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paleoanthropology, genetics and evolution

Photo Credit: 3D printing a Homo naledi cranium. John Hawks CC-BY-NC-ND

The Pacific Standard is running a nice interview with anthropologist Barbara King, by Francie Diep: “How Do Gorillas Grieve?”. It touches on the recent killing of the gorilla, Harambe, at the Cincinnati Zoo, but broadens to consider the emotional lives of gorillas.

Q: What you’re saying reminds me that humans also evolved things like maternal love and aggressive responses, but that doesn’t mean people aren’t thinking, obviously.
A: That’s exactly right. I do not think it’s anthropomorphic to talk about grief in gorillas. Anthropomorphism is a projection of human qualities onto apes. Why would we say that grief is a human thing? I don’t think it is. I think it’s an animal thing, at least for some animals.

American Scientist kindly invited me to write up a synopsis of our session on the biology of Homo naledi at the AAPA meetings in April. The article is now online: “The Latest on Homo naledi. The article is in the printed July-August issue as well.

The H. naledi analysis was unique in recent paleoanthropology for proceeding on the basis of anatomy alone, without knowing the age of the fossil deposit. This approach was taken partly out of necessity, because of the lack of many of the usual hints regarding geological age. But also, we recognized that the placement of a species into the family tree of organisms, or its phylogenetic position, is one that depends on the pattern of branching in the tree and not the age of the branches. H. naledi’s anatomical mosaic makes the age determination particularly difficult—did it acquire derived traits early or preserve primitive traits late?

I wrote up a short summary of all the new research that was presented at the symposium, and it was great to include so many of the team in the article.

Deliberate deposition and Homo naledi

Earlier this spring, the Journal of Human Evolution published a commentary questioning our team’s interpretation of taphonomic evidence from the Dinaledi Chamber. In the commentary, Aurore Val suggested that the evidence does not rule out some involvement of carnivores as accumulators of the Dinaledi hominin assemblage, and that parts of hominin skeletons may have been transported from a more accessible location by gravity or water.

Our reply was just entered into the “corrected proofs” online access to the journal today. In the reply, we provide a brief summary of the evidence, emphasizing the data that exclude any direct access to the chamber from the outside environment, exclude post-depositional transport of the hominin remains, and exclude carnivore involvement. As we emphasize in our reply, we do not claim any proof of the hypothesis of deliberate deposition of the hominin remains, but the evidence so far excludes other hypotheses that work for other cave assemblages in South Africa.

In conversations with colleagues during the past several months, I’ve been struck by how interested people are in the layout of the Rising Star cave system and the potential for alternative scenarios for the deposition of the fossil remains. People have really been amazingly creative in thinking about how to get 15 hominin bodies into a remote chamber of a cave.

Obviously our team began with many of the same questions, and we all share the perspective that we just want to find the best answers without any preconception as to what they will be. As more and more specialists became involved, each brought their own expertise to bear on the taphonomy of the remains and the geochemistry and geology of the cave. The research is truly interdisciplinary and understandably that can make it hard even for experienced scientists outside the research to follow, because some of the critical areas of evidence have to do with sediment geochemistry, invertebrate modifications on bone surfaces, and the effects of groundwater on unconsolidated sediment fills. Personally, I’ve learned more about cave snails than I ever expected to know.

Here’s a short excerpt:

H. naledi is a newly-discovered species and we consider it unwise to adopt any prior assumptions about its behavioral repertoire. Although living non-human apes do not cache bodies, they do exhibit emotional, cognitive and social prerequisites of such behaviors (Pettitt, 2011). The closest living relative of H. naledi is our own species, which exhibits elaborate mortuary behavior in every culture. Evidence of body deposition in H. naledi merely extends a behavior already observed in archaic and pre-modern humans (Formicola and Buzhilova, 2004; Carbonell and Mosquera, 2006; Pettitt, 2011; Geiling and Marín-Arroyo, 2015) to a deeper node of our phylogenetic history. The geological age of the assemblage is presently not known, but is irrelevant to interpretation of this behavior.

The great news about our research is that more results keep coming in, and the team is developing a better and better understanding of the Rising Star cave system. For example, last month Ashley Kruger and colleagues published a great paper reviewing the team’s 3-D data collection strategies, with a new laser survey map of the present route to the Dinaledi Chamber. Our original research article on the context of the fossil assemblage remains open access in eLife, with detailed maps and analyses.

Laser survey data for the Rising Star cave system
Rendering of laser survey data from the Rising Star cave system, from Kruger et al. 2016.

People who attended the symposium on the Homo naledi research at the AAPA meetings earlier this spring got a good perspective on the kinds of research we are doing to uncover more about the context of the fossil remains, and more work will be coming out in upcoming months. In the meantime, I hope people find our reply helpful in working through the basic evidence that constrains hypotheses about deposition of remains in the Dinaledi Chamber. I’ve posted the PDF on my own server, which I never do for closed access journals, but in this case the editors specifically solicited commentary on an open access article, so I believe it should be made freely available and I will be personally disappointed if the Journal of Human Evolution does not make it freely available to the public as well.

Hominin remains from Mata Menge, Flores

I was really excited yesterday to read about the work of Gerrit van den Bergh and colleagues at Mata Menge, where they have uncovered hominin fossil remains attributable to an ancient population on Flores. The six teeth and one partial jaw were recovered from a “high-volume” excavation covering more than 200 square meters. They document the existence of a small-toothed and small-jawed human population on Flores approximately 700,000 years ago.

Mata Menge MM4 mandible
Mata Menge MM4 mandible, from figure 1 of van den Bergh et al. 2016.

Phylogenetic position of the Flores hominins

Earlier this spring, I reviewed the work by Sutikna and colleagues that revised the timeline of the Liang Bua hominin sample (“What the revised Liang Bua chronology leaves unanswered”). All of the remains of small-bodied hominins from Liang Bua now predate 60,000 years ago, making them earlier than the first known occurrence of modern humans anywhere in Indonesia. Paleoanthropologists have generated rival explanations for the phylogenetic relationships of the Liang Bua skeleton. Some propose that it represents evolutionary dwarfing from a larger-boded Homo erectus ancestor; others hypothesize that a previously unknown population of australopiths or smaller-bodied Homo may have existed in Asia and given rise to the Flores population.

