john hawks weblog

paleoanthropology, genetics and evolution

A. afarensis

  • "The catechism about genetic drift"

    Tue, 2006-05-02 13:32 -- John Hawks

    Razib has been working over genetic drift real good (concerning effective population size and population history, and founder effects). It deserves it.

    This post is about genetic drift applied to phenotypic -- not molecular -- evolution. The two are distinct for two important reasons: first, phenotypes are widely genetically correlated with each other while unlinked DNA sequences are not; and second, because the theoretical reasons for some nucleotides to have no correlation with fitness are very strong, but such theoretical reasons are nonexistent for phenotypes.

    Personally, I think selection is more important than drift at the molecular level as well, for reasons having to do with those "genetically correlated" and "unlinked" assumptions. But to the extent that neutral evolution may be credible for many genes, it is much less credible for most phenotypes.

    Here's what I tell my students:

    To explain the evolution of a feature in ancient humans, genetic drift is my absolute last resort...right before sexual selection.

    Why I don't like sexual selection is a topic for another day.

    For now, on to genetic drift. Here's what Gould and Lewontin's famous "spandrels" paper has to say:

    Have we not all heard the catechism about genetic drift: it can only be important in populations so small they are likely to become extinct before playing any sustained evolutionary role (but see Lande 1976) (Gould and Lewontin 1979:585-586).

    With some math, we can show that the "catechism" is not literally true -- genetic drift can cause substantial phenotypic evolution in large populations. But ...

    Some worked examples

    Lande (1976) shows genetic drift can cause phenotypic evolution consistent with many examples in the fossil record:

    This paper presents a statistical test for the hypothesis of evolution by random genetic drift, contingent on the effective population size. In examples from the fossil record, it is found that the rates of evolution equal to or greater than those observed have a significant probability of occurring by random genetic drift even in very large populations (Lande 1976:314-315).

    Let's consider an example not examined by Lande. One of the most significant temporal trends in the early hominid species Australopithecus afarensis is a decrease in the length of the lower third premolar. This decrease in length is associated with a change in the morphology of the tooth, in which a more sectorial one-cusped form becomes less common and a more bicuspid form becomes more common. Lockwood et al. (2000) show that the P3 length decreases from an average around 10.5 mm in the early, 3.5 Ma Laetoli sample down to an average around 8.5 mm in the latest 3.0 Ma Hadar sample. Estimating the standard deviation of the sample as a whole (including intermediate time periods at Hadar) is a bit complicated, but if we consider the mean as a moving average, then the standard deviation is between 1.0 and 1.5 mm. I'll assume 1.0 mm to be conservative.

    Lande (1976) derives the distribution of phenotypic change due to genetic drift in a population with effective size Ne. The average change due to genetic drift is no change -- the most likely result of random sampling is no change at all. Populations can change in either direction (larger or smaller) due to random sampling, and larger amounts of change are increasingly less likely. More change is likely in smaller populations, so that the amount of change depends on the effective population size. Lande gives an expression for the effective population size N* at which the observed amount of change is at the 95 percent confidence limit:

    If we assume h2 = 0.5, t = 25,000 generations, and the standard deviation is 1, then N* is estimated as 12,000. Since the effective population size of all extant hominoid species is around 10,000, this estimate is fully consistent with the evolution of P3 length by genetic drift alone.

    In fact, it's pretty hard to find anything in human evolution that couldn't have evolved by drift alone, under these assumptions. For example, Wolpoff and I (2001) found that the Middle Pleistocene increase in cranial capacity was consistent with genetic drift in a population with Ne = 1.8 x 106. The increase from early Neandertals to Würm Neandertals was less likely to occur by drift alone -- our estimate of Ne = 1.2 x 103 is quite a bit less than 10,000. On the other hand, there would be many who would argue that the effective population size in Europe alone really was that small, and that therefore the Neandertals increased their cranial capacity by genetic drift also.

    Now, the increase in endocranial volume in humans is one of the most impressive long-term evolutionary trends in mammals. If even that is explicable by genetic drift, then it is pretty clear that we don't ever need natural selection at all.

    So I should really like genetic drift, right? I mean, it explains everything, doesn't it?

    The fallacy

    Of course, what is actually going on is that we have chosen a null hypothesis that is especially hard to refute. This means we should expect a lot of type II error: using this method, we can't reject the hypothesis of genetic drift even if it isn't the right answer.

    What is worse, even if we were to show that the amount of phenotypic change is too great for a given effective population size, there will always be someone to argue that the effective population size was smaller in the past. So genetic drift is a moving target -- it is effectively impossible to reject.

    The operative problems here are (i) a relatively small amount of change over (ii) a very long period of time. This combination will usually be consistent with Lande's derivation for genetic drift and reasonable effective population sizes -- particularly if we cannot establish in advance what effective population size is actually reasonable.

    There is a big contrast between a long timescale and a short timescale in this comparison. Natural selection is certainly much faster than genetic drift on a short timescale -- the time to fixation of an adaptive allele by selection proceeds as the logarithm of population size, while the fixation time by drift proceeds linearly with population size. Genetic drift can change a population quickly, but only if the population is very small. Selection can change a large population quickly.

    The fallacy is the assumption that the difference between selection and drift over short timescales also is a difference over long timescales. There is some ultimate limit on the evolution of any character. Selection may make a mouse the size of a cat in a few hundred generations, but even assuming that those cat-sized mice can stick around, there is no reason to think that dog-sized mice will be better! At some point, selection will stabilize -- and for most characters the amount of change permitted by stabilizing selection is not too great. Sampled at time intervals of many hundreds of generations, selection may look exactly like genetic drift.

    What to do

    People think about genetic drift because of its mathematical convenience. Sampling error is predictable, and the repeated occurrence of sampling error over many generations follows well-known probability distributions.

    Selection is predictable too, but it requires you to actually know something about ecology. We often don't know anything, and when we do, we usually have some particular relationship in mind, which needs to be tested. So, we test the hypothesis of neutrality, with all its mathematical simplicity.

    But remembering that the null hypothesis is sometimes -- maybe even often -- true doesn't mean that we should be satisfied with any particular test of that null. For neutral evolution of phenotypes, there are more powerful tests than evolutionary rates. The problem is that these "tests" are not in large part quantitative, but instead are logical or qualitative.

    For example, it is very likely that human brains increased in size under selection because there should clearly have been selection against larger brains because of their energetic costs. The rate of evolution does not factor in here, and is in fact irrelevant to the assessment of selection.

    The case does require a more complex model than simple directional selection -- instead it involved a structured model in which the force of selection is mostly stabilized by a counterforce of selection. It also begs an explanation for why the change should have proceeded at a given rate -- for example, was it slow because of environmental constraints? Such constraints would seem a likely explanation for the rate of change of dental size in Australopithecus afarensis.

    But when most people talk about genetic drift, their reality doesn't seem to include the mathematical consequences of genetic drift.

    For one thing, genetic drift is sloooooow. It affects allele frequencies on a time scale in generations proportional to the effective population size.

    We sometimes hear that it is a bad thing to doubt the power and ubiquity of genetic drift. This doubt is sometimes equated with adaptationism, taken as the uncritical assumption of selection as a null hypothesis.

    References:

    Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B 205:581-598.

    Lockwood CA, Kimbel WH, Johanson DC. 2000. Temporal trends and metric variation in the mandibles and dentition of Australopithecus afarensis. J Hum Evol 39:23-55.

    Hawks J, Wolpoff MH. 2001. The accretion model of Neandertal evolution. Evolution 55:1474-1485.

    Tags: 
    genetic drift
    Hadar
    Neandertals
    Middle Pleistocene
    genetic drift
    A. afarensis

  • "Spacecraft all over the Pliocene"

    Thu, 2006-04-27 08:34 -- John Hawks

    Rex Dalton has a great two-page article in Nature about the bush vs. ladder dispute. It keys off of the Middle Awash Australopithecus anamensis article by White and colleagues from a couple of weeks ago.

    If you recall that one, White et al. posited that Ardipithecus was likely ancestral to Au. anamensis, and that the two did not overlap in time. Here's the key exchange in the Dalton piece:

    This month's Nature paper makes a bold argument, and shows the Awash team seeking to put its mark on the record. Others in the
    field are impressed. "When you find 30 new hominid fossils, you are allowed a certain amount of conjecture," says Bernard Wood, a palaeoanthropologist at George Washington University in Washington DC. "As always, they have done a fantastic job."

    But he and others are unconvinced by the Awash team's conclusion: "This is only the first half of the rugby match," says Wood. Meave Leakey, lead author on the Au. anamensis discoveries in Kenya, is more blunt. "I don't believe this," she says. "We do not have the specimens to fill the gaps."

    Leakey and Wood are among those who believe that other, as yet undiscovered hominid species may have lived at this time, from 4.4 million to 2.9 million years ago. The existence of other species would cloud or eliminate the argument for a direct lineage. "My prejudice is there are more lineages rather than fewer -- more diversity," says Wood. "I have to concede these new data are dramatic. But we should beware coming out with a complete explanation when we don't have all the
    evidence."

