diet

A paper in the current Journal of Human Evolution by Victoria Wobber, Brian Hare and Richard Wrangham (Wobber et al., 2008) reports on a series of experiments trying to get great apes to eat cooked food. With meat, sweet potatoes and carrots, it seems they like the cooked version better—although with apples and regular potatoes they are indifferent. They also tried to figure out if the apes liked the cooked food because of its taste, texture, or what.

They put their paper into the context of the evolution of food preference and cooking in hominids. Cooking clearly has some benefits for hominids: it transforms some indigestible foods into useful ones, facilitates energy release from some foods with less digestive requirements, and it reduces the wear and tear on teeth. The question: When did the hominid taste system adapt to match the dietary benefits of cooking? Did hominids start out with a taste for cooked food, which they could satisfy when they invented fire? Or did hominids invent fire for other reasons (e.g., light, protection) and only later adapt their sensory systems to tolerate cooked food?

The study answers this question by showing that the taste preference for some cooked foods may have already been present in ancestral hominids. The fact that all of the great ape species showed a preference for some cooked foods is pretty convincing. It seems that the study included enough trials to show that this wasn’t simply the apes preferring to try something different from their usual diet, although this might bear more checking. One would also want to exclude the possibility that the apes had been smelling cooked foods for many years (as a result of human contact—these being captive apes).

The results raise the question of why exactly apes should exhibit a preference for a style of food they have never eaten, and would never obtain in their natural habitats. We may hypothesize that the same kinds of molecular signals that are present in certain cooked foods are also useful for differentiating between other good and bad foods. This is the explanation favored by Wobber et al.:

I find it interesting that the chimpanzees in the study exhibit such a strong preference for cooked meat. Meat gets a lot of attention in both chimpanzee and human groups, and was apparently handled more intensively by early Homo than earlier hominids. I wonder if this might have spurred experimentation to a greater extent than more quotidian plant foods.

References

Giant clams are in the news today, helping to drive the expansion of modern humans out of Africa. Can we believe it?

• The paper (Richter et al., 2008) describes a new species of giant clam, distinct from others in reproductive cycle, habitat preference and size.
• This new species is mainly found in shallow water reefs.
• Today, the species makes up a very small proportion of the total Red Sea giant clam count.
• Before the last interglacial, this species made up as much as 80 percent of the giant clam count, as assessed by shells from reef terraces. This proportion decreased around the last interglacial, and again in historic times.

This sounds like the classic megafaunal exploitation story, as it is being reported. Shells become an important debris of humans in Northeastern Africa by 125,000 years ago (Walter et al., 2000), and were important elements of the MSA along the coasts of North and South Africa (McBrearty and Brooks, 2000). So it would not be surprising if these people recovered giant clams, particularly if those clams were readily available in shallow water. Giant clams are similar to large tortoises in terms of their recovery and exploitation, and there is already good evidence that tortoise size decreased with overhunting as Late Pleistocene human populations grew. By the Upper Paleolithic, people in some parts of the Mediterranean began to harvest small shellfish to an extent that put pressure on their populations. The giant clams would be an early example of the same phenomenon, made more precarious by the shallow-water habits of this particular clam species.

Since refuting the Neandertal inferiority complex is a theme this week, I should point out that Neandertals who lived on the coast also exploited shellfish, an observation that I discussed here. The exploitation of coastal resources is not specifically“modern”. Coastal populations of terrestrial predators typically eat marine species, for example, coastal brown bears in Alaska systematically harvest soft-shelled and razor clams (Smith and Partridge, 2004).

So the clams shouldn’t be surprising. Are they interesting? I think it is another piece of evidence that human populations in Africa during the last interglacial were already large and growing. Archaeological sites from the African Late Pleistocene have been proliferating during the last few decades, but are still underrepresented compared to the density of sites in other regions, especially Europe and the Near East. So you might not get the idea from archaeological sites that the African population was especially large. Yet, across the MSA, we see increasing breadth of faunal exploitation and some systematic recovery of small resources such as shellfish and tortoises. We also see a greater intensity of raw material exploitation and movement, and

Most important, we now have clear genetic evidence for a large and diverse African population during the Late Pleistocene. That includes the mtDNA genealogy, which now supports the interpretation of an effective population size that had perhaps doubled or more by the last interglacial (I discussed that research here). Put that together with the evidence for structure within this ancient population — either regional differentiation or ecological adaptation — and we have some very interesting demographic knowledge about Africa 100,000 years ago.

References

I've followed the literature on early hominid diets from the beginning of the weblog. In 2005 I discussed Peter Ungar's analyses of dental occlusal morphology in A. afarensis versus Homo, concluding:

The contrast between Homo and A. afarensis is in the same direction as the contrast in occlusal morphology between primarily meat-eating carnivores like felids and canids as opposed to more omnivorous carnivores like bears. Another observation is that meat is a major food resource of chimpanzees, although this is hardly a fallback resource. Indeed, if meat eating was indeed an important component of the behavioral repertoire of early Homo, it probably is not fair to assert that the difference in diet between Homo and Australopithecus was primarily a difference in fallback resources. It may be true that australopithecines and early Homo overlapped in their food resources, particularly in plant species consumed. But considering the likely effectiveness of early humans as predators, I think it likely that the fallback foods of early humans--when hunting was ineffective--may well have been the preferred foods of australopithecines. And when australopithecines were forced to abandon their preferred foods by early humans, they were forced to fall back upon resources that either were common or were difficult for early Homo to exploit. The disappearance of early small-bodied Homo by around 1.6 million years ago, and the ultimate extinction of the robust australopithecines after a progressive increase in their molar sizes (Wood and Lieberman 2001) indicate that this fallback strategy could not be maintained in the face of increased hunting effectiveness by large-bodied Homo.

The concept of "fallback foods" has captured a large mindshare in explaining early hominid diets. The idea is that a species may depend on preferred, staple foods for most of the year, but adopt less preferred, "fallback" foods when their staple is not available -- for instance, during the dry season.

What can fallback foods explain about early hominids? For one thing, they could explain the difference between robust and non-robust australopithecines. We know from isotope data (reviewed in this 2005 post about Matt Sponheimer's work) that A. africanus and A. robustus had similar fractions of C₃ and C₄ plant source foods in their diets. Across the year, they may have eaten roughly the same mix of foods. A 2005 paper by Greg Laden and Richard Wrangham (discussed here) explored the idea of underground storage organs of plants, or tubers, as fallback foods for australopithecines. Later studies of isotope data using laser ablation of small segments of the enamel (discussed here) showed that diet proportions may have substantially varied across the time that teeth were developing -- possibly concordant with the idea of seasonal or longer-period fallback foods. An earlier analysis of dental microwear in the two hominids by Scott and colleagues (discussed here) came to a similar result: there was great variability in wear properties, especially within A. robustus, although the average in the two species showed a possibly greater fraction of brittle, hard foods consumed by the robust australopithecines.

So I've written about the topic a lot, and followed it closely.

Now, Peter Ungar, Frederick Grine and Mark Teaford have examined the wear properties of the molars of Australopithecus (Paranthropus) boisei. They find that -- unlike A. robustus -- none of the seven specimens showed any evidence of having eaten hard or brittle foods:

Comparisons with the extant baseline series suggest that none of the Paranthropus boisei individuals examined consumed extremely hard or extremely tough foods in the days before death. All of these specimens lacked the extremes of Asfc evinced by Lophocebus albigena and especially Cebus apella, both known to consume hard, brittle foods. Paranthropus boisei molars also lacked the extremes of epLsar seen in Trachypithecus cristata and Alouatta palliata, both known to consume tough leaves and stems. The P. boisei individuals examined evidently avoided such metabolically challenging foods, at least in the days before death. This is notably consistent with Walker's [23] early assertion that P. boisei microwear patterns resemble those of living frugivores, and differ from those of living grazers, leaf browsers, and bone feeders.

