Martin versus Falk on microcephaly

Science is carrying an exchange of technical comments about microcephaly and the endocast of LB1. Bob Martin and colleagues weigh in with an argument for why LB1 was a microcephalic. Dean Falk and colleagues respond that the microcephaly explanation can’t account for the endocast’s features. </p>

So what's the real story?

Why isn't it obvious that this specimen was microcephalic?

To some, it is a tautology: a microcephalic has a brain size significantly less than the normal range; this skull had a significantly small brain (near the minimum for Australopithecus!); ergo, this was a microcephalic.

But microcephaly is a rare condition, and it is not a single condition, but a spectrum of conditions. There is a long chain of developmental processes leading to the normal human brain, including genes and necessary nutritional and chemical conditions. A break or interruption in many of these may result in significantly smaller than normal brain size. Many of these cause different anatomical configurations -- brains of different shapes. The endocast of LB1 was broadly normal in shape (at least, compared to early Homo) but very small in size.

What seemed essential was to find a sample of modern human microcephalics that had the shape of LB1. It would be even better to find additional cranial or postcranial features of microcephaly that match the skeleton of LB1.

An earlier comment by Weber and colleagues (discussed in this post) presented a comparison with a sample of microcephalics, which easily matched the LB1 endocast in size, but not in shape. The closest endocasts in shape still presented some differences with LB1 that stand out as divergent compared to normal modern human endocasts and early hominid endocasts.

It's sort of like looking for a match with a tan Toyota Corolla, and they found a tan Honda Civic -- close in shape, but some telling differences.

Now, at this point it seems like an exercise in pattern matching. Folks are going to look through museums at microcephalics until they find one that's closer to LB1.

Did Martin and colleagues find a better microcephalic?

Here's what Martin et al. write:

Microcephalic skulls and endocasts similar to LB1 include the specimens shown in Fig. 2. Doubling of the volume for half-skull B yields a cranial capacity of 432 cc, close to that of LB1. Specimen C has a volume of 340 cc. Both lack obvious pathologies. For example, the cerebellum is tucked under the cerebrum (3).

That gets around one of the criticisms of the close endocast presented by Weber and colleagues (2005). Is it enough?

Falk and colleagues reply that the line drawings provided don't give enough detail to tell whether the "matching" endocasts actually are comparable with LB1.

There are two ways to look at this. Here's an analogy: we've found a tan Toyota Corolla, but it isn't a tan Toyota Corolla with a dent in the trunk.

The importance of the similarity depends on the question we want to answer. If we want to know if the cars were made by the same manufacturer, then we don't care about the dent, or even the color.

If we want to know if our key will fit, then it matters a lot -- and we may need to know even more, like the license plate number.

Falk and colleagues are looking for the license plate number:

Because of brain shrinkage, one would also not expect to obtain a highly convoluted endocast (like LB1's) from such a specimen (5, 6), and we gather from the lack of detail on Martin et al.'s line drawings that neither of their microcephalics reproduced endocasts that are highly convoluted.
...
Although the authors provide a line drawing for LB1's skull, no image is provided for its endocast. A line drawing is provided for an endocast of a microcephalic from the Field Museum, but not for its skull, which, as described (and illustrated in actual photographs) in the reference cited by Martin et al., "is long-headed and narrow, with a lowly vault, the face narrow, with apelike protrusion of the jaws" (8). This skull differs starkly from LB1's, which is extremely brachycephalic (2, 9).

It would be helpful if we knew in advance which features were important ones for the comparison. The size is not enough, but is the shape? Or the shape and the convolutions? Or Brodmann's area 10? It seems a bit much to suppose that a skull has to share every feature of LB1 to count as the same developmental problem. We don't demand that of any other kind of diagnosis in living people. But we do demand that a key set of symptoms be present for a diagnosis, and in this case we don't have any guidance about which are the important features.

Yuck.

What is all this about Jakob Moegele?

Martin and colleagues went into museum records to figure out the identity of the microcephalic included in the study by Falk et al. (2005a). This research showed that endocast was probably not very comparable to LB1 -- the skull belonged to a 10-year-old boy, it was a bad cast, it was a very small endocast even compared to LB1, etc.

Falk and colleagues reply that it might not matter so much that the boy was only 10 because the brain size is essentially complete, older than the median microcephalic death age, not unusual in shape compared to other microcephalics, etc.

I think there is little light here. Clearly no answers are possible from a single microcephalic. This microcephalic was not like LB1, but there are many microcephalics -- probably most -- that were not like LB1.