    This argument frustrates White. "There were Martians there back then too," he says. "And spacecraft all over the Pliocene -- we just haven't found them yet."

    Waiting for Monte Cassino

    In a series of articles since 2000, White and colleagues have laid out a systematic attack on the "bushy" phylogeny model. Their arguments have extended across four million years and seven species, with a breadth that rivals the Allies breaking the Winter Line.

    Consider the angles of attack:

    1. Au. anamensis -- Au. afarensis. Everyone basically accepts that Au. anamensis is a direct ancestor of Au. afarensis. And the two species are really not very different from each other -- for instance, they are more alike than either is to Ardipithecus. The transition between these species would look to be a simple case of anagenesis, except...

    ...for Kenyanthropus (Leakey et al. 2001). This small-toothed, flat faced hominid needs an ancestor, too. Au. anamensis might have been the common ancestor of Kenyanthropus and Au. afarensis. If so, then both these later species originated by cladogenesis from Au. anamensis. A similar argument might be made for other species, like Australopithecus bahrelghazali (Brunet et al. 1996) or the Sterkfontein Member 2 hominids. But Au. bahrelghazali is only known from a partial mandible and only differs from Au. afarensis by a three-rooted premolar, which is considered by many to be weak evidence, and the Sterkfontein Member 2 sample has not yet been taxonomically assigned -- they might turn out to be Au. afarensis, for example. Kenyanthropus remains the strongest case for cladogenesis (i.e., a "bush"). Yet...

    ...White (2003) denied that the Lomekwi skull KNM-WT 40000 was a distinct species. In particular, he argued that the extensive postmortem deformation of the skull made it impossible to substantiate an anatomical difference from Au. afarensis, and even if it was different, the anatomical diversity of living hominoid species is so great that it would probably encompass the difference between KNM-WT 40000 and known Au. afarensis crania.

    2. Earliest hominids. At the moment, the earliest putative hominids include three genera: Orrorin (Senut et al. 2000), Sahelanthropus (Brunet et al. 2002), and Ardipithecus, represented in the Late Miocene by Ar. kadabba (Haile-Selassie 2001, Haile-Selassie et al. 2004). Evidence for obligate bipedality has been challenged (by different researchers) for each of these three (I'm one of those who has questioned bipedality for Sahelanthropus).

    So far the only comparable anatomical parts from all three samples are teeth...

    ...which were examined by Haile-Selassie, Suwa and White (2004). They concluded that the variation among these three genera

    is no greater in degree than that seen within extant ape genera. Despite claims of molar enamel thickness differences among these late Miocene fossils, we question the interpretation that these taxa represent three separate genera or even lineages. Given the limited data currently available, it is possible that all of these remains represent specific or subspecific variation within a single genus (Haile-Selassie et al. 2004:1505).

    Additionally, Ohman, Lovejoy and White (2005) challenged the interpretation of the internal anatomy of the Orrorin femur, which had been suggested to be more derived than that of Au. afarensis. They wrote:

    We agree that the Lukeino femur's external morphology suggests some form of bipedality. Yet the more detailed original scans appear to show a distinct superior cortex different from Australopithecus and humans, with the cortex distribution being more primitive than that seen in any other hominid, including Australopithecus.

    The relevance of this argument to the phylogenetic diversity of early hominids depends on the anatomy of the Ardipithecus femur, which none of the rest of us are in a position to know. But one may speculate that if all these early "hominids" had femora with similar morphology, it would further reinforce the interpretation that they belong to a single lineage.

    3. Ardipithecus -- Au. anamensis. This is the current example. Here's how Dalton discusses it:

    The latest Afar discovery is exciting experts because it shows that the three hominids existing in the same area, but in successive time periods. Tim White of the University of California, Berkeley, co-leader of the Awash team, believes this points to a direct lineage between the three -- a process called phyletic evolution. The new Au. anamensis fossils are only 300,000 years younger than Ar. ramidus, meaning that if one became the other, the changes would have had to happen that fast. But the key point, says White, is that fossils of Au. anamensis and Au. afarensis have never been found in sediments the same age as those containing Ar. ramidus. If fossils of the different species were found together, that could show that they belonged to multiple lineages existing simultaneously.

    Finding remains of all three species in the same area but not from the same time period suggests they did not coexist, says White.

    ...

    The specimens also provide anatomical clues to evolutionary history. "The new Au. anamensis fossils are anatomically intermediate between the earlier Ar. ramidus and the later Au. afarensis," says White. For example, the teeth of the newly discovered Au. anamensis fossils seem adapted to chew tougher and more abrasive foods than Ar. ramidus. The researchers believe this shows that Au. anamensis had a broader diet. "All this strengthens the view that there is phyletic evolution from Ar. ramidus through Au. anamensis," says White. He believes he has nailed down the relationship between the two later species, although he says that further specimens are needed to prove the earlier link (Dalton 2006:1100).

    Of course, it would help matters if we knew in more detail what Ardipithecus looked like. But one must imagine that the stage is being set for its revelation. The unilineal interpretation places Ardipithecus at the critical point as an ancestor to the major mid-Pliocene australopithecine lineage. Extending the unilineal interpretation earlier into the Late Miocene would make Ardipithecus the earliest hominid as well.

    It is not necessary to think that taxonomic uniformity means anatomical uniformity, though. Ardipithecus already encompasses a trend of decreasing canine size and less sectorial P3 for example. A trend toward fuller skeletal adaptation to bipedality may also be imagined. But in that context, it is important to note that the time interval between the Orrorin femur and the unpublished Aramis skeleton is longer than the time between Aramis and Hadar. Those relative times may become quite important in thinking about the evolution of those postcrania.

    The Winter Line was broken at Monte Cassino, after many failed attempts from different approaches. The Aramis fossils are either the heavy shoe waiting to drop, or they are the uncomfortable foot that all this talk about phyletic evolution is meant to shoehorn into place.

    Commentary

    If all these cases are added together, they imply a single evolving lineage encompassing at least four anagenetic taxa, Ar. kadabba -- Ar. ramidus -- Au. anamensis -- Au. afarensis. This last would presumably be followed by a cladogenesis into a robust australopithecine species (Australopithecus aethiopicus) and Australopithecus africanus.

    One could add Homo erectus to this list, since White and colleagues argued in their description of the Daka skull (Asfaw et al. 2002) that the Asian and African samples represent one cosmopolitan species.

    But then one species sticks out as a surprising exception to the pattern: Australopithecus garhi (Asfaw et al. 1999). It will be interesting to see a close argument showing why this species is really different from South African Au. africanus. Say, more different than KNM-WT 40000 is from the Hadar crania. It's quite glaring, really, that this species should be there mucking up such a simple phylogeny.

    I have to say, after reviewing all these papers in one sitting -- this entire bush vs. ladder thing is getting very tiresome! I mean, isn't there something else that we could organize early hominid discoveries by? These are all papers in the top journals, and this is the (fairly specialized) discussion that has been promoted as the central issue in the field!

    The subtitle of the Dalton piece suggests that it is merely a philosophical difference:

    Deciding whether our ancestors evolved as a single lineage may depend more on philosophy than fossils.

    But that's not really true. There is a clear null hypothesis here, quite directly drawn from William of Ockham:

    entia non sunt multiplicanda praeter necessitatem

    Which of course means:

    Sometimes fossil samples really do form ancestor-descendant relationships.*

    (*) It doesn't really. It means "Entities should not be multiplied beyond necessity."

    References:

    Asfaw B, Gilbert WH, Beyene Y, Hart WK, Renne PR, WoldeGabriel G, Vrba ES, White TD. 2002. Remains of Homo erectus from Bouri, Middle Awash, Ethiopia. Nature 416:317-320. DOI link

    Asfaw B, White T, Lovejoy O, Latimer B, Simpson S, Suwa G. 1999. Australopithecus garhi: A new species of early hominid from Ethiopia. Science 284:629-635. DOI link

    Begun DR. 2004. The earliest hominins -- is less more? Science 202:1478-1480. DOI link

    Brunet M. and 37 others. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145-151. DOI link

    Brunet M, Beauvillain A, Coppens Y, Heintz E, Moutaye AHE, Pilbeam D. 1995. The first australopithecine 2,500 kilometres west of the Rift Valley (Chad). Nature 378:273-275. DOI link

    Dalton R. 2006. Feel it in your bones. Nature 440:1100-1101. DOI link

    Haile-Selassie Y. 2001. Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412:178-181. DOI link

    Haile-Selassie Y, Suwa G, White TD. 2004. Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science 303:1503-1505. DOI link

    Leakey MG, Spoor F, Brown FH, Gathogo PN, Kiarie C, Leakey LN, McDougall I. 2001. New hominin genus from eastern Africa shows diverse middle Pliocene lineages. Nature 410:433-440. DOI link

    Ohman JC, Lovejoy CO, White TD. 2005. Questions about the Orrorin femur. Science 307:845. DOI link

    Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y. 2001. First hominid from the Miocene (Lukeino formation, Kenya). Comptes Rendus 332:137-144.