LB1 preserves most of a skeleton, providing the potential for Homo floresiensis to be one of the most well-represented species in any phylogenetic analysis of the hominins. Most other hominin species are represented only by jaws and teeth, and maybe parts of the face and cranial vault. Yet despite the richness of evidence from LB1, its phylogenetic position remains uncertain.

The biggest problem is not the LB1 skeleton, it is the lack of evidence from other species.

To understand the scope of the problem, we can look at the two most recent attempts to place the LB1 specimen into the hominin phylogenetic tree. Both considered only the morphology of the skull, mandible and teeth. Valéry Zeitoun and colleagues (2016) concluded that LB1 lies within the variation of early H. erectus specimens from Java, including the Sangiran 2 and 17 specimens, the Trinil 2 specimen, added to the KNM-WT 15000 skull. They concluded that later “H. erectus” specimens from Java belong to a different clade, closer to Middle Pleistocene humans elsewhere and modern humans.

Phylogenetic analysis for Homo floresiensis by Zeitoun and colleagues 2016
Most parsimonious phylogeny from Zeitoun and colleagues (2016), figure 3. The LB1 specimen is nested within a group of specimens including Sangiran, Trinil and KNM-WT 15000 crania.

Meanwhile, Mana Dembo and colleagues (2015) concluded that H. floresiensis is an outgroup to a clade including H. rudolfensis, H. erectus and later species of Homo (but not H. habilis). However, the Bayes factor comparisons in this study could not reject the hypothesis that the closest sister group for H. floresiensis was H. erectus.

Phylogeny for hominins after Dembo et al. 2015
Highest probability phylogeny from Dembo and colleagues (2015), figure 1. In this tree, the Homo floresiensis branch is a sister to a branch including Homo rudolfensis and other species of Homo except for H. habilis. Note that the H. floresiensis branch is inferred to have originated just after 3 million years ago.

Those are two very different conclusions. The analyses included different groups of fossils, grouped them in different ways (species versus individual specimens), and looked at different sets of characters, with a different pattern of missing data. In the end, although the Bayes factor analysis by Dembo and colleagues (2015) did not look at the precise scenario favored by Zeitoun and colleagues (2016), it did show that a similar scenario cannot be rejected by the data. In the end, the data just aren’t good enough to tell between these.

It gets worse. Looking at whole-body evidence from hominin populations, it is evident that the few features of skulls and teeth that determine the outcomes of phylogenetic analyses are not necessarily typical of the skeleton as a whole. When we look at basal lineages within Homo, like populations of Homo erectus, Homo habilis, Homo rudolfensis, and Homo floresiensis, we are looking at a series of branches that diverged very close to each other, probably within a million years and potentially within a few hundred thousand years, which means that there may be few shared derived features linking the species within a clade. Yet some of those branches may be very long, particularly Homo floresiensis, meaning that there is a strong chance that the signal of phylogenetic relationship will be lost within the noise of long, independent evolutionary history.

I will add that there is a very real possibility of population mixing and introgression during the initial evolution of Homo, that would tend to obscure any simple tree of relationships among these species.

Homo floresiensis is not a uniquely confusing case. We face similar issues with the very complete skeletal evidence from Homo naledi. More evidence does not make this species easier to place on the phylogeny of Homo. In many ways, better evidence just directs our attention to how poor our efforts using partial jaws and teeth must be.

In that context, it is probably hopeless to expect that a partial fragment of jaw and six teeth are going to add useful data to better understand the phylogenetic context of the Flores hominins. Some people have commented that the Mata Menge teeth are “erectus-like”, or more similar to H. erectus than to H. habilis. I find the data unpersuasive. The jaw is unquestionably smaller than any adult mandible assigned to H. erectus, H. habilis, or H. naledi, as is the lower molar (whether it is a first or second) and the premolar. The small sizes of all these elements would be derived relative to any primitive species within Homo, so being closer in size to H. erectus is not useful information—after all, they are even closer in size to H. sapiens!

The deciduous canines and the central upper incisor stand out as unusually small and not morphologically typical of modern humans or fossil Homo erectus, but they are approximately the same sizes as the deciduous canines of Homo naledi. If no one else has suggested that H. naledi gave rise to the Flores hominins, I’ll be happy to be the first.

The mandibular corpus preserves no diagnostic morphology other than its small size, and it is within the range of sizes of modern humans. There are only a few non-metric traits of the teeth that can be assessed, which are shared with specimens of H. erectus and H. habilis, and the shape of the molar is more erectus-like than habilis-like. That’s weak evidence, since the small size of the molar probably confounds its shape (it’s like modern humans in shape as well). If these specimens had been recovered from the surface instead of from an excavation, they would have been difficult or impossible to authenticate as representing an ancient population. There’s just too little evidence there.

Flores reinvasion?

The authors of the research have done well by not over-emphasizing the quality of the morphological evidence in their research paper. The remains do not share any of the traits used to diagnose Homo floresiensis, which justifies the caution of van den Bergh and colleagues in not assigning them to that species.

The remains also do not settle whether small body size had appeared in the Mata Menge hominins. Some commentators seem to be assuming that these teeth do belong to the same population as the later Liang Bua remains, and are inferring a small body size on the basis of a slightly smaller size than the Liang Bua mandibular and dental sample. But nowhere else in the hominin fossil record would we be safe in assuming that jaw and tooth size are good indicators of body size, and I think the assumption is unwarranted here.

It is certainly possible that the small Mata Menge teeth and jaw represent a similarly small-bodied population, and I would not be surprised if the next bone to be discovered was a tiny tibia along the lines of LB6. But the next most comparable species for the sizes of the teeth are modern humans and Homo naledi, neither of which are nearly so small in body size as LB1 or LB6 from Liang Bua. More broadly, body size and tooth and jaw size are not well correlated among hominin species. There are notably big-toothed and small-bodied Homo erectus specimens, and smaller-toothed and big-bodied Homo erectus specimens. These teeth and this jaw are within the size range of modern human jaws and teeth; their bodies may have been as well.