Comparisons with the South African hominins suggest that while Paranthropus boisei may have consumed foods with similar ranges of toughness as those eaten by Australopithecus africanus, the eastern African "robust" hominin did not eat harder and brittler foods than the South African "gracile" form. Further, the patterns for P. boisei and P. robustus are very different. Paranthropus robustus likely ate foods that were on average much harder and less tough than P. boisei. The differences in both central tendencies and ranges of variation suggest different feeding strategies, and by implication, that the two species of Paranthropus probably had markedly different diets or foraging strategies (Ungar et al. 2008, italics lost).

That is very interesting that A. robustus and A. boisei are so different in their microwear patterns. It makes me wonder whether there may have been substantial habitat variation in the use of hard foods -- maybe the extant A. robustus sample, mainly drawn from a small area of South Africa, had access to some food items that were rare or absent across the larger East African range of A. boisei. But if some A. boisei populations had also depended on such hard resources some of the time, you might expect that we would have found one, or at least a bit more variability. Yet the sampled specimens, drawn from a distance from Ethiopia to Tanzania and well over a half million years of time, are pretty uniform in their microwear, showing some variability in the anisotropy dimension (here, high values have mostly parallel striations, attributed to fibrous food consumption).

So we can return to the question: the major hominid competitor of A. boisei was Homo. Both lineages appeared in the period around 2.5 million years ago, and remained sympatric throughout the next million years. Some of the dynamics of that interaction must have involved diet (considering the different dietary adaptations of the two). We can speculate that A. boisei didn't get much meat, which would then be an important difference. But what else was A. boisei eating?

Meanwhile, the data are still consistent with the idea of fallback foods in A. robustus as a driver of dental morphology, but the story for A. boisei now seems less clear. With only seven specimens, there is almost certainly not enough data to test the hypothesis -- which after all predicts that the use of hard brittle foods may be rare. But that's not positive evidence either. Is there some other food that might explain the hyperrobust craniodental morphology?

References:

Ungar PS, Grine FE, Teaford MF (2008) Dental Microwear and Diet of the Plio-Pleistocene Hominin Paranthropus boisei. PLoS ONE 3(4): e2044. doi:10.1371/journal.pone.0002044

Julien Riel-Salvatore reviews some reasons why kuru did not wipe out the Neandertals.

I don't have anything to add. The hypothesis comes from a paper in Medical Hypotheses by Simon Underdown; here's part of the abstract:

TSEs could have infected Neanderthal groups as a result of general cannibalistic activity and brain tissue consumption in particular. Further infection could then have taken place through continued cannibalistic activity or via shared used of infected stone tools. A modern human hunter-gatherer proxy has been developed and applied as a hypothetical model to the Neanderthals. This hypothesis suggests that the impact of TSEs on the Neanderthals could have been dramatic and have played a large part in contributing to the processes of Neanderthal extinction.

The short paper is admittedly speculative but quite clear. It does fail to cite the literature about selection on the prion gene, PRNP (I discussed it here in early 2006).

Riel-Salvatore points out all the reasons why it is probably wrong:

1. Neandertals were eating each other 100,000 years before they went away.

2. Neandertals didn't live as long as most humans who develop TSE symptoms.

3. Neandertals lived at much lower densities than the Kuru-spreading Fore people, and it's not credible for them to have spread a prion disease by cannibalism across this space (although, the urine-dispersed CWD seems to do spread pretty well through deer).

4. Non-Neandertals have a clear record of altering human skeletal remains also, including African Middle Pleistocene and early Upper Paleolithic Europeans.

I think these points are fatal to the hypothesis, unless we resort to a different mode of transmission; but in that case there is no reason to suppose that a prion disease would be involved rather than a viral or bacterial agent. I should also mention that despite early claims, there is not any reason now to think that the human prion gene was under long balancing selection.

References:

Underdown S. 2008. A potential role for Transmissible Spongiform Encephalopathies in Neanderthal extinction. Med Hypotheses (in press) doi:10.1016/j.mehy.2007.12.014

It's hard to improve on the headline of this story:

Why chimps eat dirt

...

[Sabrina] Krief collected the dirt along with leaves from one of the chimps' favorite foods, the Trichilia rubescens plant. She found that when eaten alone, the leaves had no pharmacological effect, but when combined with soil, the mixture had clear anti-malarial properties.

Scientists previously suspected that animals might eat dirt when stressed or as a source of missing minerals. This new result is the first suggestion that the combination of soil and other foods could have health benefits, Krief said.

The story also discusses the use of high-kaolinite dirts as antidiarrheal treatments in local peoples -- kaolinite being the nameworthy ingredient of Kaopectate, although it is no longer used in that medication.

Anyway, this is a good excuse to use the word "geophagy." Great word.

While I'm pointing to articles about obesity genetics, I should include this book excerpt by Gina Kolata, which appeared in the NY Times a couple of weeks ago:

Genes Take Charge, and Diets Fall by the Wayside

...

Before the diet began, the fat subjects' metabolism was normal — the number of calories burned per square meter of body surface was no different from that of people who had never been fat. But when they lost weight, they were burning as much as 24 percent fewer calories per square meter of their surface area than the calories consumed by those who were naturally thin.

The Rockefeller subjects also had a psychiatric syndrome, called semi-starvation neurosis, which had been noticed before in people of normal weight who had been starved. They dreamed of food, they fantasized about food or about breaking their diet. They were anxious and depressed; some had thoughts of suicide. They secreted food in their rooms. And they binged.

The Rockefeller researchers explained their observations in one of their papers: "It is entirely possible that weight reduction, instead of resulting in a normal state for obese patients, results in an abnormal state resembling that of starved nonobese individuals."

It's an interesting read on some history of research into human weight loss, weight gain, and diet. It also has a compelling ending:

The message is so at odds with the popular conception of weight loss — the mantra that all a person has to do is eat less and exercise more — that Dr. Jeffrey Friedman, an obesity researcher at the Rockefeller University, tried to come up with an analogy that would convey what science has found about the powerful biological controls over body weight.

He published it in the journal Science in 2003 and still cites it:

"Those who doubt the power of basic drives, however, might note that although one can hold one's breath, this conscious act is soon overcome by the compulsion to breathe," Dr. Friedman wrote. "The feeling of hunger is intense and, if not as potent as the drive to breathe, is probably no less powerful than the drive to drink when one is thirsty. This is the feeling the obese must resist after they have lost a significant amount of weight."

It seems to me that discussion of the evolution of obesity-related genes has been wrongly directed toward the pathological result. Instead of the variation in weight gain, we need to consider how this variability in hunger would have affected people in the relevant populations.

Mason Inman has a cute article on Inkling, titled "Do these genes make me look fat?" It's a riff on the thrifty genotype hypothesis:

But why do we have obesity genes in the first place? The most popular theory is that we have "thrifty genes," hand-me-downs from our ancestors, who periodically faced famines and scarcity. The idea is that certain genes allow us to run more efficiently and to get by on scraps when times are lean. The flip side is that when food is a-plenty, we end up carrying around a spare tire. This obesity may or may not have hurt some of our ancestors, but the advantage of being able to survive lean times outweighed the disadvantages - so the theory says. 

