Neandertal tooth development and somatic development

Roberto Macchiarelli and colleagues (2006, link) have published data regarding molar crown formation times in Neandertals. Here is their abstract:

Growth and development are both fundamental components of demographic structure and life history strategy. Together with information about developmental timing they ultimately contribute to a better understanding of Neanderthal extinction. Primate molar tooth development tracks the pace of life history evolution most closely, and tooth histology reveals a record of birth as well as the timing of crown and root growth. High-resolution micro-computed tomography now allows us to image complex structures and uncover subtle differences in adult tooth morphology that are determined early in embryonic development. Here we show that the timing of molar crown and root completion in Neanderthals matches those known for modern humans but that a more complex enamel-dentine junction morphology and a late peak in root extension rate sets them apart. Previous predictions about Neanderthal growth, based only on anterior tooth surfaces, were necessarily speculative. These data are the first on internal molar microstructure; they firmly place key Neanderthal life history variables within those known for modern humans.

The ScienceNOW article by Ann Gibbons stresses the fact that the study involves sectioned teeth instead of external perikymata counts. The result is a lack of any significant difference between the timing and duration of crown formation compared to modern humans:

When the researchers sliced thin sections of the molars, they noticed important similarities between Neandertals and modern humans. The dark birth line emerged at about the same time in dental development as in modern humans, indicating that Neandertal teeth developed at the same rate as modern human teeth do around the time of birth, the team reports online today in Nature. The researchers also found that the crowns and roots of the Neandertals grew at the same rate of those of modern humans, with root growth complete by age 9 as in modern children. "This all points to a dental developmental schedule that was most like that in modern humans," says anatomist and lead author Christopher Dean of University College London, who also is a dentist.

The tooth development story is becoming a bit complicated to follow. As applied to Neandertals, Guatelli-Steinberg and colleagues (2005), and Ramirez Rossi and Bermudez de Castro (2004) assessed dental maturation rates from anterior teeth (incisors and canines), while the current paper by Macchiarelli and colleagues (2006) is about molar development. Additionally Dean and colleagues (2001) examined early Homo and Australopithecus samples, and Ramirez Rossi and Bermudez de Castro also considered earlier Spanish Homo samples.

The notable finding by Guatelli-Steinberg and colleagues (2005) was that modern human samples are themselves hugely variable in their enamel formation times -- at least, as interpreted through enamel tissue characters. This is a very serious problem for interpreting any past population characteristics, because in fact the variation among modern sample means -- without even considering the within-sample variation -- encompasses most fossil samples of Homo and many australopithecines as well.

Here's what I wrote about this last year:

[T]he Neandertals are far from the most interesting part of this perikymata problem. Can we tell a human from an australopithecine from these data? If so, why do some of the earliest humans have the lowest (i.e. sub-australopithecine) counts?

The early human specimen that stood out (considering their anterior dentition) was KNM-ER 15000, and it is not clear from the available papers whether it is actually outside the extant modern sample ranges. Otherwise, early Homo specimens are entirely humanlike in their crown formation times, and this observation is confirmed by Macchiarelli and colleagues' present work on Neandertal molars.

In short, early Homo enamel formation times (and for that matter, non-robust australopithecines) fall entirely within the range of variation of living humans, with most specimens within the range of human population means.

The null hypothesis in this case is that enamel formation times did not differ between fossil and living humans. That hypothesis is not refuted by the available data -- and given the wide variation in enamel formation times among living human populations, it seems likely that further sampling of fossil Homo will arrive at the same result. The issue is not sample size for the fossils, in other words, it is the intrinsic variability among living people, which remains unexplained.

The variation among living humans raises a thornier problem, also. The reason why many people are interested in molar enamel deposition is the idea that enamel formation is linked to somatic maturation in general. But the great variability in enamel formation times in recent humans would seem to disprove a strong link between somatic and dental maturation.