Realistically, the morphology can give little indication that the Mata Menge hominin sample represents an ancestral population for the later Liang Bua sample. As some have pointed out, Flores may have been invaded more than once by hominin populations, and such populations may independently have evolved small mandible and tooth sizes, or even small body sizes.

To know that reinvasion is a plausible scenario, we need look no further than the local proboscideans. Flores was invaded at least twice by successive Stegodon species that apparently did evolve smaller body size independently. These creatures are abundant in the fossil record of Mata Menge and Liang Bua, and they likely existed at higher population densities than the hominins—even though elephants in general live at fairly low densities when compared to other smaller terrestrial herbivores. The idea that Flores could not have been reinvaded by hominins seems to be based on the assumption that the ancestral population arrived by accident and constituted a “lost world” phenomenon. I wouldn’t make that assumption.

Moreover, there’s a problem with the “lost world” hypothesis. If hominins on Flores had the same low population densities as we think characterized continental hominin populations during the Pleistocene, there couldn’t have been many of them. Such a population would have been more or less constantly at risk of extinction or mutational meltdown. It may not have been viable over evolutionary time.

Flores may have even undergone periods of complete abandonment followed by the introduction of new founder populations. Or new immigrants from a larger population may have had a genetic advantage within the strongly inbred Flores population. In either case, strong genetic and population turnovers may have occurred repeatedly, even if (maybe especially if) migration to the island was rare. I would even speculate that repeated entry of new populations onto Flores was accompanied by some introgression from the earlier population, if it was not extinct. Maybe small body size really did evolve a single time, and was retained over time due to adaptive introgression.

The founders of Flores populations may have come from the same source population or from different sources. As Chris Stringer pointed out in his public comment, the source population for Flores may well have inhabited Sulawesi, in which case the source population may itself have been a dwarf population of hominins, although larger in numbers than would be sustainable on Flores. For that matter, the body sizes of Javan and Chinese H. erectus populations were not as large as those reported for East African Early Pleistocene H. erectus. I wrote about this issue a few years ago (“The changing height of Homo erectus).

This is all unfounded speculation, but it is consistent with what we know (and don’t know) about the hominin fossil record and our knowledge of evolutionary processes. I remain excited about the recovery of evidence from Mata Menge, but that excitement is tempered by the inability of the evidence to test many interesting hypotheses.

Fast evolution of small body size?

Last, I’m very surprised to see paleoanthropologists in the press commenting that the dwarfing of Homo floresiensis was very rapid. The data are completely silent about the rate of evolutionary change in this case. To assess evolutionary rate, we need to know both the magnitude of change and the time available for change to have occurred. In this case, we know neither.

First, we simply do not know the body size of the Mata Menge hominins. Second, even if we assume they were small-bodied, we do not know the body size of their ancestral population. If they evolved from something like Dmanisi, we are talking about a rather minor amount of size reduction. If they evolved from an australopith-like ancestor, we may be looking at stasis in body and brain size.

Third, we have absolutely no reason to think that 300,000 years is the total time available for the evolutionary change. The first occurrence of archaeology on the island must be later than the first appearance of hominins. The artifacts from Wolo Sege show hominin activity prior to 1 million years ago, and Brumm and colleagues (2010) concluded that the existing sedimentary record of the Soa Basin “may not be old enough to register the initial arrival of hominins on the island.” We have no reason to assume that the date of the Wolo Sege artifacts was close to the arrival time.

Indeed, if Dembo and colleagues were correct about the evolutionary relationships of H. floresiensis, their estimate for the origin of the branch leading to the species is nearly 3 million years ago. Is it possible that hominins were on Flores more than a million years before the Wolo Sege artifacts? Maybe so. We cannot test the hypothesis at present.

This goes to a broader problem in paleoanthropology: Too many of our professional colleagues assume that the origin of a species can be equated with its first occurrence in the fossil record. It would be worse than foolish to assume that the record is good enough to document the earliest occupation of Flores by hominins. The literature on the subject tells us directly that the record is not good enough to test when hominins arrived on the island.

So we do not know the rate of evolutionary change in this case. I will add just say one more thing: Three hundred thousand years is a lot of time. It is more time that we used to imagine for the initial expansion of body and brain size in Homo erectus. It is plenty of time for selection to transform body and brain size in a hominin population.


van den Bergh, Gerrit D., Yousuke Kaifu, Iwan Kurniawan, Reiko T. Kono, Adam Brumm, Erick Setiyabudi, Fachroel Aziz and Michael J. Morwood. Homo floresiensis-like fossils from the early Middle Pleistocene of Flores. Nature 534, 245–248. doi:10.1038/nature17999

Brumm, Adam, Gerrit D. van den Bergh, Michael Storey, Iwan Kurniawan, Brent V. Alloway, Ruly Setiawan, Erick Setiyabudi, Rainer Grün, Mark W. Moore, Dida Yurnaldi, Mika R. Puspaningrum, Unggul P. Wibowo, Halmi Insani, Indra Sutisna, John A. Westgate, Nick J. G. Pearce, Mathieu Duval, Hanneke J. M. Meijer, Fachroel Aziz, Thomas Sutikna, Sander van der Kaars, Stephanie Flude and Michael J. Morwood. Age and context of the oldest known hominin fossils from Flores. Nature 534, 249–253. doi:10.1038/nature17663

Brumm, Adam, Gitte M. Jensen, Gert D. van den Bergh, Michael J. Morwood, Iwan Kurniawan, Fachroel Aziz, and Michael Storey. 2010. Hominins on Flores, Indonesia, by one million years ago. Nature 464, 748-752. doi:10.1038/nature08844

Sutikna, T., Tocheri, M. W., Morwood, M. J., Saptomo, E. W., Awe, R. D., Wasisto, S., ... & Storey, M. (2016). Revised stratigraphy and chronology for Homo floresiensis at Liang Bua in Indonesia. Nature. doi:10.1038/nature17179

Zeitoun, Valéry, Véronique Barriel, and Harry Widianto. 2016 Phylogenetic analysis of the calvaria of Homo floresiensis. Comptes Rendus Palevol 15, 555-568. doi:10.1016/j.crpv.2015.12.002

Dembo, Mana, Nicholas J. Matzke, Arne Ø. Mooers, and Mark Collard. 2015. Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships. Proc. R. Soc. B, 282, 20150943. doi:10.1098/rspb.2015.0943

The Guardian reports on a recent cave art discovery in Spain: “Spanish archaeologists discover cave art to rival country’s best”.