The reason why this is newsworthy is the profusion of recent papers finding "obesity genes" of one kind or another, including the mysterious FTO:

In the European population studied, around half of adults had at least one "fat" FTO allele. The new gene seems to play a role in diabetes, too - a tantalizing link, since obesity and diabetes are both rising, and the obese are at risk for developing Type II diabetes. Strangely FTO, unlike other diabetes genes, doesn't seem to influence insulin, the hormone that regulates blood sugar levels. Instead, it was directly linked to people's body mass index. And the authors have no clue how this gene works.

That will increasingly be the case; we will know that genes are correlated with phenotypes but we won't know why. It's just a consequence of gene-phenotype correlation studies proceeding faster than our knowledge of gene-gene interactions.

I often ask my students what will happen to obesity in the future. Will it decline under selection? Or will it increase? Or stay the same? It's a great example to use, because even though nobody seems to like it, and everybody thinks it might kill you, there's still not particularly any fitness disadvantage to it. That's because we fat people still reproduce!

Inman's story almost arrives at that conclusion, but sort of wimps out:

Just as natural selection favored fat genes in centuries previous, the stage seems set today for evolution to weed them out. It won't happen overnight, of course. Take the intriguing observation that mildly overweight people show lower overall mortality than normal-weight people. So perhaps, even in this modern world, a predisposition for carrying a few extra pounds might help survival.

Oh yes, surely natural selection will save us from all becoming fat. Except it won't. Moowah-ha-ha-ha!

I found this article by Loren Cordain et al. while I was looking for something else, and thought I'd point it out:

Acne vulgaris: a disease of Western civilization

Background In westernized societies, acne vulgaris is a nearly universal skin disease afflicting 79% to 95% of the adolescent population. In men and women older than 25 years, 40% to 54% have some degree of facial acne, and clinical facial acne persists into middle age in 12% of women and 3% of men. Epidemiological evidence suggests that acne incidence rates are considerably lower in nonwesternized societies. Herein we report the prevalence of acne in 2 nonwesternized populations: the Kitavan Islanders of Papua New Guinea and the Aché hunter-gatherers of Paraguay. Additionally, we analyze how elements in nonwesternized environments may influence the development of acne.

Observations Of 1200 Kitavan subjects examined (including 300 aged 15-25 years), no case of acne (grade 1 with multiple comedones or grades 2-4) was observed. Of 115 Aché subjects examined (including 15 aged 15-25 years) over 843 days, no case of active acne (grades 1-4) was observed.

Conclusions The astonishing difference in acne incidence rates between nonwesternized and fully modernized societies cannot be solely attributed to genetic differences among populations but likely results from differing environmental factors. Identification of these factors may be useful in the treatment of acne in Western populations.

The observations are well-summarized there in the abstract. The introduction points out in addition other populations where acne was apparently rare or absent before Westernization, including Inuit and Okinawan peoples. Also, acne is less prevalent in more rural samples of mixed-ancestry populations, such as Peruvians or South Africans.

In the context of an apparent increase in acne with the introduction of urbanization and Westernized diet, the paper suggests that acne mainly results from diet, in particular depending on the insulin response. This mechanism is a bit involved, so if you are interested, you should refer to the paper.

The journal accompanied that article with an editorial, which notes the interest of recent research into links between obesity, insulin resistance and hyperandrogenism.

This is a great couple of paragraphs:

Cordain et al (1) suggest that diet-induced hyperinsulinemia elicits endocrine responses that may affect the development of acne through mediators such as androgens, insulinlike growth factor (IGF) 1, IGF binding protein 3, and retinoid signaling pathways. The role of diet in endocrine activity is supported by the observation that improvements in nutrition have been linked to an earlier onset of sexual maturation and the development of acne in young girls and boys. Numerous studies have shown that improvements in general nutrition in girls have led to an earlier onset of menses and that menses is delayed in girls with low body fat such as athletes and ballet dancers. (7) In 1970, the mean age of onset of menarche in the United States was 12 years compared with age 16 years for girls in 1835. (8) Of interest is the observation that the mean age of onset of menarche in the Kitavan population is 16 years, which is significantly older than girls in westernized societies. In a 5-year longitudinal cohort study of 439 black girls and 432 white girls in Cincinnati, Ohio, Lucky et al (9) demonstrated that those with severe comedonal acne had a significantly earlier age of onset of menarche and higher serum levels of dehydroepiandrosterone than girls with mild comedonal acne. This study demonstrated that the early development of comedonal acne might be one of the best predictors of later, more severe disease. In a similar 5-year longitudinal study of 219 black and 249 white early adolescent boys in Cincinnati, black boys had higher pubertal maturation scores than white boys of the same age. (10) The prevalence and severity of acne correlated well with advancing pubertal maturation. Is the late onset of menarche in Kitavan girls "protective" against the development of acne or severe acne? Although Cordain et al do not present data regarding the age of sexual maturation of the Kitavan or Aché boys, is it also possible that their relative lack of acne might relate to a later age of pubertal maturation and sebaceous gland exposure to higher circulating levels of androgen?

If acne results from hyperinsulinemia, as proposed by Cordain et al,1 one would expect that obese individuals, who are relatively chronically insulin resistant, would have a higher prevalence of acne. Bourne and Jacobs (11) evaluated 2720 military recruits for obesity and the presence of acne and noted an association between the 2 in the older recruits (ages 20-40 years) but not in those in the age range of 15 to 19 years. This observation suggests that the presence of acne in a younger population may be associated with factors other than obesity or insulin resistance. In fact, serum levels of IGF-1 are highest during periods of the adolescent growth spurt and taper off in the 20s, which coincides with the pattern in the peak incidence of acne. (12) Insulinlike growth factor 1 functions similarly to insulin in that it can promote the growth of keratinocytes and sebaceous glands. It is possible that that the effects of the hyperinsulinemia on acne in obese adolescents may be overshadowed by the effects of high levels of circulating IGF-1. As pointed out by Cordain et al, acne has been associated with elevated serum levels of IGF-1 in adult women with acne. (13) All adolescents, including the Kitavan and Aché, would experience increases in IGF-1 during adolescence, so increases in IGF-1 alone cannot explain the presence of acne.

Yes, IGF-1 is the tiny dog gene, in case you're wondering what kind of search led me to this!

The editorial is receptive but still skeptical of the diet-acne link proposed by Cordain et al.:

Although Cordain et al. (1) make a strong argument for the role of diet in acne, we believe that it is difficult to dissociate environmental factors such as diet from genetic factors in their study. The Aché and Kitavan people live in closely knit communities, and therefore genetic factors may play a role in the relative lack of acne in these populations. Several studies point to an association of genetic factors with acne, including studies that demonstrate variations in the prevalence of acne among ethnic groups and the high degree of concordance of acne in twins. (15-19)

There are a number of later references that cite the paper by Cordain et al., if you're interested in following up -- a link between acne and diet has always been problematic, but this is probably more or less because expression of the disease also depends on several genetic factors that are difficult to untangle.

References:

Cordain L, Lindeberg S, Hurtado M, Hill K, Eaton SB, Brand-Miller J. 2002. Acne vulgaris: a disease of western civilization. Arch Dermatol 138:1584-1590.