The idea that somatic and dental maturation rates should be tightly linked comes mainly from interspecific comparisons. For example, Ramirez Rossi and Bermudez de Castro (2004:938) draw out the following logic:

Dental growth is a good proxy for the overall rate of maturation in a species (Smith 1989). Short crown formation time in fossil Homo species therefore indicates that somatic development was not as long as in H. sapiens. Importantly, Neanderthals apparently also had a faster pace of somatic development than their ancestor, H. heidelbergensis.
...
A prolonged life-history in hominids has previously been related to a reduction in the mortality rate of adults, and in turn low mortality rates have in the past been associated with an increase in brain size. Metabolic rate has also been linked to brain growth and has been implicated as a primary determinant of variation in life history. However, developmental changes are most probably related to fundamental changes in the timing and frequency of reproduction. Results presented here suggest that brain growth and brain size are not primary determinants of life-history re-scheduling in hominids; rather, it seems that high adult mortality rates are most likely to have driven such rescheduling among Neanderthals. A clearer picture of Neanderthals emerges here--as a species of Homo adapted to particular environmental conditions, when a high-calorie diet and a high metabolic rate were able to fuel fast somatic growth, as well as to grow and sustain a large brain.

This last conclusion was rejected by Guatelli-Steinberg et al. (2005) -- after all, their data showed that Neandertals didn't have short enamel development compared to living Africans.

And reflecting on the balance of data from Neandertals, an especially rapid rate of development seems quite implausible. For instance, if Neandertals had no problem fueling a 3000-5000 kcal per day energy expenditure, then why did their kids have so many enamel hypoplasias? If Neandertals had a limitless tap of food to enable their rapid somatic development, then what killed them so young?

Guatelli-Steinberg et al. (2005) posit that dental development does not provide an adequate correlate of somatic maturation, and suggest that adult brain size makes a better yardstick:

It has also been suggested that if Neandertals suffered high adult mortality rates, then they might be expected to have had abbreviated periods of childhood growth (10, 15). Adult mortality rates directly select for the timing of maturation across mammals; a larger risk of dying selects for rapid maturation (9, 30, 31). However, Smith (32) notes that if Neandertals had accelerated life histories, then this would leave them with a "peculiar" relationship between brain size and maturation, "two variables that are rarely of step [sic]." Because large brains require extended periods of childhood growth (1-7, 33), the presence of large brains in Neandertals suggests that their adult mortality risks were not high enough to have prevented them from evolving prolonged growth periods.

The logic is that a given adult brain volume is linked to maturation schedule because of learning. Crudely, a larger brain takes longer to fill with information. Or more properly (in causal terms), selection for more information processing tends to increase brain size (relative to body size), information processing ability is constrained by learning, so that brain size is correlated to maturation schedule by indirect causal mechanisms.

But I would question even this relationship. For one thing, it doesn't seem to work very well within a population. Or at least, not within the population of living humans, where variation in brain sizes show no clear relationship to skeletal maturation schedules. For another, brain sizes have shrunk in recent humans, but there is no particular evidence that maturation times have reduced, or that humans have less to learn. Some of the smaller brain sizes may be explained by smaller body size, but smaller body size also ought to be correlated with faster maturation.

It seems to me that comparing Neandertals to living people for developmental rates is misleading. Living people are different from other primates in their very low rates of adult mortality (and consequent long period of post-reproductive senescence). And we know that Neandertals were more similar to other primates in this respect: they died younger than humans. But that isn't a new development in Neandertals -- instead, the long lifespans typical of recent people are the new development.

There has as yet been little integration of the literature on human growth with these fossil-related questions. For instance, many nutritionally-limited human populations respond by delaying growth. Sometimes such delays can be resolved by rapid growth later in development, sometimes they lead to reductions in adult body size. This kind of plasticity in growth schedules and ultimate body size ought to have characterized ancient humans, which would have increased their variability (in both maturation schedule and adult body size) compared to any single living human population.

References:

Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Nat Acad Sci USA 102:14197-14202. Abstract

Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628-631.

Macchiarelli R, Bondioli L, Debénath A, Mazurier A, Tournepiche J-F, Birch W, Dean C. 2006. How Neanderthal teeth grew. Nature (early online) DOI link

Ramirez Rossi FV, Bermudez de Castro JM. 2004. Surprisingly rapid growth in Neanderthals. Nature 428:936-939. Full text (subscription)