Chief site archaeologist Diego Garate said that an estimated 70 drawings were found on ledges 300m (1,000 ft) underground in the Atxurra cave in the northern Basque region. He described the site as being in “the Champions League” of cave art and among the top 10 sites in Europe. The engravings and paintings feature horses, buffalo, goats and deer, dating back 12,500-14,500 years.

If significant cave art remains undiscovered in Spain, imagine what that says about how little we know in the rest of the world.

Neandertal stone circles at Bruniquel Cave

I want to reflect for a moment on the first passage in the recent paper by Jacques Jaubert and colleagues (2016). The paper describes a series of circular structures, made like stone fencerows out of portions of stalagmites, that ancient Neandertals constructed deep within the Bruniquel Cave some 176,000 years ago.

Here are those first two sentences (the rest of the first paragraph introduces the stone structures):

Very little is known about Neanderthal cultures, particularly early ones. Other than lithic implements and exceptional bone tools, very few artefacts have been preserved. While those that do remain include red and black pigments and burial sites, these indications of modernity are extremely sparse and few have been precisely dated, thus greatly limiting our knowledge of these predecessors of modern humans.

This short summary of the state of our knowledge about Neandertal cultures is entirely correct. But at the same time, I think it summarizes only half the problem.

Archaeologists know well that the record of material culture that they can study is biased in various ways, sometimes extreme. They know that material artifacts have multiple uses and purposes within human social systems, and that testing hypotheses about some of the functions of artifacts requires evidence of patterning that can come only from recovering thousands of them across space and time. Even when the archaeological record approaches numbers of many thousands of each type of artifact, as in southwestern France after some 50,000 years ago, the patterns left on the landscape by ancient social systems may blend and mix because the people moved and cultures changed. The cultural patterning that archaeologists find in this later Middle Paleolithic record therefore reflects aspects of human behavior that lie at a larger scale than cultures as we recognize them in the ethnographic present.

Bruniquel circular structures plan view
Figure 1 from Jaubert et al. 2016.

For this reason, archaeologists who are interested in cognitive evolution and the cultural potential of ancient humans by and large cannot rely upon spatial and temporal patterning of artifacts. Or, to the extent that they rely on patterning for evidence about such cultural abilities, they interpret the evidence as entirely negative. The Acheulean is spread across a million years of time and three continents of space, as recognized by the “type” artifact, the handaxe. To some archaeologists, this is powerful negative evidence about the cognitive and cultural abilities of ancient people. After all, if they were clever, wouldn’t they have done something more interesting? Wouldn’t they have cultural patterning on the scale of recent people? The mere existence of some spatial patterning is one of the more powerful arguments for a shift in the Middle Stone Age of Africa toward a more sophisticated array of cultural abilities. It remains unclear, however, to what extent this “change” is merely a result of the increased intensity of investigation and density of evidence from Middle Stone Age sites.

And so, archaeologists of a cognitive bent tend to focus on another category of evidence: artifacts that require a complex series of steps to manufacture, or that are themselves inexplicable without reference to social phenomena. These are the “black swans” of Paleolithic archaeology. They are intrinsically rare in the record, but it hardly matters. The mere fact that a Neandertal might produce birch pitch, with its complex series of manufacturing steps, speaks more about the cognitive abilities of these ancient people than fifty thousand side scrapers.

Going deep into a cave and building stone circles from stalagmites is clearly one such activity. The mere existence of the structures speaks by itself of a level of social and cognitive abilities in the hominins who built them. That is why the report of such a thing is newsworthy, and why it is worthwhile to document so intensively the timeline of their manufacture.

But adding rare things to the numerator of Neandertal abilities is itself a bias, because the denominator is unknown and large.

Across the entire timespan of existence of Neandertals and the branch that gave rise to them, probably fewer than 50,000 of them existed at any time. I would not be much surprised if the true number was much smaller. If the average lifespan of a Neandertal was 20 years, maintaining a population of 50,000 individuals would require around 7 births per day. For the more than half million years this population and its ancestors existed, back past Sima de los Huesos to their common ancestors with Denisovans and African peoples, we can say there were as many as 1.3 billion Neandertals.

Weigh that against how little we know of them, how few pieces of their cultures they left for us. We do not know what the cultural production of an average Neandertal could have been, this is why the denominator is unknown. But it is evident that the fraction represented by the archaeological record is tiny.

The accompanying opinion essay by Marie Soressi is well worth reading, in it she reminds archaeologists of the limits of preservation:

These structures are among the best-preserved constructions known for the whole of the Pleistocene epoch, probably because they were sealed by calcite very soon after they were erected. When the best evidence is found in the best-preserved context, it serves as a reminder for archaeologists of how much we depend on preservation. The fact that some of the art of the period is also often found deep inside caves has been alternatively interpreted as a testimony of the preservation provided by the cave environment3 or as a result of spiritual preoccupations — the underground being a special place4. Perhaps we need to further consider the idea that the fuzziness of the Neanderthal record is due to a lack of preservation.

One might argue that the fact that we only find a tiny number of uniquely informative Neandertal-associated artifact is itself information. Surely, if the Neandertals had been more culturally productive, more modern, they would have left more of a record? Soressi’s essay addresses that argument to some extent, but I want to examine a slightly different point of view. The fact is, it’s hardly just Neandertals. We know very little about the ancient cultures of modern humans.