Thiboutot DM, Strauss JS. 2002. Diet and acne revisited. Arch Dermatol 138:1591-1592. Abstract

I just wanted to take down a note about this paper from last year, along with a couple of older studies of linear enamel hypoplasia:

Brief Communication: Linear enamel hypoplasia and the shift from irregular to regular provisioning in Cayo Santiago rhesus monkeys (Macaca mulatta)

Debbie Guatelli-Steinberg, Zeynep Benderlioglu

This study investigates changes in the prevalence of linear enamel hypoplasia (LEH) before and after the shift from irregular to regular provisioning in the Cayo Santiago rhesus monkey population. Prior to 1956, monkeys on this island colony did not receive consistent provisions, and were reported to be in poor health (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). A regular provisioning program, instituted in August 1956, resulted in the improved health of individuals and the growth of the population (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). LEH, a developmental defect of enamel, is a sensitive indicator of systemic physiological stress (Goodman and Rose [1990] Yrbk. Phys. Anthropol. 33:59-110). It was therefore hypothesized that the prevalence of LEH would be higher in monkeys who were irregularly provisioned than in monkeys who experienced regular provisioning. To test this hypothesis, teeth were examined for LEH in a sample of 181 female rhesus monkeys. The results support the hypothesis: the mean number of defects was statistically significantly higher in the preprovisioned group than it was in the postprovisioned one. When LEH prevalence was assessed using only defects occurring on antimeric pairs, the preprovisioned group again had a higher prevalence than the postprovisioned one, although the difference was not statistically significant, most likely because of the reduced sample size. The results of this study indicate that changes in LEH prevalence, at least in this population of rhesus monkeys, are associated with changes in nutritional status.

Other studies have shown a relationship between LEH prevalence and malnutrition among human populations. The unique aspects of this study are that it shows the same relationship in another primate species, and that it shows the response to a change in nutritional levels.

This response was shown in a human context by Alan Goodman and colleagues in 1991:

Nutritional supplementation and the development of linear enamel hypoplasias in children from Tezonteopan, Mexico

AH Goodman, C Martinez and A Chavez

The purpose of this study was to compare the effect of nutritional intake during tooth-crown formation on the subsequent development of linear enamel hypoplasias (LEHs) in Mexican nonsupplemented (control) adolescents (n = 42) and adolescents who had received daily nutritional supplements since birth (n = 42). The proportion of individuals with LEHs was nearly two-fold greater (74.4%; 95% CI 64.7-84.1%) in the control than in the supplemented group (39.5%; 95% CI 28.6-50.4%; chi 2 = 9.44; P = 0.001). Although the estimated peak age at formation, approximately 2-2.5 y, is similar in both groups, the proportion of early (before 1.5 y) and late (after 3.0 y) LEHs was greater in the control group. LEH was also more common in females and was associated with an increase in illness days and a decrease in growth velocity. Results of this study suggest that mild to moderate undernutrition during enamel formation is causally linked to the formation of LEHs.

The distribution shows that the two samples actually are very similar in the incidence of LEH at the modal age of between 1.5 and 2.5 years. Plausibly, this is not only attributable to disease, but also stress associated with weaning; some degree of LEH incidence may be more resistant to change by nutritional supplementation. Goodman et al. (1991:780) wrote:

The greatest relative difference in freuqency of LEH between supplemented and control groups occurs before 1.5 y and after 3.0 y, or before and after weaning and the time of greatest illness. It is as if all children are at great risk of LEH immediately after weaning, but the supplemented individuals are afforded greater protection before and after weaning. These data also support the hypothesis that common respiratory and gastrointestinal illnesses are an immediate cause of LEH, especially in individuals with compromised nutritional status.

Richard May, Alan Goodman and Richard Meindl conducted similar observations in Guatemala, reported in 1993:

Response of bone and enamel formation to nutritional supplementation and morbidity among malnourished Guatemalan children

Richard L. May, Alan H. Goodman, Richard S. Meindl

Enamel matrix secretion responded positively to increased supplementation. Children who received less than 34.25 kcal/day in supplement had more LEH than those who received more supplement. No differences in ossification status were found between supplementation groups. These data suggest that enamel formation may be more sensitive to changes in nutritional status than is bone mineralization. Disruptions of bone and enamel formation were both associated with frequent illness. Children who were ill more than 3.6% of the time had more LEH and fewer ossified hand-wrist centers than children who were less frequently ill. Conclusions regarding relative environmental sensitivity must take into account the specific aspects of dental and skeletal development examined.

This last part is an observation that different teeth seem to be more or less resistant to enamel formation disruptions.

References:

Guatelli-Steinberg D, Benderlioglu Z. 2006. Linear enamel hypoplasia and the shift from irregular to regular provisioning in Cayo Santiago rhesus monkeys (Macaca mulatta). Am J Phys Anthropol 131:416-419. doi:10.1002/ajpa.20434

Goodman AH, Martinez C, Chavez A. 1991. Nutritional supplementation and the development of linear enamel hypoplasias in children from Tezonteopan, Mexico. Am J Clin Nutr 53:773-781.

May RL, Goodman AH, Meindl RS. 1993. Response of bone and enamel formation to nutritional supplementation and morbidity among malnourished Guatemalan children. Am J Phys Anthropol 92:37-51. doi:10.1002/ajpa.1330920104

Nicholas Wade has an article in the Times this weekend concerning lactase persistence in Africans, which appears to have arisen in three separate mutations, each different than the mutation leading to lactase persistence in Europeans. All four of these mutations are very recent, and they constitute some of the strongest examples of positive selection observed in human populations:

The principal mutation, found among Nilo-Saharan-speaking ethnic groups of Kenya and Tanzania, arose 2,700 to 6,800 years ago, according to genetic estimates, Dr. Tishkoff's group is to report in the journal Nature Genetics on Monday. This fits well with archaeological evidence suggesting that pastoral peoples from the north reached northern Kenya about 4,500 years ago and southern Kenya and Tanzania 3,300 years ago.

Two other mutations were found, among the Beja people of northeastern Sudan and tribes of the same language family, Afro-Asiatic, in northern Kenya.

The article says "10 times as many descendants", which isn't correct -- the selective advantage of these alleles is only on the order of 10 percent, not 1000 percent!

I was talking to some folks about the isotope values for Neandertals, and was immensely surprised to find out that nitrogen-15 (¹⁵N) proportions can be driven higher by weight loss.

Here's an abstract of an article from last year by Fuller and colleagues:

While past experiments on animals, birds, fish, and insects have shown changes in stable isotope ratios due to nutritional stress, there has been little research on this topic in humans. To address this issue, a small pilot study was conducted. Hair samples from eight pregnant women who experienced nutritional stress associated with the nausea and vomiting of morning sickness (hyperemesis gravidarum) were measured for carbon (delta13C) and nitrogen (delta15N) stable isotope ratios. The delta13C results showed no change during morning sickness or pregnancy when compared with pre-pregnancy values. In contrast, the delta15N values generally increased during periods of weight loss and/or restricted weight gain associated with morning sickness. With weight gain and recovery from nutritional stress, the hair delta15N values displayed a decreasing trend over the course of gestation towards birth. This study illustrates how delta15N values are not only affected by diet, but also by the nitrogen balance of an individual. Potential applications of this research include the development of diagnostic techniques for tracking eating disorders, disease states, and nitrogen balance in archaeological, medical, and forensic cases.

Last year, I reviewed some papers that documented high ¹⁵N values in Neandertals, which concluded that the high values may have resulted from mammoth and rhinoceros consumption. In another post, I explored the reasons why fish (also a high ¹⁵N dietary source) have been neglected as an explanation for the high Neandertal ¹⁵N values.

Now, the papers on these topics (e.g. Bocherens et al. 2005) have compared Neandertal isotopic ratios to those of other fauna from the same time period, so trophic level and other relations ought to be visible within this sample. But other evidence suggests that Neandertals were under high nutritional stress compared to most living human populations, including the high incidence of enamel hypoplasias, which are developmental deficits of tooth formation (Molnar and Molnar 1985).

