooth eruption standards.

Extended Figure 1d from the paper. Same fossil, but from the bottom, like a dentist peering into its mouth. Back is to the bottom.

Extended Figure 1d from the paper. Same fossil, but from the bottom; pretend you’re a dentist peering into its mouth. Back is to the bottom.

In addition, the M2 roots don’t look fully formed. This is especially apparent in Extended Figure 1h, a CT section through the teeth:

Extended Figure 1h from the paper, with a Demirjian developmental stages, modifed from Table 2 from Kuykendall et al., 1996. Compare the M2 roots with  completed roots of the M1 (to the left).

Left side: Extended Figure 1h from the paper. From left to right, the teeth are P3, P4, M1, and M2. For comparison, to the right are Demirjian tooth development stages, modified from Table 2 of Kuykendall, 1996. Also compare the M2 roots with completed roots of the M1.

 

In many human populations, this stage of M2 development is reached (on average) between 11-13 years (Liversidge et al., 2006). In the wild Taï Forest chimpanzee sample, two individuals with M2 root completely formed (Stage H) are 10 and 11 years old (Smith et al., 2010). These apes would not be fully mature and their facial dimensions would likely have increased had they reached adulthood (Zihlman et al., 2007).

So what this suggests to me is that this maxilla may not accurately represent adult anatomy in this newly described species. In humans, the face continues to grow downwards from adolescence into adulthood, and in apes the face continues growing both forward and downward. In the differential diagnosis of A. deyiremeda, Haile-Selassie and team state, in layman’s terms, that the cheeks are positioned more toward the front than in A. afarensis, and that the front of the face doesn’t stick out as much as in A. garhi. If this specimen was not fully grown, it is likely that the true adult anatomy would have had a face that sticks out more and has less forward-positioned cheeks than in this specimen.

But, this is all speculative, and I’d like to reiterate that these observations of dental development are based only on the published pictures. Just a thought!

Gona … Gona … not Gona work here anymore more

The Gona pelvic remains (A-D), and the reconstructed complete pelvis (E-J), Fig. 2 in Simpson et al., 2008.

A few years ago, Scott Simpson and colleagues published some of the most complete fossil human hips (right). The fossils are from the Busidima geological formation in the Gona region of Ethiopia, dated to between 0.9-1.4 million years ago. (Back when I wasn’t the only author of this blog, my friend and colleague Caroline VanSickle wrote about it here)

Researchers attributed the pelvis to Homo erectus on the basis of its late geological age and a number of derived (Homo-like) features. In addition, the pelvis’s very small size indicated it probably belonged to a female. One implication of this fossil was that male and female H. erectus differed drastically in body size.

Christopher Ruff (2010) took issue with how small this specimen was, noting that its overall size is more similar to the small-bodied Australopithecus species. Using the size of the hip joint as a proxy for body mass, Ruff argued Gona’s small size would imply a profound amount of sexual dimorphism in H. erectus: much higher than if Gona is excluded from this species, and higher than in modern humans or other fossil humans. Ruff thus proposed an alternative hypothesis to marked sexual dimorphism, that the Gona pelvis may have belonged to an australopithecine.

Fig. 3 From Ruff's (2010) reply. Australopiths (and Orrorin) are squares and Homo are circles. Busidima's estimated femur head diameter is represented by the star and bar.

Fig. 3 From Ruff’s (2010) reply. Australopiths (and Orrorin) are squares and Homo are circles. Gona’s estimated femur head diameter is represented by the star and bar.

Now, Simpson & team replied to Ruff’s comments, providing a laundry list of reasons why this pelvis is H. erectus and not Australopithecus. They cite many anatomical features of the pelvis shared with Gona and Homo fossils, but not australopithecines. They also note that there are many other bones reflective of body size, that seem to suggest a substantial amount of size variation in Homo fossils, even those from a single site such as Dmanisi (Lordkipanadze et al., 2007).