As recently as the mid-twentieth century, the world’s peoples spoke more than 6000 languages, each representing a culture with some time depth, some antiquity. Yet the vast majority of these languages could be grouped into a much smaller number of families of languages, most of which had their own origins within the last several thousand years. The number of branches leading to extant languages that existed more than 10,000 years ago is today tiny. Ten thousand years ago, the world was full of modern humans. Their languages, their cultures, which must themselves have numbered in the thousands, are mostly today extinct. As we know increasingly from ancient DNA, today’s people derive most of their genetic heritage from only a very small subset of the people who existed 10,000 years ago. That is, early modern humans around the world have left very few cultural traces and many of them have left no genetic traces in today’s peoples. They are gone, almost without a trace.

How surprising is this absence of information from these earlier modern humans? Surely the situation is not so bad as for Neandertals, after all, we have the fairly dense Upper Paleolithic record of Europe, the Maghreb, the Natufian, there are real areas where we have lots of archaeological information from these people between 30,000 and 10,000 years ago. But Southeast Asia and large parts of Africa–home to the majority of the world’s population at the time–have a very sparse archaeological record with many blank spaces. As we are increasingly becoming aware, the first third of human occupation of the Americas is documented by only a handful of archaeological sites. Who knows how many millions of people lived without leaving any record that archaeologists have yet found?

Worldwide, they were not nearly so sparse as Neandertals. Of these early modern humans, by the time they inhabited Australia and entered the Americas, there were tens of millions. If the lifespan of these modern humans averaged 25 years, it would take on the order of 1000 births a day to maintain a population of 10 million humans. From 30,000 years ago to 10,000, a mere 20,000 years of time, some 7.3 billion modern humans would have existed, under this set of assumptions. The true number of course was probably more. This is not the same space as Neandertals; these modern humans lived around much of the world, not just western Eurasia. But without question their population was an order of magnitude larger.

Arguably, our archaeological knowledge of these vast multitudes of people is much greater than what we know so far of Neandertals. As Soressi points out, the archaeological record is biased by time, by the better chance of preserving evidence from these recent time periods, by the kind of artifacts that some of these modern humans made. What is clear is that even for modern humans within the last 30,000 years, vast spans of time and space are complete unknowns.

Again, we do not know the true size of the denominator, but it is large enough to know that the fraction archaeologists see is tiny.

We know so little about the past. As long as this is true, our view of the past will disproportionately be based on the greatest achievements we have found so far. Water crossings imply maritime abilities, technology for sailing and navigating. Regular use of deep underground spaces implies controlled fire, dominance over other fauna that use caves, social systems capable of escape if the light should be lost.

This logic does not apply only to Neandertals, of course. I really like the methodology applied by Jaubert and colleagues, and the paper is basically straightforward. Still I do have a bone to pick with the paper’s review of the use of cave environments by hominins:

Deep karst occupation does not appear to have occurred in Africa in any period, whether the Early or Middle Stone Age, or even the Late Stone Age if we exclude shelters and cave entrances with evidence for human presence in South Africa, Ethiopia and Maghreb (Extended Data Fig. 8). The oldest evidence for the appropriation of this difficult environment is found in Europe, Southeast Asia/Sunda, Wallacea and Australia/Sahul. The accumulation of human bodies by Acheuleans at Sima de los Huesos, Spain (0.35 Ma) is very different from the Bruniquel structures, however. In other examples, the human frequentation of caves is linked to engraving, painting or sculpting activities. These sites are thus younger than 42,000 calibrated years before present and are always associated with Homo s. sapiens. Symbolic, cultural or funerary activities were the main reasons for these cave visits. Until now no evidence has been found for regular Neanderthal incursions into caves, except for a possible case of footprints27, and Neanderthal constructions inside caves, at least at a distance that is no longer exposed to daylight, were totally unknown. Moreover, Upper Palaeolithic constructions in caves are limited to fireplaces, simple hearths, and some rock or speleothem displacements. Even in caves regularly visited since the Aurignacian, constructions are non-existent or anecdotal.

I am very familiar with one African site in which a primitive non-modern hominin species is clearly in a deep cave environment. Homo naledi is there deep in the Rising Star cave with no direct surface access. It’s not quite as far as Bruniquel, but it’s not peanuts, either. That is good evidence for some degree of deep cave access by that species.


Jaubert, J. and many others. 2016. Early Neanderthal constructions deep in Bruniquel Cave in southwestern France. Nature doi:10.1038/nature18291

Soressi, M. 2016. Neanderthals built underground. Nature doi:10.1038/nature18440

The developmental obstetrical dilemma

Alik Huseynov and colleagues have a data-rich paper in the Proceedings of the National Academy of Sciences examining age-related changes in the human pelvis: “Developmental evidence for obstetric adaptation of the human female pelvis”. In the paper, Huseynov and colleagues present a new hypothesis for the evolution of sexual dimorphism in the hominin pelvis: the “Developmental Obstetrical Dilemma” hypothesis.

Here’s the paper’s abstract:

The obstetrical dilemma hypothesis states that the human female pelvis represents a compromise between designs most suitable for childbirth and bipedal locomotion, respectively. This hypothesis has been challenged recently on biomechanical, metabolic, and biocultural grounds. Here we provide evidence for the pelvis’ developmental adaptation to the problem of birthing large-headed/large-bodied babies. We show that the female pelvis reaches its obstetrically most adequate morphology around the time of maximum fertility but later reverts to a mode of development similar to that of males, which significantly reduces the dimensions of the birth canal. These developmental changes are likely mediated by hormonal changes during puberty and menopause, indicating “on-demand” adjustment of pelvic shape to the needs of childbirth.

I really like this paper and the Developmental Obstetrical Dilemma hypothesis. I think the idea makes a great deal of sense. What I see as the most important result of the paper is that the authors find that the female pelvis achieves its maximal inlet dimensions only around age 25-30. As the authors indicate, this is when female fertility is at a maximum. But from an evolutionary point of view, this timing reflects a serious trade-off that has previously not been clearly recognized. Females mature sexually, in many societies marry, and begin having offspring at substantially younger ages than 25.

If a woman is still developing her pelvic inlet at these younger ages, then infants born at those ages face a higher risk of fetal-pelvic disproportion, elevating the chances of a difficult birth and infant mortality, and slightly increasing the mortality risk of young mothers. All this is concordant with conventional wisdom about births to young mothers.