Comparisons suggest that Neandertal nutritional stress was not outside the range of living populations, with a similarity in the proportion of linear enamel hypoplasia in Neandertal and Inuit samples (Guatelli-Steinberg et al. 2004). In isotopic terms, this is a difficult comparison, since Inuit do eat lots of fish, marine mammals and other ¹⁵N-enriched foods.

Another element of complexity is that ¹⁵N composition responds to weaning time, because breast milk is enriched in ¹⁵N content also. This effect diminishes during childhood after weaning, by around age 7-9, so it shouldn't affect adult Neandertal specimens, but I point it out because nutritional stress may also affect the age of weaning or dietary independence, which might conceivably deplete ¹⁵N in lactating women. One might imagine lactation balancing some of the ¹⁵N surplus resulting from pregnancy or nutritional stress.

So it may be awhile before we will know what the full effect of nutritional stress may be on these isotope values.

References:

Bocherens H, Drucker DG, Billiou D, Patou-Mathis M, Vandermeersch B. 2005. Isotopic evidence for diet and subsistence pattern of the Saint-Césaire I Neanderthal: review and use of a multi-source mixing model. J Hum Evol 49:71-87.

Fuller BT, Fuller JL, Sage NE, Harris DA, O'Connell TC Hedges RE. 2005. Nitrogen balance and delta15N: why you're not what you eat during nutritional stress. Rapid Commun Mass Spectrom 19:2497-2506. PubMed

Guatelli-Steinberg D, Larsen CS, Hutchinson DL. 2004. Prevalence and the duration of linear enamel hypoplasia: a comparative study of Neandertals and Inuit foragers. J Hum Evol 47:65-84. PubMed

Molnar S, Molnar IM. 1985. The incidence of enamel hypoplasia among the Krapina Neandertals. Am Anthropol 87:536-549. JSTOR

Schurr MR. 1998. Using stable nitrogen-isotopes to study weaning behavior in past populations. World Archaeol 30:327-342.

Sponheimer and colleagues (2006, link) zapped some Swartkrans teeth with lasers to measure their ¹³C content. I wrote quite a bit here last year about australopithecine diets, including a long review of isotopic evidence for australopithecine diets.

With respect to dietary differences between A. africanus and A. robustus (the two species with any substantial isotopic sampling), there are four essential observations:

1. The apparent C_{4 dietary content of the two species is basically the same, and fairly high.}
2. High C₄ foods are not so easy to come by, they include some grasses and sedges and the animals who eat them.
3. The Sr/Ca ratios of the two species are fairly different.
4. The postcanine teeth of A. robustus seem to be adapted to crushing and grinding, moreso than A. africanus.

One hypothesis for the difference in Sr/Ca ratios is exploitation of underground tubers (warthogs and mole rats have elevated Sr/Ca similar to A. africanus). A mix of C₄ foods has been proposed to solve the grass-eating problem, including seeds, rhizomes, insects, lizards, and herbivore meat. But these don't really solve the postcanine tooth conundrum, and while they may both be true; neither is really testable.

OK, so does the new laser ablation study solve any problems? First, let's read a bit about what exactly it is, and why it might be useful. Ann Gibbons has written a ScienceNOW article:

[A] team of American and British researchers studied the teeth of four individuals of Paranthropus robustus (also known as Australopithecus robustus) from the Swartkrans Cave in South Africa. The team scanned the teeth with a sensitive laser, which did not destroy the teeth but etched them lightly enough to free carbon gases long trapped in the enamel. Because different plants absorb atmospheric carbon dioxide differently, the researchers were able to see what types of vegetation the hominids ate based on the ratio of carbon isotopes in their teeth.

An accompanying perspective by Stanley Ambrose explains:

In contrast to conventional methods, the laser ablation technique used by Sponheimer et al. barely penetrates the enamel surface of an area of less than 0.5 mm² and is thus nearly nondestructive (2). Laser ablation also avoids the problem of time averaging in large drilled grooves. Moreover, perikymata can be counted, providing a good estimate of the minimum time interval sampled and of the duration of tooth formation.

The Paranthropus teeth studied by Sponheimer et al. show interesting patterns of seasonal variation in diet and climate. All have the isotopic composition of mixed feeders, and two show at least ca. 40% variation in the proportions of C3- and C4-based resources over 1 year. One individual had a predominantly C3-based diet and foraged in a cooler, more humid environment; it may have formed its tooth in a very wet year. The others ate more C4-based foods in a warmer, drier environment. Their average carbon-isotope ratios are similar to those of adaptively versatile savanna baboons (2). Analyses of seasonal variation in teeth of modern and fossil baboons and of other hominin species are necessary to evaluate dietary specialization in Paranthropus and niche overlap with other hominin species.

Back to me. There are two possibilities. First, the differences between ¹³C values for different samples might be sampling the actual dietary variability of single A. robustus individuals over the course of their tooth development (in this paper, sampled over a course of a couple hundred days).

Or second, they may just be sampling noise.

The paper presents comparative data to suggest that this is actual variability in diet and not isotopic noise. They sampled some steenbok teeth from Swartkrans with the same technique. Steenbok are consistent C₃ browsers; their diet doesn't vary much in its ¹³C proportion over time. And the samples from the steenbok teeth didn't show very much variation across different sampling zones from the same tooth. Hence, it looks like the samples from different perikymata actually may give a consistent picture of dietary ¹³C composition over time.

Compared to the steenbok, the A. robustus samples show great heterogeneity in ¹³C content. This heterogeneity is manifested when looking at multiple samples from the same tooth, and it is also manifested when looking at different individuals. So far, that would seem to indicate dietary heterogeneity -- the A. robustus individuals ate a different mix of foods over time, and different individuals ate different foods.

On the basis of the magnitude of difference (particularly within the single specimen SKX 5939), Sponheimer et al. propose that some individuals must have gone from a diet predominantly composed of C₃ foods to one predominantly C₄ within the span of two years (estimated 644 days).

Here's how their paper concludes:

A dental microwear study of the earlier (3.0 to 3.7 Ma) hominin Australopithecus afarensis found no evidence that its diet changed over time or in different habitats (20). In contrast, stable carbon isotope (3, 4) and dental microwear texture analyses (1) of the slightly younger (3.0 to 2.4 Ma) hominin A. africanus demonstrated that its diet was far more variable. This suggests the possibility that a major increase in hominin dietary breadth was broadly coincident with the onset of increasing African continental aridity and seasonality after 3 Ma (21, 22) and only shortly antedated the first probable members of the genera Homo and Paranthropus (23-25) and the earliest stone tools (26). The undoubted toolmaker Homo is thought to have been a dietary generalist that consumed novel foods such as large ungulate meat and tubers that are abundant in savanna environments (27-30). Paranthropus, in contrast, with its extremely large and flat cheek teeth, thick enamel, robust mandible, and heavily buttressed facial architecture, is often portrayed as a dietary specialist (27-29). Further, it has been argued that this specialization contributed to its extinction when confronted with increasingly dry and seasonal environments later in the Pleistocene, whereas Homo's generalist adaptation was crucial for its success (28, 29). Our results suggest that Paranthropus had an extremely flexible diet, which may indicate that its derived masticatory morphology signals an increase, rather than a decrease, in its potential foods. Thus, other biological, social, or cultural differences may be needed to explain the different fates of Homo and Paranthropus (31).