    White T. 2003. Early hominids -- diversity or distortion? Science 299:1994-1996. DOI link

    Tags: 
    Miocene
    Homo erectus
    A. afarensis
    A. africanus
    Pliocene
    Sterkfontein
    Sahelanthropus
    Orrorin
    Hadar
    A. anamensis
    Ardipithecus
    Kenyanthropus

  • New news in New World settlement

    Sun, 2006-04-16 18:32 -- John Hawks

    Afarensis has a post on Brazilian evidence relating to the origins of Native Americans (via Gene Expression). It's a good summary of recent work by Neves and colleagues, including the background to this:

    In essence, Neves et al, is saying that Paleoindians were part of the expansion of H. sapiens out of Africa, whereas Native Americans represent a later expansion of specialized populations. I find this suggestion intriguing. There are skeptics, as you can see from the above quote from The National Geographic article. Powell is arguing that because America was populated by small populations, genetic drift would kick in and you would see a lot of variation between populations and that the Lagoa Santo populations fit within the pattern af variation seen in Native American populations. If that is the case, I would expect one or two populations to display morphology similar to Australians and Melanesians. Instead, what we have is a series running from southern Chile to Florida - and now Kennewick in Washington (which was not included in either study)- all of which display morphology similar to Australians, Melanesians and Polynesians.

    The idea of a "generalized" form for early modern humans has been around for awhile now, applied not only to Paleoindians, but also the Upper Cave crania from Zhoukoudian, and -- by some -- early modern Europeans.

    Tags: 
    America
    A. afarensis
    Zhoukoudian
    archaeology

  • A ladder, not a bush?

    Thu, 2006-04-13 01:52 -- John Hawks

    Tim White and colleagues (2006) report on new fossils from Aramis and a new site, Asa Issie, with estimated dates between 4.1 and 4.2 million years ago.

    In addition to the paper, there are articles in the New York Times (by John Noble Wilford), the Associated Press (by Seth Borenstein), and BBC (by Paul Rincon).

    The story is being played as another "missing link" -- this one between Ardipithecus and Australopithecus. From the Times:

    Tim D. White, a paleontologist at the University of California, Berkeley, who was a leader of the team, and his colleagues said the 4.1-million-year-old fossils were anatomically intermediate between the earlier species Ardipithecus ramidus and the later species Australopithecus afarensis, the Lucy family. The newfound bones and teeth are the earliest remains of the most primitive Australopithecus, known as anamensis.

    "This new discovery closes the gap between the fully blown australopithecines and earlier forms we call Ardipithecus," Dr. White said in a statement. "We now know where Australopithecus came from before four million years ago."

    The fossil specimens are a partial maxilla from Aramis, ARA-VP-14/1; two partial maxillary dentitions from Asa Issie numbered ASI-VP-2/2 and ASI-VP-2/334; and a large femur shaft fragment, ASI-VP-5/154. There are also several postcranial bones -- phalanges, vertebrae, a metatarsal -- that are pictured in some of the press accounts and briefly discussed but not pictured or numbered in the paper. The postcanine teeth in the maxillary specimens are larger than the known sample of Ardipithecus, but the canines are larger and more mesiodistally elongated than in Australopithecus afarensis. The best anatomical match for these features is with the Kanapoi and Allia Bay samples assigned to Australopithecus anamensis, and White and colleagues assign the new fossils to that species.

    So why are these fossils important? On the surface, there isn't very much to them. Three piecemeal upper dentitions don't tell much. They have big molars and big canines, both within the range of Au. anamensis. Neither they nor the femur shaft extend the known range of variation in early hominids.

    Remembering that every fossil fragment is a precious relic of a bygone age, the main importance of these is that they may address hypotheses about the biogeography of Early Pliocene hominids. The maxillae show that a large-molared hominid existed in the same geographic location at a later time than the small-molared Ardipithecus. That could be interesting, and it is the hook for the news stories and the team's press statement.

    The strongest part of this story is the geographic -- finding them in the Middle Awash instead of Kenya -- and the paleoenvironmental. There is some suggestion in the paper that there may be a paleoenvironmental difference at the sites that currently have evidence of Au. anamensis:

    Palaeoenvironmental circumstances surrounding Au. anamensis ~1,000 km to the south in Kenya have been described for Allia Bay as a mixed assemblage sampling aquatic, forest, grassland and bushland. Nearby Kanapoi conspecifics were found in another mix of environments described as dry, possibly open, wooded, or bushland conditions with a wide gallery forest in the vicinity. Habitat preferences in such mixed assemblages are difficult to ascertain despite the assertion that the hominids "favored mosaic settings". In contrast, the Ethiopian occurrence of Au. anamensis described here allows its tight spatial and temporal placement in a vertebrate assemblage with taphonomic integrity. Its relative abundance suggests that it was a regular occupant of a wooded biome that appears to have persisted in this part of the Afar during the 200,000-yr interval subsequent to Ar. ramidus at Aramis (White et al. 2006:887-888).

    This points to two salient facts about the Australopithecus lineage: they were able to disperse effectively across relatively long distances, and occupy at least those habitats where wooded cover and resources were available.

    On the other hand, the fossils don't really "fill a gap" between Ardipithecus and Australopithecus, because they are pretty firmly within the time range of known Au. anamensis, being around the same age as the Au. anamensis sample from the Lake Turkana area -- the oldest Kanapoi hominids may be between 4.1 and 4.2 million years old also. The paper points out the other East African examples of Australopithecus at or above 4 million years ago; but it omits the Sterkfontein Member 2 remains, which are also conceivably in the age range of Au. anamensis. Or, for that matter, the Lothagam mandible, which might be the earliest australopithecine even if its date weren't as high as the >5 Ma estimate.

    The paper attempts to close off -- for the moment -- the idea that there were allopatric species of early (ca. 4 Ma) australopithecines with differing dietary adaptations. But the paper cannot reject this hypothesis without caveats:

    Two phylogenetic hypotheses concerning the origin of Australopithecus can be offered to account for the available data. The first hypothesis derives Au. anamensis phyletically from Ar. ramidus within a 200,000-yr interval [i.e., between 4.4 and 4.2 Ma]. The second involves cladogenesis of Au. anamensis from an ancestor (presumably Ardipithecus or some close relative) even deeper in the Pliocene or Late Miocene. Under the latter hypothesis, Ar. ramidus would represent a relict species in an ecological refugium (White et al. 2006:888).

    This latter alternative is the only "bushy" interpretation -- the idea that known species of Ardipithecus can't really be the direct ancestors of Australopithecus, but that there must be some as-yet-undiscovered hominid (or better yet, hominids) that are the common ancestors, cousins, and other bushy relatives of the known species. White and colleagues cannot reject it, but they clearly do not favor it.

    In its place, they suggest Ardipithecus ramidus as a lineal, possibly anagenetic ancestor of Au. anamensis, and Au. anamensis as the anagenetic ancestor of Au. afarensis. It's a ladder from primitive to derived, small-molared to big-molared, big-canined to small-canined.

    I tend to think this is the null hypothesis -- we have sampled adaptations that differ because of evolution in what is essentially a single lineage of successive species. I say "essentially" because there was not necessarily a wholesale transformation of one species to another across its entire range. Instead, dispersals of new adaptive packages by population movements were probably important biogeographic aspects of evolution in these early hominids. But I think it important to recognize that one species can indeed be the ancestor of a later species.

    People who like their phylogenies bushy and their speciations punctuated can take solace in that 200,000-year gap. The finding of Au. anamensis within the already-known time range of Au. anamensis means that the new fossils haven't really added much to the question of phylogenetic diversity in early hominids.

    As a postscript, I have a nomination for "most significant sentence" in the paper:

    At Aramis, the lone hominoid and largest primate was Ar. ramidus (109 of 6,156 identified specimens so far) (White et al. 2006:888, emphasis added).

    References:

    White TD and 21 others. 2006. Asa Issie, Aramis and the origin of Australopithecus. Nature 440:883-889. DOI link

    Tags: 
    Sterkfontein
    A. afarensis
    A. anamensis
    Ardipithecus
    Miocene
    A. africanus
    Pliocene

  • Flores update, October 2005

    Tue, 2005-10-11 23:20 -- John Hawks

    This week's Nature is carrying a paper by Morwood, Brown, and colleagues (2005) presenting additional skeletal material from Liang Bua as well as a commentary by Daniel Lieberman. Thanks to a reader, I found the permission slip from Nature lifting the embargo, so I can let fly without bogarting the kind journalist who forwarded me the paper.

    What is noteworthy about the new bones?

    The paper discusses three important specimens. The first is the adult mandible LB6/1. In its overall size and morphology it is similar to the mandible of LB1, reported last year. Like LB1 it lacks a chin and Morwood et al. (2005:1013) compare its symphyseal morphology to Dmanisi D211. Overall, the mandible is slightly smaller in tooth size and corpus size compared to LB1, and its ramus is quite a bit shorter.