But from an evolutionary point of view, this seems paradoxical. The force of selection is maximal on individuals just at the beginning of their reproductive lives, when they have survived infant and juvenile mortality, and have all their adult reproduction ahead of them. The force of selection on 25-year-old mothers is actually lower than that on 18-year-old mothers. Why do younger women not develop their pelves faster, so that their early offspring will have the lower risk of birth complications enjoyed by children they have in their late twenties?

I don’t think the “pelvic shape on demand” aspect of the Huseynov paper answers this question. But I think the paper’s results point to a reason for the delayed pelvic development. The early component of a woman’s reproductive life, from menarche to maximal pelvic development is essentially a compromise between the fitness advantage of early reproduction and the fitness advantage of a large (and large-brained) offspring. The answer to “why don’t women develop faster” is that if they developed their skeleton faster, they would move first birth even younger than it already is. Natural selection would favor even younger births just to the point that the mortality cost balances the fertility advantage.

When we look at the average age of male first reproduction in traditional societies, it is substantially later than female first reproduction, but much more similar to the time that women gain their maximal pelvic dimensions. From this point of view, the component of a woman’s reproductive lifespan before this time is a roll of the evolutionary dice. Early children contribute very strongly to the growth of populations, so there must have been a strong selective pressure for early reproduction during the origin of modern humans, and probably at many earlier times in our evolutionary history.

The press coverage of this paper has largely focused on one aspect of the analysis; the observation that female pelves continue to change in shape as women age, so that post-menopausal women have slightly more constricted pelvic inlets than younger women. This is a bit unfortunate for two reasons. First, the amount of change in older women is relatively slight. Speculations about the selective value of pelvic changes in older women are probably without much merit, considering that the force of selection on older individuals of both sexes is very small, and the amount of change posited here is so small.

Second, the sample examined here is not a longitudinal sample, it is a cross-sectional sample. The human individuals are a wonderful resource and irreplaceable, and I sincerely hope that CT-scans of these will be made available on an open access basis. But they do not document age-related changes in the same individuals over time, they document the way that dead people of different ages vary. This means that the 80-year-olds do not represent the same set of birth cohorts as the 40-year-olds and the 20-year-olds. This difference is not such a factor when looking at the initial development of the pelvis through childhood and early adulthood, but it does make a big difference when comparing mature and senescent samples. I do not doubt that some age-related changes documented here in this sample are really characteristic of the European population. But older individuals represent a very different early childhood nutritional and disease history than younger individuals in this sample.

In other words, the study does not address, and does not present data to reject, the hypothesis that the 80-year-olds may have already had pelvic morphology at age 40 that was different from the 40-year-olds in the sample. That being said, I do think the comparison with males, which do not exhibit the same pattern of age-related changes, is sufficient to lead us to think that a female-specific pattern exists.

But at any rate, this part of the study is not central to the evolutionary history. Changes to pelvic morphology associated with very elevated ages must be a very recent phenomenon within human populations, and selection associated with them must have been very slight. What the study shows about the development of the pelvis in early adulthood is comparatively profound.


Huseynov A, Zollikofer CPE, Coudyzer W, Gaschoc D, Kellenberger C, Hinzpeter R, Ponce de León MS. 2016. Developmental evidence for obstetric adaptation of the human female pelvis. Proceedings of the National Academy of Sciences, USA (online) doi:10.1073/pnas.1517085113

Mitochondrial evidence of introgression among North American mammoths

Hendrik Poinar and colleagues have a new paper in Frontiers in Ecology and Evolution that reports new mitochondrial genomes from 67 North American mammoth specimens. These include specimens attributed to three mammoth species defined by paleontologists, the Columbian mammoth (Mammuthus columbi), the Jefferson mammoth (M. jeffersoni) and the pygmy mammoth (M. exilis), which they add to pre-existing data from permafrost-preserved woolly mammoths (M. primigenius). This dataset enabled them for the first time to generate a picture of the diversity of this ancient extinct lineage extending into temperate latitudes of North America.

Mammoth tooth detail
Mammoth tooth. Photo credit: James St. John CC-BY

What they found is that the mitochondrial clades exhibit many instances of non-correspondence with mammoth species as recognized by paleontologists. The paper’s discussion of mammoth phylogenetic hypotheses is extensive but a bit cloudy. The main issue is the relationship of Columbian and woolly mammoths. Columbian mammoths were endemic in North America and evolved sometime early in the Pleistocene. Woolly mammoths seem to have evolved relatively recently from the steppe mammoth M. trogontherii, inhabited northern parts of Siberia and Beringia, but reached south of the ice sheets in North America only within the past 125,000 years. After that time, they both coexisted in parts of North America.

Paleontologists have previously hypothesized hybridization between these mammoth species, looking both at skeletal and genetic evidence. Mammoth systematics has relied heavily upon molar morphology, and the number of lamellar plates of the molars is a main diagnostic criterion. Individual mammoths varied in the number of these enamel plates; Columbian mammoths had an average of 18-20 lamellar plates in their molars similar to steppe mammoths, while woolly mammoths tended to have more plates, at a higher density. The woolly mammoth morphology appeared first in Siberia and spread into Europe some 200,000 years ago. Some paleontologists had already suggested that Jefferson’s mammoth is an ecotype within the eastern United States that resulted from hybridization between Columbian and woolly mammoths.

An earlier mitochondrial study by Enk and colleagues (2011) found that two Columbian mammoths had mtDNA types that nest within the variability known for woolly mammoths, this despite the fact that Columbian mammoths were in North America long before the first woolly mammoths appeared in Eurasia. This finding seemed to point to a recent introgression of woolly mammoth mtDNA types into Columbian mammoth populations. What remained was the question of whether this introgression might represent a widespread replacement of Columbian mammoth mtDNA by the woolly mammoth haplogroup, or whether they had just sampled hybrids by chance.

The current study adds dozens of specimens of Columbian and Jefferson mammoths, and these form a fairly clear picture in comparison to the woolly mammoths. Woolly mammoths of Siberia and Beringia belong to three mtDNA clades, which share a common mtDNA ancestor sometime in the Early to Middle Pleistocene. Two of these are quite divergent and relatively rarely found within the sample studied here. One of the clades is very diverse and includes woolly mammoths from Siberia, Beringia, and North America south of the icen sheets. This clade, which the study denotes as “clade 1”, also includes the Columbian and Jefferson mammoths.