We have lots of other reasons to believe that robust australopithecines were not dietary specialists, as pointed out by Wood and Strait (2004). Robust australopithecines had broad geographic ranges, were able to disperse over long distances, and persisted despite substantial climatic and environmental changes. The evidence for dietary differences across the lifespan is certainly consistent with this.

It does, however, make for an interesting conundrum: if australopithecines were selected on the basis of their ability to find different foods over the course of years, that suggests a strong role for social learning of more food types and broader geographic ranges. But if this was the path taken by robust australopithecines, what was the path taken by Homo?

References:

Ambrose SH. 2006. A tool for all seasons. Science 314:930-931. DOI link

Gibbons A. 2006. Not just nuts and berries for these hominids. ScienceNOW 9 Nov. Full text

Sponheimer M, Passey BH, de Ruiter DJ, Guatelli-Steinberg D, Cerling TE, Lee-Thorp JA. 2006. Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science 314:980-982. DOI link

Wood B, Strait D. 2004. Patterns of resource use in early Homo and Paranthropus. J Hum Evol 46:119-162. DOI link

Is it so wrong that my guilty pleasure this week is reading this man's diary of his experiment in eating only monkey chow?

I'm tired of cooking. I hate scrubbing pots and pans. I've wasted too much time in the checkout line. It's time to eat chow.

What is fascinating is that the thing clearly would have ended already, except that people started blogging about it! Now the frustration with the chow is competing with the allure of attention. How much does the attention have to wane before he gives it up?

Oops, sorry, that should be "the parallel evolution of bitter taste"...

Stephen Wooding and colleagues (2006) show that the ability to taste PTC -- long known to be a shared polymorphism in humans and chimpanzees -- evolved separately in each of these species:

It was reported over 65 years ago that chimpanzees, like humans, vary in taste sensitivity to the bitter compound phenylthiocarbamide (PTC). This was suggested to be the result of a shared balanced polymorphism, defining the first, and now classic, example of the effects of balancing selection in great apes. In humans, variable PTC sensitivity is largely controlled by the segregation of two common alleles at the TAS2R38 locus, which encode receptor variants with different ligand affinities. Here we show that PTC taste sensitivity in chimpanzees is also controlled by two common alleles of TAS2R38; however, neither of these alleles is shared with humans. Instead, a mutation of the initiation codon results in the use of an alternative downstream start codon and production of a truncated receptor variant that fails to respond to PTC in vitro. Association testing of PTC sensitivity in a cohort of captive chimpanzees confirmed that chimpanzee TAS2R38 genotype accurately predicts taster status in vivo. Therefore, although Fisher [yes, the Fisher] et al.'s observations were accurate, their explanation was wrong. Humans and chimpanzees share variable taste sensitivity to bitter compounds mediated by PTC receptor variants, but the molecular basis of this variation has arisen twice, independently, in the two species.

References:

Wooding S and 9 others. 2006. Independent evolution of bitter-taste sensitivity in humans and chimpanzees. Nature 440:930-934. DOI link

Melanie McCollum and colleagues have a short paper in JHE about the evolution of MYH16, the myosin gene associated with masticatory musculature.

Much of the article is devoted to debunking the connection of MYH16 to the expansion of the brain. There's not much to that story -- muscles beating down on the skull don't inhibit brain growth. And they discuss the implications of the revised date estimate for the deactivation of the gene by Perry and colleagues (2005).

But by far the most interesting part of this is their discussion of the effects of the evolution of masticatory myosin in other mammals:

With respect to interspecific variation in the expression of "masticatory" myosin, it is important to note that humans are not unique in their failure to express this particular isoform. "Masticatory" myosin is lacking in the jaw-closing muscles of a number of mammals, most notably ungulates, rodents, rabbits, and kangaroos (Kang et al., 1994, Sfondrini et al., 1996, Hoh, 2002 and Qin et al., 2002). Comparative genetic studies suggest that the masticatory MyHC gene originated through duplication of an ancestral striated MyHC gene expressed in the mandibular arch musculature of early gnathostomes, and that it has since been retained as the primitive phenotype in vertebrates (Qin et al., 2002). Functional loss of masticatory myosin in a number of non-carnivorous mammalian species is believed to have followed shifts in dietary strategies that ultimately freed these taxa from the need for powerful jaw closure. As a consequence, these taxa are believed to have replaced their masticatory myosin with functionally more appropriate myosin isoforms (e.g., slow/beta-cardiac fibers in ungulates, Kang et al., 1994; fast MyHCs in rodents, Sfondrini et al., 1996) (McCollum et al. 2006, references in original).

This would seem to support the hypothesis that changing masticatory function in hominids (caused by dietary changes) favored the gene's deactivation. But deactivation might have preceded the conversion of the gene into a pseudogene:

However, the very fact that muscle fibers readily change their myosin heavy chain expression suggests that masticatory myosin in hominids could very well have been significantly, if not totally downregulated prior to its conversion to a pseudogene. If this were the case, inactivation of the MYH16 gene would have had little impact on the muscles of mastication of early hominids and far less severe consequences for its carriers. In fact, the introduction of a nonsense mutation in the MYH16 gene may have been below the threshold of selection. If this alternative is correct, then the real question of interest is whether the change in masticatory function that occurred during hominid evolution and that led to MYH16 downregulation and inactivation was diet-related, as has been recently suggested (Hoh, 2002), or instead reflected changes in social behaviors that would have eliminated the need for an aggressive bite, as was suggested over 20 years ago (Rowlerson et al., 1983).

OK, so we have first the question of the date (2.4 million vs. 5.3 million years ago), and second the question of whether the functional change -- whatever it was -- preceded the date. So this could reflect anything from change associated with hominid origins up to the origin of Homo.

McCollum et al. make clear in their description of muscle fiber function that we may be looking not at a muscle decrease but a functional change. In which case, the deactivation might have accompanied greater masticatory force instead of less.

What a mess.

References:

McCollum MA, Sherwood CC, Vinyard CJ, Lovejoy CO, Schachat F. 2006. Of muscle-bound crania and human brain evolution: The story behind the MYH16 headlines. J Hum Evol (in press) DOI link

There's a new paper in AJHG by Patin and colleagues, which is just chock full of interesting stuff. The genes studied are NAT1 and NAT2, called "N-acetyltransferase genes" (OMIM entry), and are involved in the metabolism of certain drugs and carcinogens.

For example, they detoxify some of the carcinogenic amines that result from grilling meat. Different alleles of the genes are involved in some harmful drug interactions, since they affect the rate of drug metabolism. In other words, these are the kinds of genes that people interested in "personalized medicine" are most interested in -- they help to determine the response to harmful environmental agents and outcomes to treatment.

Patin and colleagues (2006) studied the evolution of polymorphisms of the two genes. Here's a quick review of what they knew starting out:

Both genes carry functional polymorphisms whose effects on enzymatic activity have been well studied (Hein et al. 2000). Whereas the variants associated with reduced activity attain only low frequencies in NAT1, they constitute common polymorphisms in NAT2 (Upton et al. 2001). Two main classes of NAT2 phenotypes are therefore observed: the "fast-acetylation" phenotype, which refers to the wild-type acetylation activity, and the "slow-acetylation" phenotype, which results in reduced protein activity. In addition, NAT1 and NAT2 metabolize numerous common carcinogens, and variation in these genes can result in varying susceptibility to cancer (for a review, see the work of Hein [2002]). For example, the slow-acetylator NAT2 phenotype has been associated with side effects to the commonly used antitubercular isoniazid (Huang et al. 2002) and with higher risk for bladder cancer (Cartwright et al. 1982; Garcia-Closas et al. 2005). Nevertheless, most NAT2 mutations leading to the slow phenotype are found at high frequencies worldwide, calling into question the role of altered acetylation in human adaptation.