    LB6/1 is part of a partial skeleton. The other elements are not described in the paper, but they are listed: a portion of proximal ulna, a partial right scapula, a foot bone, one each of finger and toe bones, and a complete radius 157mm long. That's a short radius -- barely more than 6 inches. It was broken during life and healed.

    Wait a minute. Did you say a 6-inch long radius?

    Funny how nobody else seems to have picked up on this yet.

    The authors estimate a brachial index (radius to humerus) for LB1 of 78 percent, estimating likely radius length from the ulna. This would put LB1 within the range of "tropical" human populations. If the LB6 individual had the same "tropical" brachial index, its humerus would be around 200mm long. That's 43mm shorter than LB1.

    This admits a couple of explanations:

    1. LB6 was simply a smaller individual than LB1. The mandible is more or less consistent with this hypothesis, which may therefore be the most likely.
    2. LB6 did not have the unusually long arms of LB1. Where LB1 is australopithecine-like, perhaps LB6 was more humanlike. This seems less likely, but it would be consistent with the idea that the proportions of LB1 represent some kind of pathology.

    Wait a minute. Did you say australopithecine-like proportions?

    Yes, the LB1 humerus and ulna are relatively long compared to the femur:

    For example, the humerofemoral index of 85.4 is outside the range of variation for H. sapiens, but is the same as AL 288-1 A. afarensis, and midway between the indices for apes and humans. The more complete left ilium [pelvic bone] also indicates that the pelvis is flared antero-laterally, consistent with an australopithecine-shaped thoracic region. Body proportions of LB1 are the same as AL 288-1 A. afarensis, but differ from all other hominins for which they are reliable data, including H. erectus (Morwood et al. 2005:1016).

    "Outside the range of H. sapiens" is also outside the range of any Pleistocene human, by the way.

    Didn't you say this was an australopithecine when it came out a year ago?

    Well, yes. My first post on the subject was titled, "Liang Bua: an australopithecine from Flores?" And I did present a rationale for believing that the skeleton was australopithecine rather than Homo. My point initially was that the combination of small body size and relatively small brain size was very simple to imagine as a descendant of an australopithecine, but very difficult to imagine in a descendant of Pleistocene Homo.

    Some other features of the skeleton resemble Australopithecus. None of them individually is sufficient to label the skeleton as australopithecine, but together they are suggestive. For example, the pelvis is broad, with a very prominent anterior superior iliac spine. It's very similar to australopithecines like AL 288-1 (Lucy) or Sts 14.

    But we don't know to what extent the breadth and morphology of australopithecine pelves are consequences of their phylogeny as opposed to allometric consequences of their small body sizes. In other words, LB1 might look australopithecine-like because it is small, instead of actually being an australopithecine.

    The postcanine teeth are relatively large for a human, but they are far from australopithecine-like in size. Aside from their size, the first molars are the largest; just the opposite of the australopithecine condition. The roots of the premolars are completely uninformative, since both australopithecines and early Homo have the bifurcated roots found in both Liang Bua mandibles. So if this was an australopithecine-derived population, it had evolved considerably smaller teeth. Happily, this evolution of smaller teeth might also account for the gracile, Homo-like facial morphology.

    OK, so it's an australopithecine, right?

    Maybe. It would not only have to be an australopithecine; it might have to be a DWARF AUSTRALOPITHECINE.

    Consider that the femur length of LB1 is just a millimeter shorter than Lucy and its body proportions are basically the same. Lucy (AL 288-1) is not only the most complete known australopithecine skeleton (barring STW 573, which is yet to be described), it has the smallest limbs. There are some individual bone fragments with smaller dimensions than Lucy's, but not very much smaller. At the same time, there are many larger specimens. Some of these, like the Sibilot radius KNM-ER 20419, are a whole lot larger.

    Now at Liang Bua, LB1 is nearly the biggest specimen. Brown et al. (2004) do report another radius from an older part of the deposit with an estimated length of 210mm. Again assuming the same brachial index, this would correspond to a humerus of 269mm, around an inch longer than LB1.

    But the other two adult long bones reported are the LB6 radius (157mm) and the LB8 tibia. At an estimated 216mm, this tibia is substantially shorter than the 235mm LB1 tibia. There is no comparably complete australopithecine femur, but if Lucy (missing around a third of the shaft) was around the same length as LB1, then LB8 would be shorter than any australopithecine.

    Even worse, it is shorter than all but one of 47 chimpanzee tibiae in my comparative data. That's really short.

    So as it stands, it appears that the Liang Bua sample is substantially shorter than australopithecines. At the same time, remember that the brain size of LB1 (estimated by Falk et al. 2005 as 417 ml) is smaller than all but three australopithecines (KNM-WT 17000, AL 162-28, and AL 333-105). Together with the facial and tooth reduction, this is good evidence for selection for smaller size in an australopithecine-like population.

    OK, so that rules out any chance that it is a dwarf modern human population, right?

    Probably. This would have to be an exceptionally short sample of an exceptionally short population. But then it partly depends on how accurate the stature regressions are. As you get to the bottom of the size range of skeletons from which a regression is calculated, you get less accurate body size estimates. And the proportions affect the estimates. These deserve to be gone over carefully.

    And there is no reason in principle why a modern human population could not have been smaller than any pygmy populations of today.

    There are two stumbling blocks to the hypothesis that this sample represents a dwarf modern human population. The first is the fact that neither mandible looks modern. It is very hard to argue that the features of these mandibles are the consequence of small body size alone; they genuinely appear archaic.

    The second is the size of the brain.

    Speaking of the brain, is it small enough to rule out descent from early Homo?

    That's a very good question. Large-bodied early Homo appears to have an average endocranial volume around 800 ml. A reduction in body size to LB1 should not have cut the endocranial volume in half -- we would expect a volume closer to 600 ml. In fact, an average of around 600 ml is just about what we observe for small-bodied early Homo, including H. habilis in Africa, and possibly including the Dmanisi sample of early Homo from the Republic of Georgia.

    To get from a habiline-sized hominid to LB1 body size would take relatively little size reduction. This means that the brain size of LB1 would be very surprisingly small for a habiline of its body size (particularly since many habilines are its size, yet have much larger brains).

    So to go from any variety of early Homo to LB1 in brain size would require pretty substantial selection for smaller brains. It is hard for me to see that happening in a hominid population, because it would likely lead to functional compromise of some kind. In particular, if most of the selection for larger brains in hominids has been to promote social intelligence, it is hard to see how selection for smaller brains would happen.

    On the other hand, who knows? There is, after all, the endocast shape, which is Homo-like (Falk et al. 2005). And the facial morphology. And the teeth.

    In the face of all this, Morwood et al. (2005) appear to be persuaded most strongly by the limb proportions. Maybe an australopithecine-like limb ratio is a good phylogenetic indicator, but considering the recent spat over early hominid limb proportions in Current Anthropology, this might not be the best hook to hang your hat on.

    Didn't you say six months ago that LB1 is pathological? Well, what do you say now, smarty-pants?

    I still think it's pathological. We have so far seen a few of the details that point to that conclusion. For example, there's the low torsion of the humerus. "Torsion" refers to the angle between the axis of the head and the axis of the distal end of the bone. The humerus of LB1 is unlike any hominid. It's unlike any great ape. It's like monkeys and gibbons. That's weird. Then there is the bowed tibia, and the rotated premolars, all clearly in the reports so far.

    We will see if these and other features can be combined into a single diagnosis of pathology, one that possibly includes the small size of the brain or details of its endocast morphology. For myself, I think there is sufficient evidence to question whether LB1 is characteristic of its population.

    Now we have additional evidence of body size in the population, including the two very short elements described above. Is that enough to believe that the brain is characteristic of the population? If there has ever been a case to invoke the "extraordinary claims require extraordinary evidence" clause, it is this one. LB1 is not only small-brained for a human, it is small-brained for any hominid.

    So I don't think that pathology is a magic wand that is going to make this population into ordinary modern humans. But I'm not ready to jump to the conclusion that this was a population of hominids with australopithecine-sized brains. There is, after all, the problem of how they got to that island in the first place.

    Speaking of getting to the island, what about their technology?

    I think the tools are a complete red herring. There is every reason to think that modern humans were on Flores throughout the Liang Bua sequence. After all, modern people were on Australia by 50,000 years ago, and out to New Britain by 35,000. Maybe they bypassed Flores on the way, but it seems more likely that it would have been occupied long before these more far-flung locations.

    Therefore, it is simplest to assume that modern humans made the tools and hunted the stegodon. Maybe they hunted the hobbits. Maybe some of the bones at the site are modern humans. Maybe some of them were dwarf modern humans.

    Seems all tangled up, doesn't it? Yet the behavior speaks to the presence of Homo, and from the character of the tools, modern human seems likely. If those modern humans weren't the hobbits, then they lived alongside the hobbits.