The figure from the paper that shows this phylogeny is large and complicated, too much to try to include here – it’s a whole page multi-pane figure with three distinct color schemes and legends describing them. It has geographic, phylogenetic and taxonomic information all mixed together, and while it is a great figure, it’s probably crying out for a better visualization method. So I’m leaving it out of this post.

There is structure within the mtDNA clade that includes both Columbian and woolly mammoths. The Columbian mammoths are all part of a single branch, and the sister of this branch includes mtDNA lineages mostly found in woolly mammoths of eastern North America, along with some Beringian woolly mammoths. Jefferson mammoths are scattered across both these branches. To the extent that the Jefferson mammoths are morphologically intermediate and suggestive of hybridization between woolly and Columbian mammoth populations, their highly diverse mtDNA suggests that they were likely the result of multiple introgression events. In the earlier paper by Eck and colleagues (2011), they compare this situation to forest and savanna African elephants, which have multiple instances of mtDNA introgression as well.

I’m never in favor of interpreting too much on the basis of the single mtDNA phylogeny. The paper agrees that nuclear DNA will be necessary to resolve how introgression and hybridization have really affected the mammoth populations.

That being said, the mtDNA in this case is provocative for more than the apparent mixing represented by the Jefferson mammoths. The mtDNA clade that includes both Columbian and some woolly mammoths seems younger than the origin of Columbian mammoths. The paper goes into substantial detail about why it is difficult to get accurate estimates of the time of mtDNA common ancestors, largely because the “tips” of the branches are separated in part by slightly deleterious mutations that would not persist over very much evolutionary time, so the deeper “roots” of the tree reflect a relatively slower rate of substitutions. But some problem remains even if the age of this clade is somewhat older than the rates suggested in this paper. The paper suggests two possible resolutions. Less likely, the authors propose that the Columbian mammoths had their mitochondrial genomes completely replaced by a woolly-mammoth-derived mtDNA clade sometime after the arrival of woolly mammoths

More likely, the authors propose that mtDNA introgression went the opposite direction, with woolly mammoths taking a North American clade and invading Eurasia with it. They support this by observing that mammoths carrying the clade 1 seem to have included the latest survivors in Eurasia, as if this successful lineage of mammoths had reinvaded and supplanted the earlier, more diverse mammoths belonging to clades 2 and 3. Possibly these woolly mammoths carried adaptive traits with origins in North America that helped them to spread; or maybe they simply exploited an opening left by the decline of woolly mammoths in Eurasia during the later part of the last Ice Age. It is even conceivable that the mtDNA itself was a target of selection, comparison to the phylogeography of nuclear loci would help to settle this.

This scenario is not quite as good a fit to the mtDNA phylogeny; it would require some incomplete lineage sorting to explain why Columbian mammoths are nested within the woolly mammoth clade 1 instead of having the most basal clade 1 subclade. But it fits within the evidence of dynamic replacement of mtDNA within the population of Eurasia.

And it raises interesting possibilities. Woolly mammoths originated from steppe mammoths by reducing body size, shortening the skull, and increasing the number and density of enamel plates in the molars. By the late Middle Pleistocene, they had supplanted steppe mammoths across Eurasia.

In North America, the Columbian mammoth was in many respects the ecological equivalent of the steppe mammoth; so much so that some paleontologists consider them a geographic continuation of the same species lineage. When woolly mammoths re-encountered this species in the Late Pleistocene, they evidently had no reproductive barrier and may have picked up many adaptive traits.

Poinar and colleagues consider what these scenarios mean for taxonomic practice within the mammoths:

Are columbi and primigenius still to be regarded as “good” species if they were capable of introgressing despite a possible million-year difference in their divergence times from trogontherii ancestors? Or is this lengthy difference illusory, because mammoths on both sides of the Bering Strait experienced dynamic population histories of immigrations, contractions, expansions, introgressions and replacements [13; 14; 18], a now well-established finding that throws into question traditional species designations. This point also applies to making assumptions about unidirectional change in morphological attributes, a highly unlikely proposition now that hybridization between supposedly long-separate lineages of North American mammoths has been adequately demonstrated.

From my point of view, all these estimates of timing of population separation and contact seem familiar. The establishment of the Columbian mammoth population in the Early to Middle Pleistocene ran along the same approximate timescale as the differentiation of African and Eurasian archaic human lineages, including the Neandertals and Denisovans. The introduction of woolly mammoths into North America occurred around the same time that modern humans may have been introduced to Asia. The back-migration of North American mtDNA lineages into Eurasian mammoths occurred around the same time that modern humans were dispersing into Australasia and northward into Siberia and Europe.


Poinar H, MacPhee R, Enk J, Devault A, Widga C, Saunders J, Szpak P, Southon J, Rouillard J-M, Shapiro B, Golding B, Zazula G, Froese D, Fisher D. Mammuthus Population Dynamics in Late Pleistocene North America: Divergence, Phylogeography and Introgression. Frontiers in Ecology and Evolution (in press) doi:10.3389/fevo.2016.00042

Enk, J., Devault, A., Debruyne, R., King, C. E., Treangen, T., O’Rourke, D., ... & Poinar, H. (2011). Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths. Genome biology, 12(5), R51. doi:10.1186/gb-2011-12-5-r51

Dmanisi and dispersal of Homo from Africa

Discover last April ran a feature article about the finds from Dmanisi. They have made this available online: “The First Humans to Know Winter”. Dmanisi is in some ways a keystone: Earliest site to preserve evidence of fossil humans outside of Africa, earliest site with clear evidence of H. erectus-like cranial and dental morphology, better chronological control than most East African contexts.