So, the polymorphism of NAT2 is a bit mysterious -- what advantage might the slow-acetylators have to keep them around?

They did the usual sampling on "geographically diverse samples" and a chimpanzee sequence to determine site polarities. A twist makes the study a bit more complicated than usual: the genes are physically close together, so an allele for NAT2 may be significantly correlated with an allele for NAT1, for example.

The paper finds good evidence for selection on NAT2 alleles. Different alleles in different populations appear to cause the slow-acetylator phenotype. One of these, mainly in Europeans (NAT2*5B) has a stronger phenotypic effect (i.e., slower-acetylation), and has the strongest signature of recent selection. They infer that this allele came under selection between 5800 and 7000 years ago.

The footprints of natural selection identified in western/central Eurasians raise the question of which event(s) may have provoked fluctuations in the spectrum of xenobiotics inactivated/activated by NAT2 (e.g., NAT2 activates heterocyclic carcinogens found in well-cooked meat [Hein et al. 2000; Hein 2002]) in these populations. In this context, given the geographic distribution of the slow-acetylator phenotype and the estimated expansion time of the slowest-encoding 341TC mutation (5,797Ð7,005 years ago in western/central Eurasians), it is tempting to hypothesize that the emergence of agriculture in western Eurasia could be at the basis of such environmental changes. Indeed, there is accumulating evidence that this major transition resulted in a profound modification of human diets and lifestyles (Cordain et al. 2005) and, consequently, in the exposure of humans to chemical environments (Ferguson 2002). Moreover, the highest frequencies of slow acetylators are observed in the Middle East (fig. 5), one of the first regions where agriculture originated 10,000 years ago, and these frequencies decrease toward western Europe, North Africa, and India, three regions where agriculture was subsequently diffused from the Fertile Crescent (Harris 1996). However, the hypothesis that the transition to agriculture influenced both the human exposure to xenobiotic environments and, consequently, the selective pressures at NAT2 remains tentative and requires a better characterization of the naturally occurring substrates of the NAT2 enzyme.

The story for NAT1 is even more interesting. The coding region as a whole is much less variable than NAT2. But there is a divergent haplotype, separated by 17 SNPs from the rest of the alleles, and found in only three individuals (in France, India, and Thailand). Patin and colleagues propose that the haplotype may represent ancient population structure, similar to the earlier study from last year by Garrigan et al. (2005). Here's the relevant section of the paper:

Purifying selection may not be the only evolutionary force that has influenced NAT1 diversity. Indeed, one of the most salient observations of this study is the highly divergent tree topology and high TMRCA (2.01 ± 0.29 MYA) of this locus (fig. 2). This binary pattern is translated into significant departures from neutrality in populations presenting the divergent haplotype NAT1*11A (see table 7 and results of the HKA test). The probability of finding such a high TMRCA under a Wright-Fisher model was found to be low (P = .029). Different hypotheses can be proposed to explain such long basal branches in the NAT1 gene tree. First, long-term balancing selection can result in divergent haplotype clusters, by maintaining two or more alleles over time, provided that they result in functional differences. Nevertheless, our data do not support this hypothesis, since the two nonsynonymous mutations separating the two clusters (fig. 2) have been shown to have no significant effects on the in vivo protein activity in human cells (Hein 2002) or on the stability and activity of the recombinant protein in yeast (Hughes et al. 1998). Any kind of selection due to a hitchhiking effect with neighbor genes is equally unlikely, because the two closest genes (ASAH1 located 5 and NAT2 located 3) behave as independent haplotype blocks (this study and the HapMap database). Furthermore, our sequence data from the NAT1 coding region are consistent with the action of purifying selection rather than balancing selection, with the first selective regime having a minor influence on tree topologies (Williamson and Orive 2002). Second, gene conversion could also lead to such divergent haplotype patterns by the replacement of a segment of NAT1 with a tract from its nearby paralogs (NAT2 and/or NATP). This alternative is unlikely, however, since the 17 SNPs separating the two divergent NAT1 lineages are not physically clustered (fig. 2) as one would expect after gene conversion between duplicated loci (Innan 2003). Thus, if gene conversion formed the basis of such a haplotype pattern, multiple conversion events must be invoked, with some tracts of lengths <5 bp. Yet, the conversion-tract lengths have been estimated to range from 55 bp to 290 bp, through sperm-typing analyses (Jeffreys and May 2004).

In this view, an alternative and most likely scenario to explain our data is a demographic event such as ancient population structure. A number of studies have recently reported gene genealogies that present not only unexpectedly old coalescent times (2 MYA) but also long basal branches (Harris and Hey 1999; Webster et al. 2003; Barreiro et al. 2005; Garrigan et al. 2005; Hayakawa et al. 2005). Our observations at NAT1, together with these studies, further support the view that some diversity in the genome of modern humans may have persisted from a structured ancestral population (Harding and McVean 2004). In addition, NAT1*11A appears to be absent in sub-Saharan Africa, since it was not detected in either our genotyping panel of 144 sub-Saharan Africans from distinct geographic locations or 600 African American individuals reported elsewhere (Upton et al. 2001). Therefore, the observation that the NAT1 gene tree is rooted in Eurasia questions the geographic location of such a structured ancestral population (Takahata et al. 2001). The origins of NAT1*11A could thus be placed either in sub-Saharan Africa, from where it must have subsequently disappeared, or in Eurasia. Should the latter be the case, the NAT1 gene tree is at odds with the commonly accepted replacement hypothesis (Lewin 1987) and is more parsimoniously explained by the occurrence of partial hybridization between modern humans expanding from Africa and preexisting hominids in Eurasia, as recently sustained by the RRM2P4 locus (Garrigan et al. 2005). However, such inferences require further support from the analyses of multiple independent loci in increased numbers of samples and human populations.

And all this from some cooked meat genes.

References:

Patin E et al. 2006. Deciphering the Ancient and Complex Evolutionary History of Human Arylamine {N}-Acetyltransferase Genes. Am J Hum Genet (online early) Full text

Last year, Stedman et al. (2004) presented an analysis of the evolution of the MYH16 gene in humans, which concluded that a mutation deactivating the gene was fixed in the human lineage around 2.4 million years ago. An accompanying editorial by Pete Currie summarizes the story spun from this mutation:

The particular gene in question, MYH16, is specifically expressed in the jaw muscles of humans and monkeys. But, surprisingly, a mutation in the human gene prevents the accumulation of MYH16 protein. Stedman et al. found that, by contrast, all non-human primates for which genome sequence could be obtained have an intact copy of the gene, and have a high level of MYH16 protein in their jaw muscles. An analysis of the time at which the mutation arose during hominid evolution places it at about 2.4 million years ago, the period just before the evolution of the modern hominid cranial form. These findings suggest a seductive hypothesis: that a decrease in jaw-muscle size, produced by inactivation of MYH16, removed a barrier to the remodelling of the hominid cranium which consequently allowed an increase in the size of the brain (Currie 2004:373).

Two essential facts suggest the hypothesis that MYH16 evolved in association with the appearance of Homo: the estimated date for the frameshift mutation is 2.4 million years ago, and the gene is transcribed only in the muscles of the head, "specifically those derived from the embryonic first pharyngeal arch, including temporalis and tenso veli palatini."

Since then, some question has arisen about the date.

Paleoanthropology has a strange relationship with dates. On the one hand, new dates for fossils or archaeological sites are often put to rigorous criticism. We are rightly critical of dates, because they are so important to putting our evidence into sequence. Dates have power.

