by Greg Mayer

While in Colombia last week, Jerry directed my attention to a paper by Roy Britten (abstract only free) in that week’s issue of the Proceedings of the National Academy of Sciences. Britten is a venerable figure in evolutionary molecular genetics, one of the pioneers of DNA-DNA hybridization who helped elucidate the structure of the genome long before sequencing was possible. The paper was indeed interesting. This post is a bit longer and more data-and-analysis-laden than usual, but I think the paper merits discussion.

Britten summarizes his latest paper’s conclusions succinctly:

The aim of this paper is an explanation for the high speed of evolution of the human lineage, which has been exceptional compared with other animals. The high speed of evolution of human lineage brain size is recognized by comparison of fossil brain sizes (1, 2). Evolution of the lineage leading to humans during the last several million years was striking. … A major source of variation [for brain evolution] has been the insertion of transposable elements (TEs).

He goes on to note that besides rapid brain evolution, humans have many TE insertions. For him

This is an extraordinary correlation. Human evolution has been rapid, particularly brain evolution in the last several million years. It is the only species known to make such rapid evolutionary progress. Now it is shown that human is the only species studied to have so many TE insertions. Recognition of this correlation leads to the concept that Alu insertions underlie rapid human evolution.

Importantly, he states up front that:

We believe the brain evolution was due to natural selection and genomic variation.

He is thus not seconding Colin Blakemore’s unwarranted claim that brain size is a neutral character, conferring neither selective advantage nor disadvantage, that must therefore have evolved via genetic drift. Britten is definitely not saying this, and is thus not open to the criticisms of Blakemore made by Jerry (here and here) and John Hawks. Britten thinks a big brain is advantageous.

So, how well supported are the claims he does make? I’d first note that one data point does not a correlation make, especially not an extraordinary one. TE’s, by increasing mutation rates, can certainly increase evolutionary rates, but all sorts of other singular characteristics apply to the Homo lineage. In addition to having many TE’s, they were savannah-dwelling, nearly hairless, bipedal, etc. Which of these correlates with rapid brain growth is the important one? I don’t know, but a more forceful argument than simple occurrence in the same lineage would be needed to establish which is the most likely causal factor.

And what about the factual points? Much of the paper is devoted to establishing the prevalence of TE’s in the human lineage, and I, as at least a first approximation, would yield to Britten’s expertise on this point. What about the rate of brain size evolution? (To be fair, Britten takes his cue here from the literature; the high rate is a premise, not a conclusion.) G.G. Simpson, one of the founders of modern evolutionary biology, spent a major part of his career documenting the variability of evolutionary rates. He showed that there is great variability of evolutionary rates between lineages, among characters within lineages, and within lineages at different times. The following figure is based on an original in Simpson’s 1953 Major Features of Evolution. It shows that the rate of evolution in lungfish was high about 300 million years ago, but not so much at other times (i.e. variation within lineages at different times).

Historically, claims of human exceptionality have tended to become less exceptional when examined more closely. Huxley’s debate with Owen over the brain is perhaps the classic example: contra Owen, Huxley “showed that the brains of apes and humans were fundamentally similar in every anatomical detail.” Knowing this, I decided to check on this important premise of Britten’s paper. Is the speed of evolution of the human brain “striking”, and “exceptional compared with other animals”? In a word, no: over the last several million years, human brain size has evolved at rates which are typical of paleontologically measured evolutionary rates.

Here’s a graph by John Hawks (using the same or similar data as Lee and Wolpoff, 2003) showing the pattern of change in cranial capacity (on the vertical axis, in cubic centimeters) over the last 2 million years or so.

There are a number of ways of measuring evolutionary rates of morphological features such as cranial capacity. One useful measure is the haldane, developed by Phil Gingerich (1993) of the University of Michigan Museum of Paleontology, based on a suggestion made in 1949 by the original most interesting man in the world, the great geneticist-physiologist-soldier-pacifist-communist-Hindu-atheist-patriot-expatriate J.B.S. Haldane, one of the founders of modern evolutionary theory. The haldane is the change, on a logarithmic scale, of the feature in question in units of the standard deviation (a measure of how variable the feature is), per generation.

Using data from three papers on modern human cranial capacity, I found the average to be 1345 cubic centimeters (cc), calculated as the unweighted average of males and females from the measured populations from Korea, Turkey, and Nigeria (a total sample of 1151). 1.8 million years ago, the cranial capacity of the Homo lineage was 702 cc, calculated as the average of skulls of that age from Perning, Kenya (one each, given by Lee and Wolpoff, 2003), and Dmanisi (three skulls, given by Gabunia et al., 2000, for two of them, and the median of two estimates by Lee, 2005, for the third).