    So what's next?

    We should see before long at least two (and possibly more) papers that dispute the Homo floresiensis interpretation. Carl Zimmer reports at his weblog that one of these will come from Robert Martin:

    "Regardless of one's stand on this issue," Dr. Martin wrote to me in an email, "it is about time that the message got out that there are serious grounds for doubt about current interpretation of the Flores remains."

    I think that's right. Of course Martin's interest is allometry of the brain, which made the initial interpretation -- island dwarfing of an early Homo variant -- seem very unlikely from the start. An australopithecine origin is less problematic from the point of view of allometry, but introduces the problems of biogeography -- how did they get there, and why weren't they anywhere else? Pathology would help a lot to explain that brain....

    The pathology work will be the most interesting; I know there are many people working very hard to find a single pathology explanation that is consistent with the anatomy of LB1. If they have succeeded (and we should find out before long) it will be a major accomplishment.

    And there will be comparative anatomical and possibly genetic work on pygmy people in the region. Remember the Rampasasa Pygmy Somatology Expedition? It will be coming to a journal near you.

    The stealth factor is whether Max Planck (or anybody else) has gotten any DNA out of the bones. Wouldn't it be interesting if part of the mtDNA sequence looked like one of the more ancient human-specific nuclear genome mtDNA inserts (numts)? If this is an australopithecine population, mtDNA would be enough to show it.

    More information here

    All the Flores files

    Original discovery

    Endocast study

    The damage to the specimens

    Myth of the ebu gogo

    References:

    Brown P, Sutikna T, Morwood MJ, Soejono RP, Jatmiko, Saptomo EW, Due RA. 2004. A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 431:1055-1061.

    Falk D, Hildebolt C, Smith K, Morwood MJ, Sutikna T, Brown P, Jatmiko, Saptomo EW, Brunsden B, Prior F. 2005. The brain of LB1, Homo floresiensis. Science 308:242-245. Full text (subscription)

    Morwood MJ, Brown P, Jatmiko, Sutikna T, Saptomo EW, Westaway KE, Due RA, Roberts RG, Maeda T, Wasisto S, Djubiantono T. 2005. Further evidence for small-bodied hominins from the Late Pleistocene of Flores, Indonesia. Nature 437:1012-1017.

    Tags: 
    Late Pleistocene
    Homo erectus
    Flores
    Dmanisi
    Homo habilis
    A. afarensis

  • News trickling about Liang Bua

    Tue, 2005-10-11 10:43 -- John Hawks

    I am seeing news reports this morning about this week's upcoming paper in Nature about the Homo floresiensis bones.

    The paper is supposed to be under embargo until tomorrow afternoon; Nature is reporting on it early under its pay-per-news site; Reuters has a short article, and New Scientist has a longer one (Google says subscription-only, but once again I got it without a subscription).

    Here's my favorite quote from Reuters:

    The newly found remains, dug up in 2004, consist of a jaw, as well as arm and other bones which the researchers believe were from at least nine individuals.

    That's right, we're going back ... TO THE FUTURE! Here it's not even so bad -- I mean, these bones were found just last year. Just wait until they have to report on future past discoveries.

    I'm keeping the embargo, so you can expect to see my review of the papers tomorrow afternoon. Yes, that's right -- this humble blog is keeping its word while MSM giants break theirs. Anyway, come back tomorrow for the real story.

    In the meantime, enjoy this quote from New Scientist:

    And in the light of the new finds, Morwood's team is itself moving away from the dwarfing theory. The hobbits have disproportionately long arms relative to their legs, and so cannot be scaled-down versions either of modern humans or Homo erectus, who have had the same body proportions for 1.6 million years.

    Ancestral line

    They say that a more likely ancestral line goes back to australopithecine species such as 3-million-year-old "Lucy", found in Ethiopia (Australopithecus afarensis).

    "The combination of skeletal attributes that [the hobbits] share is not found in any modern human," says team member Peter Brown. "The bones of the hands and feet don't look like those of arboreal apes, but like everything else to do with Homo floresiensis, they are not like humans either."

    I'm certainly enjoying it.

    Tags: 
    paleonews
    A. afarensis
    Homo erectus
    Flores

  • Tuber or not tuber? Rats are the question

    Wed, 2005-08-24 17:08 -- John Hawks

    From a new paper by Greg Laden and Richard Wrangham:

    We propose that a key change in the evolution of hominids from the last common ancestor shared with chimpanzees was the substitution of plant underground storage organs (USOs) for herbaceous vegetation as fallback foods. Four kinds of evidence support this hypothesis: (1) dental and masticatory adaptations of hominids in comparison with the African apes; (2) changes in australopith dentition in the fossil record; (3) paleoecological evidence for the expansion of USO-rich habitats in the late Miocene; and (4) the co-occurrence of hominid fossils with root-eating rodents. We suggest that some of the patterning in the early hominid fossil record, such as the existence of gracile and robust australopiths, may be understood in reference to this adaptive shift in the use of fallback foods. Our hypothesis implicates fallback foods as a critical limiting factor with far-reaching evolutionary effects. This complements the more common focus on adaptations to preferred foods, such as fruit and meat, in hominid evolution.

    Tubers are not the only kinds of USOs; there are also corms, bulbs, and rhizomes. I tend to use "tuber" as an easier-to-type version of USO, though. I was practically dared to review the paper here (nota bene: I do respond to dares, albeit more carefully and slowly than for most things), and Carl Zimmer has also written a short item on the idea. The mole rats are the lede, but there is much more to it than them, and in many respects they are the least problematic part.

    So here is my semi-rambling take.

    Take one

    In 1999, Wrangham and Laden, along with David Pilbeam, James Holland Jones, and NancyLou Conklin Brittain, suggested that tuber cooking was central to the adaptation of early Homo. The evidence for that suggestion was and remains essentially absent. As Henry Bunn put it in his comment to the paper:

    Why is there abundant evidence of hunting and some form of scavenging, carcass transport, butchery, and sharing and consumption of meat and fat in the behavioral and dietary adaptations of early Pleistocene Homo (e.g., Oliver, Sikes, and Stewart 1994 and references therin)? Why are the earliest stone tool kits of the Oldowan dominated by sharp-edged cutting tools? Why is there intensive meat polish on the edges of stone flake knives studied for microwear (Keeley and Toth 1981)? Why is there not microwear evidence of grit or sediment damaged on the teeth of supposedly tuber-feeding hominids themselves, including the robust australopithecines (Kay and Grine 1988)? (Bunn 1999:580)

    Additionally there is the problem of the complete lack of evidence for cooking and the weakness of evidence for early control of fire, compared to the strong and substantial evidence for both much later in the Pleistocene.

    So early Homo just doesn't show any signs of having been a serious tuber-eater. Not to say it is impossible; just that there isn't any particular evidence for the idea.

    Take two

    Now, Australopithecus, that's another story. Robust australopithecine teeth in particular have a lot of pits and scratches on them, as if they were eating some hard, gritty foods. Underground storage organs fit that bill. Eating a lot of dirt along with them might well explain the high rate of dental wear that robust australopithecines clearly had -- many had their first molars worn almost completely flat before the third molars came into occlusion.

    In this context the fallback food idea seems like an especially good one. The tooth anatomy and microwear evidence indicate that robust and nonrobust australopithecines probably did not differ in most of their dietary spectra, but instead in the accentuation of different food sources that were shared by both. If food shortages were important in the evolution of these hominids, one way that the difference between them might have been sustained was an ecological difference in fallback food utilization. Hominids like A. afarensis and A. africanus undeniably had teeth adapted to heavy grinding, fracturing off brittle foods, and intensive attrition compared to any other living or fossil primate. So it makes no sense to propose that the difference between these "gracile" australopithecines and later robust australopithecines was that the "gracile" ones lacked the high-chewing element. Rather, it makes considerably more sense to suppose that both kinds of hominids were eating the high-chewing foods, with the robust ones making a more intensive use of them, and possibly lacking some of the tough pliable foods eaten by earlier nonrobust species. A difference in fallback strategies might comprise exactly this kind of dietary prediction.

    To me, the coolest thing about the hypothesis is that it explains the postcanine adaptations of australopithecines without reference to the now-well-known carbon isotope data. Indeed, the question of C4 versus C3 foods is entirely irrelevant. I discussed the carbon and other stable isotope data in an earlier post; the short story is that all kinds of australopithecines appear to have included around a 25 to 30 percent component of C4 foods, which include grasses, some sedges, and the animals who ate them.

    Peters and Vogel (2005) proposed that the C4 component of the early hominid diet could be explained as a sum of several different plant and animal sources, including around 5 percent each of seeds, roots and pith, insects, small mammals and vertebrates, and large mammal meat. That does a good job of describing a diversified hominid diet without reference to tubers.

    But the thing about USOs is that relatively few of them are C4 plants. If hominids did eat tubers, in other words, they still wouldn't account for the C4 fraction of the overall diet.