Interestingly, neither of these parties compared the implied size variation with that of living apes. So I’ll do it! Now, I do not have any acetabulum data, but a friend lent me some femur head measurements for living great apes a few years ago. Gona is a pelvis and not a femur, but there are more fossil femora than hips. Because there’s a very high correlation between femur head and acetabulum size, Ruff estimated Gona’s femur head diameter to be 32.6 mm (95% confidence interval: 30.1-35.2; Simpson et al. initially estimated 35.1 mm based on a different dataset and method). To quantify size variation, we can compare ratios of larger femur heads divided by smaller ones. Now, this ratio quantifies inter-individual variation, but it will underestimate sexual dimorphism since I’m likely sampling some same-sex pairs that aren’t so different in size. But this is just a quick and dirty look. So, here’s a box plot of these ratios for Homo fossils, larger specimens divided by Gona’s estimated femur head size in different time periods:

Ratio of a fossil Homo femur head diameter (HD) divided by Busidima's HD. E Homo = early Pleistocene, Contemporaneous = WT 15000 and OH 28, MP = Middle Pleistocene Homo. White boxes are based on Ruff's Busidima HD estimate, green boxes are based on Simpson et al.'s estimate.

Ratios of fossil Homo femur head diameter (HD) divided by Busidima’s (Gona’s) HD. E Homo = early Pleistocene, Contemporaneous = WT 15000 and OH 28, MP = Middle Pleistocene Homo. White boxes are based on Ruff’s Gona HD estimate, green boxes are based on Simpson et al.’s larger estimate. Boxes include 50% quartiles and the thick lines within are sample medians.

Clearly, Gona is much smaller than most other fossil Homo hips, since ratios are never smaller than 1.14. Average body size increases over time in the Homo lineage, reflected in increasing ratios from left to right on the plot. Early Pleistocene Homo fossils are fairly small, including Dmanisi, hence the lower ratios than later time periods. Middle Pleistocene Homo (MP), represented by the most fossils, shows a large range of variation, but even the smallest is still 1.17 times larger than the largest estimate of Gona’s femur head size. To put this into context, here are those green ratios (assuming a larger size for Gona) compared with large/small ratios from resampled pairs of living apes and humans:

*

The fossil ratios of larger/smaller HD from above, compared with resampled ratios from unsexed living apes and humans. Boxes include the 50% quartiles, and the thick lines within are sample medians. **(05/03/14: This plot has been modified from the original version post, which only included the fossil ratios based on the smaller Gona estimate)

What we see for the extant apes and humans makes sense: humans and chimpanzees show smaller differences on average, whereas average differences between gorillas and orangutans are larger. This accords with patterns of sexual dimorphism in these species. **What this larger box plot shows is that if we accept Ruff’s smaller average estimate of Gona’s femur head size (white boxes), it is relatively rare to sample two living specimens so different in size as seen between Gona and other fossils. If we use Simpson et al.’s larger Gona size estimate, variation is still elevated above most living ape ratios. Only when Gona is compared with the generally-smaller, earlier Pleistocene fossils, does the estimated range of variation show decent overlap with living species. Even then, the overlap is still above the median values.

These results based on living species agree with Ruff’s concern, that including Gona in Homo erectus results in an unusually large range of variation in this species. Such a large size range isn’t necessarily impossible, but it would be surprising to see more variation than is common in gorillas and orangutans, where sexual size dimorphism is tremendous. Ruff suggested that the australopith-sized Gona pelvis may in fact be an australopith. This was initially deemed unlikely, in part because the fossil is well-dated to relatively late, 0.9-1.4 million years ago. However, Dominguez-Rodgrigo and colleauges (2013) recently reported a 1.34 mya Australopithecus boisei skeleton from Olduvai Gorge, so it is possible that australopiths persisted longer than we’ve got fossil evidence for, and Gona is one of the latest holdouts.

So many possible explanations. More clarity may come with further study of the fossils at hand, but chances are we won’t be able to eliminate any of these possibilities until we get more fossils. (also, the post title wasn’t a jab at the fossils or researchers, but rather a reference to the movie Office Space)

References

Dominguez-Rodrigo et al. 2013. First partial skeleton of a 1.33-million-year-old Paranthropus boisei from Bed II, Olduvai Gorge, Tanzania. PLoS One 8: e80347.