The logarithmic standard deviation is well approximated by the coefficient of variation (CV: the untransformed standard deviation divided by the mean; Lewontin, 1966). The unweighted average CV for the modern humans was .0955, and for the five early Homo it was .1149; averaging, we get .1052.

So, the amount by which cranial capacity has changed on the log scale is ln(1345)-ln(702)=.6502; dividing this by the estimated logarithmic standard deviation, .1052, gives 6.181. In the last 1.8 million years, our cranial capacity has increased about 6 standard deviations. We don’t know generation time for early Homo, but we do know it for modern humans (about 25-30 years) and chimps (19-24 years; Matsumura and Forster, 2008). Using 25 years as an estimate for the whole lineage, we get 72000 generations in the last 1.8 million years, giving an evolutionary rate for brain size of .00008584 (or 10^-4.066) haldanes.

Is this a high rate or a low rate? Neither– it’s absolutely typical for evolutionary rates measured over this generational time scale. Gingerich (2001) compiled a large data set on rates of evolution, measured in haldanes, over a wide variety of time scales. He states:

Macroevolutionary studies yield rates on the order of 10^-2–10^-6 haldanes calculated over intervals of geological time ranging from 10^2–10^6 generations.

If we look more precisely, at about 72000 (10^4.86) generations, we find measured rates of about 10^-3.5 to 10^-6.5. So the rate of human brain evolution is above the median, but nothing “exceptional”. Could this unexceptional result be due to the particular initial time (1.8 mya) selected? What if we looked further back in time? I redid the analysis using an average chimpanzee cranial capacity of 383 cc (McKee et al., 2005), and a divergence time of 6 million years. Using the same logarithmic standard deviation and generation time, we get  [ln(1345)-ln(383)]/.1052 = 11.940 standard deviations, nearly twice the 6 standard deviation change in the last 1.8 million years. Dividing by the 6 million years/25 years per generation = 240000 generations gives .00004975 (or 10^-4.3) haldanes. Again, above the median, but nothing exceptional.

So, there’s nothing much remarkable about the speed of human brain size evolution. If the TE’s (or hairlessness or bipedalism or whatever) of the Homo lineage had an effect on human evolution, it was not expressed as an unparalleled increase in the rate of evolution of cranial capacity.

________________________________________________________

Acer, N., M. Usanmaz, U. Tugay, and T. Ertekin. 2007. Estimation of cranial capacity in 17-26 years old university students. Int. J. Morphol. 25:65-70. pdf

Britten, R.J. 2010. Transposable element insertions have strongly affected human evolution. Proceedings of the National Academy of Science 107:19945-19948.

Gabunia, L., et al. 2000. Earliest Pleistocene hominid cranial remains from Dmanisi, Republic of Georgia: taxonomy, geological setting, and age. Science 288:1019–1025.

Gingerich, P. D. 1993. Quantification and comparison of evolutionary rates.  American Journal of Science 293A: 453-478. pdf

Gingerich, P. D. 2001. Rates of evolution on the time scale of the evolutionary process. Genetica 112-113: 127-144. pdf

Haldane, J.B.S. 1949. Suggestions as to quantitative measurement of rates of evolution. Evolution 3:51-56.

Hwang, I.-L., et al. 1995. Study on the adult Korean cranial capacity. Journal of Korean Medical Science 10:239-242. pdf

Matsumura, S. and P. Forster. 2008. Generation time and effective population size in Polar Eskimos. Proc. R. Soc. B (2008) 275:1501–1508. pdf

McKee, J.K.,  F.E. Poirier, and W.S. McGraw. 2005. Understanding Human Evolution. Pearson, Upper Saddle River, New Jersey.

Lee, S.-H. 2005. Is variation in the cranial capacity of the Dmanisi sample too high to be from a single species? American Journal of Physical Anthropology 127:263–266. pdf

Lee, S.-H. and M.H. Wolpoff. 2003. The pattern of evolution in Pleistocene human brain size. Paleobiology 29:186-196. pdf

Lewontin, R.C. 1966. On the measurement of relative variability. Systematic Zoology 15:141-142.

Odokuma, E.I., P.S. Igbigbi, F.C. Akpuaka, and U. Esigbenu. 2010. Craniometric patterns of three Nigerian ethnic groups. African Journal of Biotechnology  9:1510-1513. pdf

Simpson, G.G. 1953. Major Features of Evolution. Columbia University Press, New York.