The article has an interesting exchange involving quotes from Michael Chazan and Martha Tappan, about the dispersal of early Homo:

Says Chazan: “The problem that keeps you awake, if you think about these things, is that if there was a dispersal event 2 million years ago, before H. erectus, would we see it? If they were using stone tools made of local materials, would we even pick it up? Are we building our models based on things we can’t see?” Dmanisi team member Tappen agrees the site’s fossils are challenging our current understanding of human evolution — but she’s not losing sleep over it.
“As archaeologists, we go with what we have. We make hypotheses and try to test them, and then you dig up something new and go ‘oops.’ And you have to make up a new hypothesis,” says Tappen.
“The Dmanisi individuals are not too different from H. habilis. We should find them dispersing out of Africa 2.5 million years ago,” she explains. “We don’t have that evidence yet, but we have to expect it’s out there.”

That kind of evidence is what some archaeologists claim to have found in Pakistan, with claimed early stone tools from Riwat and the Pabbi Hills; others believe that a pre-erectus habitation of Asia is necessary to explain the morphology of the Homo floresiensis remains from Liang Bua. In light of recent discoveries, I have no reason to think that such a pre-erectus emigration from Africa need have been very much like H. habilis or H. rudolfensis, though.

Jonathan Tennant and colleagues have a new review of the impacts of open access scientific publishing: “The academic, economic and societal impacts of Open Access: an evidence-based review”. The review comments on the costs of traditional subscription publishing:

The question of the current publication cost is difficult and confounded by estimates of the total global publishing costs and revenue. Data provided by Outsell, a consultant in Burlingame, California, suggest that the science-publishing industry generated $9.4 billion in revenue in 2011 and published around 1.8 million English-language articles. This equates to an approximate average revenue per article of $5,000. A white paper produced by the Max Planck Society estimated costs at €3,800–€5,000 per paper through subscription spending, based on a total global spending of €7.6 billion across 1.5–2 million articles per year in total (Schimmer et al., 2014). Other estimates suggest that the total spend on publishing, distribution and access to research is around £25 billion per year, with an additional £34 billion spent on reading those outputs, a sum which equates to around one third of the total annual global spend on research (£175 billion; Research Information Network (2008)).

I had a short Twitter convo the other day with a reader who felt unable to pursue open access publishing because of author fees. I’m no purist; many of my papers are best placed in subscription journals. But fees do not stop me from publishing articles in open access journals. Responsible journals waive fees for authors who do not have institutional or grant support for author fees, and of course many open access journals publish papers without any author fees.


Tennant JP, Waldner F, Jacques DC, Masuzzo P, Collister LB, Hartgerink CHJ. 2016. The academic, economic and societal impacts of Open Access: an evidence-based review. F1000 Research 5:632. doi:10.12688/f1000research.8460.1

Nature has an essay by Alex Csiszar recounting the first episode of peer review by the Royal Society, negotiated between William Whewell and John Lubbock on a paper about orbital motions by George Airy in 1831: “Peer review: Troubled from the start”. It went about as well as you would expect:

Feeling that they had reached an impasse, Lubbock went to the author himself to deliver his suggestions for improvement. Airy was understandably irritated that his manuscript was being subjected to this strange new procedure. “There the paper is,” he wrote to Whewell, “and I am willing to let my credit rest on it.” He had no intention of changing his text. Lubbock threatened to pull out, but ultimately relented and swallowed his criticisms, acknowledging that this was “the first report which the Council have ever made” and trying to see the bigger picture. He thanked Whewell for putting his “shoulder to the wheel” and signed his name to the report.

Seems like the first instance of the referee trying to horn his way in as an author.

Discover magazine did its March, 2016 cover story on the recent hominin discoveries of South Africa, including Rising Star and Malapa, and other important finds. They have now made that article available online: “Rethinking Humanity’s Roots”.

Genetic flatlining of island foxes

Carl Zimmer’s article on “Foxes That Endure Despite a Lack of Genetic Diversity” is interesting and useful:

However the animals arrived on the Channel Islands, they adapted quickly. The oldest island fox fossils date back 7,000 years and show that they were small even then. The Great Shrinking required less than 2,200 years, it seems.
Like other animals, island foxes carry two copies of each gene, inheriting one copy from each parent. In large populations with a lot of genetic variation, there can be many versions of any given gene. An animal may inherit two varying copies of a gene from its parents.
But the scientists discovered virtually no differences in the DNA the foxes had inherited. “We call it genetic flatlining,” Dr. Wayne said.

This is an extreme example of the situation that we consider likely to have generated substantial genetic load in Neandertals. In the foxes, there has been substantial phenotypic change but biologists do not yet know what negative or deleterious effects on the fox population may have resulted from the limited genetic variation. Several of the populations are endangered, and it is hard to know how much of their demographic challenge may be from their intrinsically low genetic variation as opposed to human disturbance to their habitat.

An even better hominin analog may be the Homo floresiensis situation, which was probably nearly as limited in genetic diversity, potentially for a much larger number of generations. Could a hominin population have persisted for thousands of generations in a “genetic flatline” situation?

Lee Berger had been named one of the “Pioneers” in the Time 100 Most Influential People. It’s quite an accomplishment for any anthropologist to make such a list, and it’s great to see the impact of recent fossil hominin discoveries ranking among the most significant news items in the world.

Australopithecus sediba fossils now on MorphoSource

Lee Berger gave the luncheon plenary lecture at the meeting of the American Association of Physical Anthropologists last Saturday, covering the recent discoveries from the Dinaledi Chamber and a broad historical overview of his exploration work.

MH1 skull

At the end of his lecture, he announced that the collection of hominin remains from Malapa are now available freely for download from the MorphoSource site. These remains include parts of two skeletons, designated MH1 and MH2, which belong to the species Australopithecus sediba. Sixty-eight specimens are currently on the site, including the MH1 skull and mandible, the pieces of the MH2 mandible, individual bones of the MH2 hand, and pelvic, vertebral, ribs, and long bones of both skeletons.

These are an incredible collection, and together with the surface scans of the Dinaledi hominin material, they provide a detailed comparison of the anatomy of two species across much of the skeleton.

Much credit belongs to Steven Churchill, who worked long to get these scans uploaded and released in conjunction with Lee’s announcement, as well as the many team members who carried out laser scanning of the material, particularly Scott Williams, Lauren Schroeder, Cody Prang, Ellie McNutt and Daniel Garcia-Martinez.