Ruff C. 2010. Body size and body shape in early hominins – implications of the Gona pelvis. Journal of Human Evolution 58: 166-178.

Simpson S et al. 2008. A female Homo erectus pelvis from Gona, Ethiopia. Science 322: 1089-1092.

Simpson S et al. In press. The female Homo pelvis from Gona: Response to Ruff (2010). Journal of Human Evolution. http://dx.doi.org/10.1016/j.jhevol.2013.12.004

The small, big new Dmanisi skull

The 5th skull early Homo skull from the site of Dmanisi was announced last week. The skull was discovered nearly 10 years ago, but is finally (and very comprehensively) published in Science (Lordkipanidze et al. 2013). The ‘new’ D4500 cranium goes with the massive D2600 mandible, making this the earliest and most complete skull of Homo that I know of. It’s really a remarkable specimen, for a number of reasons beyond its age and completeness. I’ve been busy traveling, teaching and writing lately, so I haven’t yet gotten to pore over the details as much as I’d like. So I hope to sporadically post thoughts on this badass new skull as they come to me. In the mean time, several of what I’d consider the top biology/anthropology blogs*** have discussed the skull, so do check those out if you haven’t already.

The first thing I noted about D4500 is its small brain size, estimated at a mere 546 cubic centimeters. For perspective, D4500 is the green point in the following plot showing brain size in early human evolution:

Endocranial volume for various fossil hominin fossils. 1: Australopithecus afarensis, africanus & boisei; 2: Dmanisi specimens; 3: "habilines" 4: early African Homo erectus; 5: Indonesian and Chinese Homo erectus

Endocranial volume for various fossil hominin fossils. 1: Australopithecus afarensis, africanus & boisei; 2: Dmanisi specimens; 3: “habilines” 4: early African Homo erectus; 5: Indonesian and Chinese Homo erectus. D4500 is green with envy.

I got to see (but not study) the cranium a few years ago when I was helping with the Dmanisi Paleoanthropology field school, and I remember noting just how “robust” the specimen was – big mastoid processes, prominent and thick brow ridge, huge attachments for the neck muscles. In humans, and presumably our fossil forebears, these features are more developed in males than females, and so presumably D4500 was a male (consistent with the huge, associated D2600 mandible). In many primates, and 4 to ~1 mya hominins so far as we can tell, males are larger than females. So it is surprising that a robust probable male cranium is in fact not only the smallest in the Dmanisi sample, but also at the low end of early African Homo (i.e. habilis or rudolfensis), comparable to the largest australopiths. Of course, the only other faces known from Dmanisi are either not fully grown (D2700 and D2282) or old and decrepit (D3444), so perhaps the larger-brained specimens would have been at least as robust as D4500. An untestable hypothesis!

The new skull really highlights the overlap, or continuous variation between later australopiths and early Homo known also from eastern Africa. In association with the postcranial remains known from Dmanisi, the authors the paper posit that early Homo may have been distinguished from Australopithecus not so much in brain size as in body size. We could probably add body shape (limb proportions) and tool use to that list of distinguishing features, and to be sure there are Oldowan tools and small but human-like body size and shape indicated by postcrania at Dmanisi. But then, evidence for body proportions and for/against tool use in Australopithecus, especially later in the record, is somewhat equivocal…

More thoughts to follow.

*** https://blogs.wellesley.edu/vanarsdale/2013/10/17/uncategorized/the-new-wonderful-dmanisi-skull/; http://johnhawks.net/weblog/fossils/lower/dmanisi/d4500-lordkipanidze-2013.html; http://ecodevoevo.blogspot.com/2013/10/how-many-human-species-are-there-is-it.html

Reference: David Lordkipanidze, Marcia S. Ponce de León, Ann Margvelashvili, Yoel Rak, G. Philip Rightmire, Abesalom Vekua, and Christoph P. E. Zollikofer. 2013. A Complete Skull from Dmanisi, Georgia, and the Evolutionary Biology of Early Homo. Science: 342 (6156), 326-331.