    However, they might account for the postcanine dental adaptations of later hominids, under the assumption that they represent a substantial part of the C3 fraction. And the replacement of C3 fruits by C3 tubers would explain why robust and nonrobust hominids both have approximately the same C4 fraction, while differing so greatly in their dental adaptations and dental microwear.

    As far as I can tell, nobody has mentioned this implication, but it should be the next thing to test.

    The evidence

    But although I think Laden and Wrangham's study has some interesting possibilities, I think the data is a bit short of where it needs to be. What about the four lines of evidence used by Laden and Wrangham? Are they to be believed?

    The first thing to point out is that a reading of the paper finds little detail to go along with two of the lines of evidence. It is true that australopithecine teeth are not like ape teeth, and that robust australopithecines were different from nonrobust ones. The innovative suggestion here, although brief, is that an enlarged oral cavity in australopithecines, particularly robust ones, may be an adaptation to increase the exposure of masticated tuber to salivary digestion.

    But the dental discussion appears less as two independent lines of evidence converging to one conclusion, and more as throwing up whatever seems relevant to see what will stick. A review of early hominid dental evidence also reveals plenty that is less consistent with the hypothesis that USOs were an important food for most early hominids.

    For one, the comparative dental evidence is questionable. As Laden and Wrangham review the issue, Hatley and Kappelman originated the argument that the early hominid dentition was adapted to tuber-eating:

    In 1980, Hatley and Kappelman pointed out parallels in dental morphology that suggested that bears, pigs, and hominids are all adapted to eating significant amounts of plant underground storage organs (USOs). They summarized their argument as follows: "We believe that postcanine similarities evident among ursids, suids, and hominids are in part an adaptation for processing this tough, fibrous, and gritty plant part. Bears, pigs, and humans are adapted to exploiting plant roots and tubers, although their methods of food gathering are functionally rather than morphologically analogous. Convergence upon the resource of belowground plant storage parts appears to make the responses of nonretractable claws, cartilaginous snout, and digging stick equivalent" (Hatley and Kappelman 1980:380, quoted in Laden and Wrangham 2005:1).

    This isn't obviously true. For one thing, Pliocene pigs appear to have been mainly grazers (Harris and Cerling 2002 -- not cited by Laden and Wrangham 2005). They increased in molar size and complexity in several different lineages, as a reflection of their increased reliance on C4 vegetation. The diet of current-day suids in particular seems to share little in common with early hominids, at least as far as their stable isotope ratios are concerned. Nor are large and flat early hominid molars particularly analogous to those of most bears -- perhaps the closest are pandas, which are far from dedicated tuber-eaters.

    Then there is the problem with the earliest hominids. These, like the later ones, are found alongside mole rats, at sites like Aramis and Lukeino. But they don't have the postcanine adaptations of later hominids. The essential problem with the earliest hominids is not postcanine specialization, but instead the changing role of the canine-premolar complex, and the reduction of the canines. There is no reason (at least that I can think of) to suppose that small canines are adaptive to tuber-eating (and a search of the paper finds no occurrences of the word "canine").

    One way to avoid this problem is to suppose that the USO-eating adaptation was simply a feature of later hominids --- say, A. anamensis and later. Perhaps it's true, but if so, the hypothesis loses some of its punch, and possibly one of the converging lines of evidence, since the expansion of USO-rich savanna central to Laden and Wrangham's paper starts in the Miocene.

    And the paper would prefer to displace the importance of tubers earlier rather than later in time:

    There is growing evidence that middle to late Miocene hominoids, mainly in Europe, exploited relatively open habitats, and may have exhibited dietary adaptations (Teaford and Ungar, 2000, Smith et al., 2003 and Smith et al., 2004) that we claim here to be related to USO consumption. This lends support to our assertions that a USO niche may have emerged during the Miocene, that this niche may have been important for non-fossorial mammals, and that certain features, such as thick enamel and large teeth, can arise in response to this niche. However, we do not wish to make claims beyond the hominid taxon at this time, other than to note that this may be a fertile area of future research (Laden and Wrangham 2005:13).

    If you are a student looking for a thesis topic, don't pick this one.

    The most original suggestion is that hominid and mole rat remains are significantly coassociated. On the surface, this looks like fairly convincing evidence that the hominids lived in USO-rich environments, which is precisely what Laden and Wrangham conclude. And indeed, the number of sites either possessing both kinds of animals or lacking both (27) is higher than expected considering the small number that have one kind but lack the other (11).

    But wait a minute. Neither "mole rats" nor "hominids" are species, they are groups composed of several species. Let's consider the same kind of comparison for other kinds of animals. How many hominid sites lack bovids? Or suids? Or crocodilians? Keep in mind that some groups are rare at early hominid sites because they hadn't diversified yet, like papionins, or hadn't yet appeared in Africa, like equids. But these groups are found at many later hominid sites. And of course, for many sites the total species list may reflect less intensity of sampling rather than the paleohabitat.

    In other words, the mole rats may show that hominids had the opportunity to eat USOs -- at least, if they could compete effectively with the mole rats for them. But they don't show that the hominids actually ate USOs. At least not if we aren't equally willing to believe that the presence of crocodiles at hominid sites meant that hominids swam in rivers and ate migrating wildebeest.

    The weaknesses NOT mentioned

    I see two significant weaknesses in the hypothesis. The first is the simpler of the two: digging up tubers is a lot of work.

    For groups like the Hadza who eat a lot of them, this work takes many hours (at least by some group members). That kind of work seems unlikely for australopithecines, even hungry ones. Especially considering the full scenario: australopithecines digging intensively for savanna-living tubers for hours at a stretch would have been highly exposed to predation and heat stress for hours at a stretch.

    Might they have done it if they had nothing else to eat? Sure. But could they have done so efficiently enough to get a net return on their effort? There's a question worth answering.

    Might they have banded together into large defensive groups? Maybe, but that would seem likely to decrease foraging efficiency -- how many tubers are there in any small patch of ground? However, there is slight evidence for large multimale groups (chiefly AL 333), as well as pretty good evidence that predation was high and survivorship into adulthood low. Another question worth answering.

    There may be a solution for this problem: perhaps the plants themselves have evolved under intensive hominid predation. Maybe today they put their roots further underground, or maybe the plants with tougher and more fibrous roots have predominated since the Pliocene. If so, australopithecines might have had an easier time of digging them up.

    The other problem is more vexing. How can we demonstrate that an extinct species was adapted to eat a food that it did not eat very often? Bone chemistry must predominantly reflect the foods that make up the majority of the diet, not those that are consumed only intermittently. Microwear also ought to reflect the majority foodstuffs, although perhaps more weakly -- especially if mortality occurs mostly during periods of dietary stress, when animals are eating more of their fallback foods than usual. This is perhaps worth looking into.

    Maybe the most promising test would be variability in tooth wear. Presumably the need to rely on fallback foods would vary in accordance with climatic conditions, on a multigenerational timescale. If so, then some individuals might exhibit relatively great amounts of attrition due to their reliance on fallback foods during long periods of resource stress, while other individuals might have lived in times of relative abundance, and therefore not have experienced significant amounts of wear. This kind of heterogeneity would itself have created differences in selection on tooth size, enamel thickness, and occlusal anatomy over time: perhaps in ways that could be differentiated from alternative strategies. But even so, that kind of comparison is relatively far from the direct evidence, and may be impossible with the fossil record we have available.

    Summary

    Looking back at the post, I've written a balance of critical comments and supportive ones. I guess my opinion overall is that the USO hypothesis is certainly worth presenting, but it has a ways to go before it is really testable. I think there is a balance of good ideas here and evidentiary weaknesses, and it is certainly worth talking about them, perhaps with a bit more skepticism and documentation than has yet been done.

    And if you are serious about tubers, as Wrangham clearly has shown himself to be, then you are going to have to choose a time when they were important. With this paper, I have now read that tubers were the key adaptation for Miocene apes, the earliest hominids, australopithecines, robust australopithecines, early Homo, and recent humans.

    It can't be all of these. If it were, they would all look the same. And there wouldn't have been any reason for one to change into anything else! So you have to pick.

    And making a choice means more than saying, "well, Miocene apes tasted tubers, early hominids needed them when the fruit ran out, for australopithecines they were a fallback food, robust australopithecines ate them all the time, early Homo cooked them, and recent humans pickled them with vinegar and caraway seeds. As yet, the many tuber hypotheses have been just-so-storytelling at its most self-contradictory.

    If I were picking, I would put the best odds on Laden and Wrangham's current argument: USOs were important fallback foods for nonrobust australopithecines like A. afarensis and A. africanus, and equally or more important for robust australopithecines. In contrast, early Homo was adapted to meat eating, and the earliest hominids -- who lack the postcanine specializations of later hominids -- remain as yet a mystery, although a fundamentally apelike diet is a good first guess.