Indeed, I wouldn't rule out that LB1 was microcephalic even if no modern microcephalics have its exact characteristics, since no modern microcephalics lived relatively long lives in Stone Age societies. There is a component of variability in examining such ancient skeletons that cannot be corrected with comparisons of living and recent humans. This may be a part of that.

How about the dwarfing allometry stuff?

Martin and colleagues present an argument for why the brain size of LB1 could not result from dwarfing:

The tiny cranial capacity of LB1 cannot be attributed to intraspecific dwarfism in H. erectus. Body size reduction in mammals is usually associated with only moderate brain size reduction. Starting from three potential ancestral forms (H. erectus broadly defined; the chronologically and geographically closest H. erectus specimens from Ngandong, Java; and the substantially earlier Dmanisi hominids from Georgia) and following a range of possible dwarfing models, the predicted body size of a dwarf hominid with the cranial capacity of LB1 ranges from less than 1 g to 11.8 kg (Table 1 and Fig. 1) (4). Most of the figures calculated are at least an order of magnitude smaller than the estimates for LB1 (16 to 29 kg) (1). The largest are based on the insular dwarfing of elephants on Mediterranean islands (Model A) from 10,000 to 15,000 kg down to 100 kg. Despite the extreme dwarfing involved, and the relatively steep brain-body size scaling slope, the predicted body size for the dwarf hominid is still unrealistically small. Typical mammalian intraspecific scaling (Model B) indicates a maximum body weight less than half that estimated for LB1. Intraspecific brain-body size scaling in primates, including humans, is notably flat, particularly for males and females separately (5). This model (Model C) predicts tiny body weights for LB1.

There are also an associated figure and table. This critique is correct, and close to close to what I wrote in my 2004 FAQ on the specimen. You can't accuse me of leaving out the significant details!

But Falk and colleagues aren't hemmed in by this critique, because they aren't committed to the position that LB1 was a phyletic dwarf. For all they know, it could be an australopithecine -- in which case, the brain would not be unusual. That hypothesis presents its own problems (how did they get to that island, again?) but the brain size is certainly not one of them.

What do I think?

For the most part, my opinion from the October 2005 update still holds. I still think the specimen has widespread pathology, and I still think that's sufficient to question whether it was representative of its population.

But... I have a new hypothesis I've been working on. It's secret. OK, so now I am leaving out significant details....

Personally, I can't wait to see the long critical papers come out. Then we'll have a better idea of the boundary conditions.

I think that Carl Zimmer makes a great point in his post this week:

I wondered [in October], and I wonder now, why the editors of Science don't make sure that everyone agrees on the ground rules for comparing these brains before they publish? Otherwise both sides just squabble about methods and presentation, rather than about meatier matters.
The problem may be that in both cases Science has relegated this exchange to the "Technical Comment" section, where reports are much shorter than normal papers. The descriptions of methods used in the research are often scant, and the comments also tend to include cryptic interpretations that cry out for more explanation. Falk and her colleagues say that the Hobbit's brain is consistent with apes or australopithecines, not Homo erectus. Now, I'd imagine that this might imply that the Hobbit descends not from Homo erectus, but from some Australopithecine that came out of Africa. That would be huge news if true. Yet the scientists just leave us hanging with a statement that is so cryptic as to be nearly useless.

They must face this problem a lot, though. Who is Science going to bring in as a referee to make the two sides agree? And are they willing to let it go to another journal? Because these folks will take their work elsewhere rather than be forced to use someone else's methods.

Personally, I think they should have a special hobbit issue where they hash out all these things. If they can have special Drosophila genome issues and special Cassini issues, they can surely have a special hobbit issue.

I'd be happy to contribute a paper!

References:

Falk D, Hildebolt C, Smith K, Morwood MJ, Sutikna T, Jatmiko, Saptomo EW, Brunsden B, Prior F. 2006. Response to comment on "The brain of LB1, Homo floresiensis". Science 312:999. DOI link

Falk D et al. 2005a. The brain of LB1, Homo floresiensis. Science 308:242-245. Full text (free)

Falk D et al. 2005b. Response to comment on "The brain of LB1, Homo floresiensis". Science 310:236. Full text (subscription)

Martin RD, MacLarnon AM, Phillips JL, Dussubieux L, Williams PR, Dobyns WB. 2006. Comment on "The brain of LB1, Homo floresiensis". Science 312:999. DOI link

Weber J, Czarnetski A, Pusch CM. 2005. Comment on "The brain of LB1, Homo floresiensis". Science 310:236. Full text (subscription)