Life history trade-offs and human pygmies

Every few years a paper comes out "explaining" short stature in one or more Pygmy groups. Most of the time the new work ads new information and new ideas but fails to be convincing. This is the case with the recent PNAS paper by Migliano et al.

From the abstract:

Every few years a paper comes out "explaining" short stature in one or more Pygmy groups. Most of the time the new work ads new information and new ideas but fails to be convincing. This is the case with the recent PNAS paper by Migliano et al.

From the abstract:

Explanations for the evolution of human pygmies continue to be a matter of controversy, recently fueled by the disagreements surrounding the interpretation of the fossil hominin Homo floresiensis. Traditional hypotheses assume that the small body size of human pygmies is an adaptation to special challenges, such as thermoregulation, locomotion in dense forests, or endurance against starvation. Here, we present an analysis of stature, growth, and individual fitness for a large population of Aeta and a smaller one of Batak from the Philippines and compare it with data on other pygmy groups accumulated by anthropologists for a century. The results challenge traditional explanations of human pygmy body size. We argue that human pygmy populations and adaptations evolved independently as the result of a life history tradeoff between the fertility benefits of larger body size against the costs of late growth cessation, under circumstances of significant young and adult mortality. Human pygmies do not appear to have evolved through positive selection for small stature--this was a by-product of selection for early onset of reproduction.

I would like to add right in the beginning that the evolution of stature is probably, in my opinion, widely misunderstood. There are two problems. The first, which is not too related to the present discussion and that I'd like to dispense with right away, is that change over time in human stature is not easily attributed to genetic change. Secular change in body size seems in itself to be a capacity of certain mammals and may be a long or medium term response to ecological change. Increase in stature in human groups documented over the last century or more of time is not genetic change. We have no evidence that the short people ... the people carrying hypothetical "shortness" alleles ... were killed off differentially or failed to reproduce. Rather, increased nutrition (of some sort) seems to produce somewhat taller offspring in each generation. Perhaps there is a limit on growth that is determined by the mother. If nutritional load is increased beyond some limit, a given population produces somewhat larger (but not maximally larger) offspring, but over several generations, the full potential stature is realized.

But that is not the issue with African Pygmies, who are genetically short-statued.

The second issue is the idea that short stature is a derived adaptation in relation to "normal" or "typical" taller stature. The authors of this paper correctly point out that there is not a good single explanation for short stature. There are at least two possible reasons for this. First, we have not thought of an explanation yet, or among the list of possible explanations is the actual explanation, but we have not identified it or demonstrated it to a sufficient degree. Second, some subset of previously proposed explanations (possibly all of them?) is at work, but to different degrees in different situations. In other words, stature is an epiphenomenon resulting from multiple causes.

I would like to suggest that we begin to think of stature in a somewhat different ways. I propose that the following two things are true:

1. 1)For certain reasons, increased stature in humans is always good. Male-male competition, increased ranging behavior, and anti-predator tactics come to mind as selective forces for increased stature.
2. 2)For certain reasons, smaller stature in humans is always good. In the absence of selection for tallness, shortness has a significant energetic advantage, for instance.

The tradeoff between good reasons to be tall and good reasons to be short are always in play, so the optimal stature for a given population may shift even so dynamically that stature changes through either secular variation or allelic changes are only barely able to track the optimum.

This is why the life history approach taken by the research being discussed here is a good one. Life history theory is about tradeoffs. In the absence of a qualitative shift of some kind, an organism has a limited amount of energy that must be budgeted over short periods of time and over a lifetime. Classically, the three major "budget lines" for this energy are growth, reproduction, and maintenance (maintenance including immune system activity). Stature does not fit into one of these categories, but rather, should be responsive to all three. Stature determines a good portion of the energy partitioned into growth. Larger vs. smaller individuals have more vs. less daily maintenance demand, and producing larger vs. smaller offspring demands more or less energy.

This paper attempts to assertain if Pygmy stature is a function of nutritional variation by comparing data from Pygmies with other groups to examine the growth curve. This is largely a rehash of previous research, done some time ago, that established that African Pygmies are genetically short of stature. This is one of those rare cases where a genetic cause is not only evidenced by the appearance of the phenotype, but the gene involved is known.

The next thing they do is to estimate mortality and fertility patterns for Pygmies, and in this effort they find Pygmies to be more akin to Chimpanzees than to other humans. This result is fairly dicey, however. The ideal data for both mortality and fertility is simply not available for chimps or humans. Yes, there are data, but the sample sizes are inadqueate. In addition, their literature search indicates that Pygmy life expectancy is low, averaging 18 years and ranging from 15.6 to 24.2 years, compared to other groups including the !Kung, Ache and Turkana. The problem with this is that while !Kung and Ache life expectancy is indicated to be longer, they are not at all very much taller, and the !Kung live in a savanna environment. In other words, the comparison is being made between mostly rain forest populations with data collected from periods when disease from the outside may have a strong effect, with data from various time periods of people living in environments including those with much less disease. The authors write-off the importance of these effects but, well, they can't really do that.

I would not be surprised if there was a link between stature and life span, but the data available at this time are not sufficient to make the case. Indeed, the relationship could easily be the opposite of what is asserted here. Life history theory would predict that growing big could produce, as a matter of trade offs, decreased life span, when comparing populations that are different in their life history parameters but otherwise similar (same species, same environment, same diet, etc.).

I still prefer the hypothesis of diet and thermoregulation as explanations for Pygmy stature and body form. The authors of this paper produce a red herring by grouping together Asian and African populations into one, ignoring what is known about the histories of the two groups. African Pygmies have been living in the rain forest for quite some time, as opposed to non-Pygmy groups who have moved into the region fairly recently. The history of Asian "Pygmy" populations is probably less well understood, but there is reason to expect a similar history. The authors cite Diamond's conjecture that forest dwelling is not an explanation for pygmy stature because of the Asian cases, but Diamond is probably simply wrong on this. South Asian short stature groups may well have been living in rain forests much longer than other groups.

Bamberg Migliano, Andrea Vinicius, Lucio Lahr, Marta Mirazon. Life history trade-offs explain the evolution of human pygmies. PNAS Proc. Natl. Acad. Sci. USA, 10.1073/pnas.0708024105, ().