    This post doesn't account for all the details of early hominid diets, but some previous posts review other sources of evidence, including:

    Stable isotope analyses

    Dental microwear

    Occlusal anatomy

    References:

    Hatley T, Kappelman J. 1980. Bears, pigs, and Plio-Pleistocene hominids: a case for the exploitation of belowground food resources. Hum Ecol 8:371Ð387.

    Laden G and Wrangham R. 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J Hum Evol in press (online)

    Wrangham RW, Jones JH, Laden G, Pilbeam D, Conklin-Brittain N. 1999. The raw and the stolen: cooking and the ecology of human origins. Curr Anthropol 40:567-594.

    Tags: 
    Miocene
    diet
    A. anamensis
    Pliocene
    A. afarensis
    Early Pleistocene
    A. africanus

  • Ape to Man

    Sun, 2005-08-07 22:18 -- John Hawks

    OK, we have it on, and I've already had a couple of laughs, so I guess I'll take some notes as it goes.

    8:10 They didn't really just say that did they? Oh yes they did: Neandertals had big noses because they had a good sense of smell. Arrrggh!

    Evidence: against. Human smell receptors have been evolving to inactivity for far longer than our common ancestor with Neandertals; there's no compelling reason to think their sense of smell was different from our own.

    8:12 I'm not sure I would call Fuhlrott a "Victorian naturalist"; he was, after all, a German living in Germany.

    8:20 On to Dubois on Sumatra. Is it just me, or does he look like Mr. Bean wandering around the forest? He even talks like Mr. Bean (that is to say, his Dutch sounds remarkably like Mr. Bean's mumbling).

    8:24 By this time, this seems to me to have a remarkably low information density. There are many silent moments lacking voiceover. Is it really that dramatic to watch Dubois open a crate? I'll grant that the Dutch argument had some drama, but what does it really accomplish other than to show Dubois was a jerk? They don't really explain allometry, which was Dubois' major innovation. Of course, that's usually left out of the story anyway.

    8:26 OK, here's an actor dressed up like Homo erectus. Do they really have to pay new people to do this every time? Or does the BBC use old footage from the last time they dressed somebody up like Homo erectus? It's not like they're different or anything.

    And why should Homo erectus be hairier than us? Or at least than people living in Java today? If it's true that they were sweating, which seems likely, then they shouldn't be sporting all that fuzz.

    8:44 Piltdown. Now this is possibly my biggest complaint. I understand that this is a show about the history of the field, rather than about what we actually know. But it seems like such a waste.

    They're setting it up to look like Dawson is the culprit, by the way.

    8:51 Of course the entire point of the Piltdown story is to make Dart look like a hero. As perhaps he should, but I wonder if the story is really so simple. There were plenty of Piltdown doubters, and plenty of Australopithecus believers. We don't hear their story very often.

    And this telling is a very British-centric story, having to do with Arthur Keith's influence on the British scientific establishment (although Keith features in the program only in a minor way). The story in Germany is very different, and America presents a blend of the two.

    9:02 Ape-woman sniffing at rubber carcass is not engaging me.

    9:09 Twenty-five years after Piltdown was found, it was "examined scientifically for the first time." What, anthropology isn't scientific? You have to burn something in chemicals to be science? Sheeesh!

    And it doesn't really reflect the history. Piltdown was proved a hoax after more australopithecines emerged in South Africa. The anthropology led here, not the chemistry. I wonder what happened to Robert Broom, by the way, who entered the story to console young Dart, but didn't get to make his pre-Leakey discoveries....

    9:16 Nice choice of actor for Louis Leakey.

    9:21 "Leakey decides that this was the toolmaker." Only problem: the cast they are showing with the voiceover is KNM-ER 1813, from a different site, a different country, and found fifteen years later. Can we not understand fragments? Or did they just have trouble finding a cast? Their cast of OH 5 is comical, so I guess it's probably the latter.

    I wonder if Tobias is ticked about this, since he described both.

    9:24 Colin Menter is drawing a phylogeny in the sand. Or...is he starting an episode of "Lonely Planet"?

    9:30 Nice choice of actor for Johanson.

    Is there supposed to be some suspense about these reenactments? We know they found something, otherwise it wouldn't be in the program. So why is their long, long, long, period of not finding anything in the program? Are we supposed to learn from this? Because I am afraid that what viewers may be learning is that paleoanthropology is bo-ring.

    9:38 Bipedal locomotion. Once again, wondering what happened to Broom. Did we know that australopithecines were bipedal before Lucy? Hmmm...I'm thinking Broom would know. If only we could see Broom and his discoveries...then we would know all....

    9:40 Traveling back in time through a long, long, long line of ape-people, single file, over hills into the past. Wouldn't that be a ladder, not a bush?

    Hey, there has been no mention of bushes in this show at all! My opinion is going up!

    9:45 Neandertals again, back "on the scent of red deer." But we saw them rub red deer scat all over themselves. How exactly did they follow the scent, then?

    9:47 Wow. Krings worked for CSI!

    The thing is, I'm sure most viewers probably believe that genetics labs have this moody coroner lighting (I think it may actually be from a BBC crime drama, can't remember the name). And that the Feldhofer fossils were kept in some kind of cold metal lockup with clanging steel bars (they actually do have a lockup now, but I don't recall the bars and clangs).

    Oh, oh...this is looking suspiciously like a bush coming up...

    The first meetup between Neandertals and modern humans "was a profound shock". As in, "Whoa, man, what's that plasticine junk on your face"? And why is it that no "modern human" in these shows ever has a superciliary arch? Did they screen out all the tough-looking actors?

    9:55 Modern humans "supplemented their diets with fish, spurring their brain development."

    Evidence: against. Neandertals had equally large brains. And there's no special reason to think Neandertals didn't eat as much fish as early modern humans.

    9:57 They hunted down the Neandertal and killed him! I've never seen that before! Poor Neandertal. I can remember him now: "I'm just a caveman. Your modern world frightens and confuses me."

    My opinion

    The history is pretty standard. Since this is The History Channel, that's a good thing.

    But it's pretty slow. It really makes the field look duller than it is. And it focuses too much on a few discoveries and not enough on how the context of science changed.

    I wouldn't show it in class. It's too long, for one thing. And it would put everybody to sleep.

    But more important, it doesn't present any alternative views. The best in-class use of video is to show opposing scientists in their own words. The scientists here are good ones, and their film clips don't present any controversial ideas, but there are just not enough of them to give the flavor of the field.

    And they would need more historians of the field to give a flavor of the history. You want the Piltdown episode in? Tell the whole story, including the early detractors and the whodunnit theories. Want Johanson to make A. afarensis the common ancestor of Homo habilis and Australopithecus? Then you'd better cover his debate with Richard Leakey.

    I don't have a good feel for how much more they could have added, but they certainly could have knocked out much of the reenactment, which featured a lot of fluffy voiceover, or even silence. I think a Ken Burns-like approach could pack in a lot more information; with interviews and voiceover going over video and pictures, and actors reading some original passages from the discoverers themselves.

    On second thought, Ken Burns isn't very exciting either, so you'd have to replace the slow photo pans and maudlin music. Maybe opera music?

    Tags: 
    tv
    Neandertals
    Homo erectus
    Homo habilis
    A. afarensis

  • Sexual dimorphism in A. afarensis, again

    Mon, 2005-07-25 15:22 -- John Hawks

    Earlier this year, Michael Plavcan et al. (2005) had a critique in Journal of Human Evolution of the 2004 paper by Philip Reno et al. in PNAS concerning sexual dimorphism in A. afarensis. Now, in the August issue of JHE, Reno and colleagues have a reply. I have previously written about the Plavcan critique and a news report on the issue.

    The reply by Reno et al. (2005) covers the four areas raised by Plavcan et al. (2005) thusly:

    1. Is the AL 333 sample biased? And how many individuals are there? Reno et al. (2005) present new simulations to show that a very small number of individuals at the site would still result in an interpretation of low dimorphism. So a smaller sample size than they originally assumed does not explain their interpretation of low dimorphism (although it does limit the information provided by the data). They further argue that it is likely the non-AL 333 sample that is biased, because it does not represent the number of intermediate-sized (presumptive female) individuals found at AL 333.
    2. How does temporal variation affect the estimate of dimorphism? Plavcan et al. (2005) used a clever illustration to show that temporal variation may have no effect on dimorphism estimates. Reno et al. (2005) respond with another clever illustration showing that temporal variation may affect dimorphism estimates substantially, usually by causing overestimation. This point is essential to their argument that the AL 333 site is more representative of dimorphism than the other, temporally dispersed, localities.
    3. Is skeletal dimorphism well-related to body mass dimorphism? This problem is third on the list generated by Plavcan et al. (2005), but Reno et al. (2005) tackle it first. That may be because they caught the prior authors in an error:

      Plavcan et al. make a fundmental error in their Figure 3. This figure shows body mass dimorphism (BMD) plotted against femoral head dimorphism in apes and humans. They also plotted values for A. afarensis calculated from our template estimates of FHD on this figure. They claim that these values imply marked femoral head dimorphism for A. afarensis. They do not. This figure mistakenly commingles FHD estimates for A. afarensis, i.e., template sexual dimorphism (our TSD) and actual values obtained by direct measurement of specimens with known sex, i.e., direct sexual dimorphism (our DSD) (Reno et al. 2005:280).