On the other hand, two different things having the same date are "seductive". In paleoanthropology, mere coincidence may always be a possibility, but it doesn't drive any headlines. Same date, same cause.

Of course, no dates from the past are really the same. They just have overlapping confidence intervals. And few things are worse for the estimation of confidence intervals than genes. Stedman et al. (2004) gave the MYH16 deactivating mutation a confidence interval of +/- 300,000 years. Anywhere in that range of dates is potentially associated with the appearance of Homo, since we really don't know when Homo originated, more specifically than between around 3 million and 2 million years ago. The "seductive" part of the hypothesis is that the mean date estimate for the gene, 2.4 million years, is the same as the estimate for AL 666-1, which is a plausible candidate for the first fossil evidence of Homo. But the date doesn't have to be the same for the gene and genus to be associated -- there is much uncertainty about both.

To some extent, this begs the question about dates in paleoanthropology. Two things that are plausibly causally associated might still be as much as several hundred thousand years different in dates. So how are we to resist the hypothesis that two events with the same date are causally associated? We may never confirm the hypothesis that two events actually do have the same date -- there is no statistical test for "significantly the same", just "not significantly different".

There are two ways to test the hypothesis that two events are causally related. One is to show that the causal link is impossible. In the case of MYH16, the proposed causal link makes a lot of sense, at least with respect to jaw muscle function.

The other test is to show that the dates really are significantly different. For MYH16, that is precisely the approach taken by Perry et al. (2005):

We describe the pattern of molecular evolution at a sarcomeric myosin gene, MYH16, using more than 30,000 bp of exon and intron sequence data from the chimpanzee and human genome sequencing projects to evaluate the timing and consequences of a human lineageÐspecific frameshift deletion. We estimate the age of the deletion at approximately 5.3 MYA. This estimate is consistent with the time of human and chimpanzee divergence and is significantly older than the first appearance of the genus Homo in the fossil record. We also find conflicting estimates of nonsynonymous fixation rates (dN) across different regions of this gene, revealing a complex pattern inconsistent with a simple model of pseudogene evolution for human MYH16.

The date estimate here comes from an assumption about what happens when the gene is deactivated. The downstream part of the gene was no longer functional after the frameshift deletion mutation happened. It should have evolved neutrally after the mutation, but not before. And Perry et al. found that there was only one nonsynonymous substitution on the chimpanzee lineage, but 16 on the human lineage. The reason the human lineage has more is assumed to be the absence of purifying selection against these substitutions in the period of time after the deletion.

The supplementary information for Stedman et al. (2004) puts the logic as thus:

Briefly, the assumption is made that non-synonymous mutations are selected against until the gene is inactivated, thereafter mutations at both synonymous and non-synonymous sites accumulate at the neutral mutation rate. Quantification of lineage-specific mutation rates at synonymous and non-synonymous sites remote from the inactivating deletion provides the information necessary for the calculation.

So to find the date of the deactivation, you assume that the substitution rate at synonymous and nonsynonymous sites after the deactivation was the same, and solve for the date that makes that ratio. The technique is simple, and was taken from Chao et al. (2002). That study used two different sources of evidence for dating the deactivation of the CMAH gene -- the gene sequence of the Alu insertion that deactivated it, and the number of nonsynonymous mutations in the newly-minted pseudogene. Both those approaches led to the same date. The latter approach -- the one used for the MYH16 gene also -- has no confidence interval. I may write more about that paper later, because it is interesting for several reasons, but at the moment it helps me very little.

You see, I have two questions that remain unanswered: (1) where does the confidence interval in Stedman et al. (2004) come from, and (2) what factors of uncertainty does that confidence interval leave out?

As far as where the confidence interval comes from, I'm afraid I am left with no clue. Neither the paper nor the supplementary information of Stedman et al. (2004) tell how a confidence interval on this estimate is derived, other than citing Chao et al. (2002), who don't report a confidence interval at all for this method.

Now as far as the second question, I'm wondering where the additional uncertainty may be in the estimate, because the estimate given by Perry et al. (2005) is so different. Consider:

Based on a 6-Myr divergence of the human-chimpanzee lineages (Haile-Selassie 2001; Brunet et al. 2002) and 15 nonsynonymous human lineage substitutions, we estimate the age of the exon 18 deletion at 5.3 ± 1.0 MYA. Similar to Stedman et al. (2004), our confidence interval incorporates standard errors involving a 5 to 7 MYA range for human-chimpanzee lineage divergence as well as the genome-wide estimate of human-chimpanzee silent site nucleotide divergence (Yi, Ellsworth, and Li 2002). This age estimate is not only outside the confidence interval of the 2.4 ± 0.3 MYA estimate obtained by Stedman et al. (2004) and significantly older than the first appearance of Homo in the fossil record but also consistent with an origin around the time that human and chimpanzee lineages diverged (Perry et al. 2005, emphasis added).

Reading this another way -- the "confidence interval" in the first analysis did not actually include all the uncertainty in the estimate. If it had included all the uncertainty, then the confidence interval should have been so wide as to include the later estimate, based on "better" data. So the true range of error was actually much larger than reported.

This is a major underestimated problem with associating any event with genetic changes. Nobody ever reports estimates of confidence intervals that account for these kinds of sampling errors. It's rare enough that we get any kind of confidence interval at all. For the most part, geneticists just don't know what the error from sampling could possibly be for any given dataset. There are just too many factors that might affect it, from population structure to the recombination rate to the timing of selection.

What about the estimate given by Perry et al. (2005). Is it right? Is its confidence interval accurate? At least as far as the confidence interval is concerned, the paper spells out what is included:

Similar to Stedman et al. (2004), our confidence interval incorporates standard errors involving a 5 to 7 MYA range for human-chimpanzee lineage divergence as well as the genome-wide estimate of human-chimpanzee silent site nucleotide divergence (Yi, Ellsworth, and Li 2002).

In other words, the 1 million years on either way is a safety margin based on the fact that the estimate of human-chimpanzee divergence date has a million years of uncertainty either way. Other sources of uncertainty, such as the stochastic nature of drift, or possible error in the assumption that distant silent sites and downstream nonsynonymous sites have the same mutation rate, etc., are not included.

I'm bothered by the functional part of Stedman et al. (2004), though. If this gene was deactivated in hominids 5.3 million years ago, and the gene is only expressed in muscles of the skull, including temporalis, then why did hominids get massively larger jaw muscles starting after 5.3 million years ago?

I'm waiting to be seduced by some explanation here. Anyone?

References:

Chao H-H. et al. 2002. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Nat Acad Sci USA 99:11736-11741. Full text (free)

Currie P. 2004. Muscling in on hominid evolution. Nature 428:373-374. Full text (subscription)

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Discovery News has an article summarizing some of Peter Ungar's recent work on tooth anatomy and wear in early Homo.

The study suggests Homo habilis, which some researchers have nicknamed "the handy man" because this species made the first known stone tools, was more of a fruit and veg eater than the apparent omnivore Homo erectus.

Teeth for the latter had greater numbers of pits, while handy habilis teeth had more striations suggestive of pulling down on fruit and leaves.

"Both of the species would probably have focused on high energy-yield, easy-to-consume foods, such as soft fruits when they could get them," Ungar told Discovery News. "The differences between H. habilis and H. erectus suggest that the latter may have focused a bit more on tough foods. They could have been meat, tough tubers or other items."

This is the most-studied dietary transition in human evolution, and it looks like the answers are getting more solid.

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