      The two are not comparable, so this is an apples-and-oranges comparison. For the rest, Reno et al. (2005) correctly point out that body size dimorphism is not what they are trying to estimate, since skeletal dimorphism is all that fossils present:

      Skeletal dimorphism is only one aspect of size dimorphism. It is not, and can never be, a simple surrogate for dimorphism in body mass. First, these characters have only partial association in hominoids; humans display moderate skeletal dimorphism and low levels of mass dimorphism, but chimpanzees show the opposite relationship (as we discussed, see: Reno et al., 2003). Second, body mass (and therefore body mass dimorphism) is unknowable for fossils. It is therefore impossible to derive a regression with which to estimate it without substantial error, because such regressions must be based on extant species that are likely to be biologically dissimilar to extinct ones. Skeletal dimorphism, however, is dependent only upon skeletal dimensions, which are directly measurable in fossils. Plavcan et al.Õs discussion of scaling and allometry robustly demonstrates the regression problem. That is why we do not use regression. However, we certainly understand why they were able to "corroborate previously reported findings that A. afarensis [body] size dimorphism falls between that of chimpanzees and gorillas." (p. 318). For skeletal dimorphism this range includes virtually all primates (Reno et al. 2005:281).

      This is certainly the safe route, although the claim does raise a critical question, discussed below.

    4. Does body mass dimorphism predict social or behavioral features of primates? Of course, what primatologists usually study is body size dimorphism, and not skeletal dimorphism. So if skeletal dimorphism is what we are limited to studying in fossils, then where is our comparative data? Here, Reno et al. (2005:285) present some theory, focusing on bimaturational patterns:

      There has long been a sub rosa assumption that body mass dimorphism is the primary target of sexual selection. However, body mass is a complex character and incorporates several morphological components (Leigh, 1992), particularly (but not exclusively) both skeletal and muscle mass. Muscle mass and skeletal dimorphism can be differentially regulated during mammalian development (McMahon et al., 2003), and our results suggest that this is likely to be the case in chimpanzees and humans. Thus, sexual selection can independently affect skeletal and muscle growth.

      That's certainly something to chew on, as are the details of chimpanzee and gorilla developmental hypotheses presented later. They conclude that no extant ape or primate provides a valid model for A. afarensis, and therefore it is necessary to construct one.

    At the end, the paper asks an interesting question of A. afarensis:

    If its skeleton was largely modern in structure, is it not also likely that much of this derived physiology and anatomy had evolved by the dawn of the Pliocene in ecogeographically unique and cosmopolitan A. afarensis? (Reno et al. 2005: 286-287, emphasis in original).

    "This derived physiology and anatomy" includes

    ...concealed ovulation and permanently enlarged mammary glands implying female reproductive crypsis, elaborated epigamics in both sexes (implying bi-directional mate choice), minimal semen coagulation, moderate muscularity of the vas deferens, relatively small testes and sperm midpiece, retention of scrotal rather than peritoneal testes, a remarkably rapid loss of olfactory receptors, a loss or failure to develop significant vocal sacs, and hormone profiles potentially paralleling those of some extant monogamous mammals (ibid., 286, citations elided).

    I have only one thing to say. If the "largely modern" skeleton of A. afarensis is enough to infer all this stuff, then why are we talking about Neandertals? Of course, it's because a "largely modern" skeleton isn't enough to infer anything.

    References:

    Plavcan JM, Lockwood CA, Kimbel WH, Lague MR, Harmon EH. 2005. Sexual dimorphism in Australopithecus afarensis revisited: How strong is the case for a human-like pattern of dimorphism? J Hum Evol 48:313-320.

    Reno PL, Meindl RS, McCollom MA, Lovejoy CO. 2005. The case is unchanged and remains robust: Australopithecus afarensis exhibits only moderate skeletal dimorphism. A reply to Plavcan et al. (2005). J Hum Evol 49:279-288.

    Tags: 
    Neandertals
    A. afarensis
    Pliocene

  • The robotic Lucy model

    Thu, 2005-07-21 13:03 -- John Hawks

    The BBC is running this article about a new study that evaluates the bipedality of A. afarensis using robotic design software:

    Now, a team of scientists from around the UK have used computer robotic techniques to work out the most energy efficient gait for afarensis based on Lucy's skeleton and the Laetoli footprint trails.

    They claim to have cleared up the debate by finding that, based on their model, Lucy almost certainly did walk tall.

    There has been a long-standing debate about how human Lucy was
    "Assuming that the early human relative Australopithecus afarensis was the maker of the Laetoli footprint trails, our study suggests that by 3.5 million years ago at least some of our early relatives - despite their small stature - could sustain efficient bipedal walking at absolute speeds within the range shown by modern humans," co-author Weijie Wang, from Dundee University, told the Scotsman newspaper.

    So what we seem to have here is a computer software equivalent of early 1980's science. Perhaps they programmed Owen Lovejoy?

    The paper (abstract) is a little more interesting than the BBC description. It does a kind of optimization modeling to find the speed and style of locomotion with the lowest energy cost. That lowest-cost speed was associated with a human-like gait at around 1 meter per second (m/s). Here is the logic:

    Rather than trying to interpret the behaviour of such species by a combination of analogies to humans in certain anatomical regions with analogies to other apes elsewhere, it seems sensible to adopt a reverse-engineering approach and determine what kind of locomotion a particular set of body proportions were best 'designed' to perform. Since the locomotor system is concerned primarily with the application of external force by the body, simulation techniques drawn from mechanical engineering are a potential means of predicting the significance of differences in proportions for the motion and force characteristics of bipedal locomotion (Sellers et al. 2005: 2).

    The authors relate their gait findings to the preserved Laetoli footprint trails, and find something very interesting. The trails have footprints that are very close together -- especially for the larger, possibly dual G2 trail. This has previously been interpreted as meaning that the walking speed of the larger individual who made this trail was very slow (Alexander 1984; Charteris et al. 1984) -- only around 0.7 - 0.8 m/s. The model in this study predicts a faster speed of around 1 m/s, which would be close to the optimal walking speed estimated for Lucy's proportions.

    They do not address a relevant question, which is whether the larger trail was made by an individual larger than Lucy, who might have had a different optimal walking speed. Indeed, there is a basic assumption of monomorphism. It is partly covered by the fact that living people don't exceed 1.0 m/s for their average walking speed by very much, so the variation between large and small A. afarensis individuals may have been slight. The basic finding seems to be that shorter legs have an optimum gait that involves more, slightly shorter, steps, while longer legs take fewer steps more slowly. This isn't surprising based on a pendular model: shorter pendula have shorter periods, and longer steps with a shorter leg must require more energy-wasting up-and-down motion.

    An important weakness of the model is that it considers costs only due to motion in two dimensions: forward and up-and-down. The wide pelvis of A. afarensis might be expected to exert greater costs in a side-to-side dimension compared to recent humans, and that energy effect is not considered.

    But the bottom line:

    Thus, within the limits of our model, and assuming that Taylor and Rowntree's (1973) data are reliable, the bipedal performance of Australopithecus afarensis, as predicted by our model is not only much closer to that of modern humans than to that of bipedally walking great apes, but at normal walking speeds, shows a clear speed/cost advantage over chimpanzee quadrupedalism. Climbing remains significantly more energetically expensive than terrestrial quadrupedalism for chimpanzees, despite their musculoskeletal adaptations (Pontzer and Wrangham 2004). Pontzer and Wrangham (2004) have shown that the costs of locomotion in chimpanzees are nevertheless dominated by terrestrial walking, because of very high daily travel distances, versus only limited use of climbing. If we make the major (and quite likely incorrect) assumption that the African apes existing at the time of A. afarensis were ecologically, morphologically and physiologically similar to modern common chimpanzees, then our data would tend to support Rodman and McHenry's (1980) argument that the adoption of bipedalism offered energetic advantages to early human ancestors (ibid., 9).

    In any event, it won't quiet doubters:

    However, Professor [Christopher] Stringer believes the controversy will not vanish overnight.

    "There are still some people who argue that, looking at the anatomy of the foot bones of afarensis, that they were unlikely to have made the Laetoli footprints," he told the BBC News website.

    "So it doesn't end the argument because there is still the possibility that there were different creatures around at the time."

    No doubt soon, Kent State will have a droid afarensis army to finally crush this dissent and bring order to the galaxy.

    References:

    Sellers WI, Cain GM, Wang W, and Crompton RH. 2005. Stride lengths, speed and energy costs in walking of Australopithecus afarensis: using evolutionary robotics to predict locomotion of early human ancestors. Roy Soc Interface Online

    Tags: 
    robots
    A. afarensis
    bipedalism

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