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Weaning in TEETH!

Written by: Katie Hinde, Ph.D. | Issue # 17 | 08 2013

  • When to wean? Humans wean early compared to our ape relatives.
  • Researchers are using a new technique to measure elements in teeth to track weaning.
  • The new method has been validated prospectively in humans and in monkeys.
  • Scientists have even used these new tools to study a fossil Neanderthal tooth.

Weaning in primates is a fascinating process in which ingestion of mother’s milk, as a proportion of daily dietary intake, incrementally declines as the infant ages. From moment to moment, this exquisite negotiation of nipple access between mother and infant can vary in relation to food availability, maternal style, and the compelling power of the infant demand (a.k.a. weaning tantrum). And lots of other factors can influence the weaning process, too.

One of the more remarkable features of human development is that cessation of breastfeeding occurs earlier for us than for our closest ape relatives. This is not just an artifact of a modern industrial world. In 2001, Dan Sellen reviewed >100 non-industrial populations using demographic and ethnographic records. The average age of the introduction of supplemental solids was estimated to be ~5 months (±4 months) and cessation of breastfeeding on average was estimated to be ~30 months (±10 months). Chimpanzees, one of our two closest living relatives, complete weaning ~55+ months (Kappeler & Pereira, 2003).

Our accelerated transition to foods other than mother’s milk is thought to have emerged in our ancestral history in part due to more cooperative infant care and access to a more nutritious diet (Reiches et al., 2009; Kramer and Ellison, 2010; Kaplan et al., 2000). Shorter lactation periods can translate into shorter interbirth intervals and higher reproductive rates. This has likely played a part in the relatively high lifetime fertility in humans compared to other apes, even before the advent of modern industrial food production. Note the slow reproductive rate of other great apes makes their populations especially vulnerable to deforestation and hunting; they just can’t recover faster than we can destroy.

Paleoanthropologists debate exactly when in our evolutionary history accelerated weaning emerged. For many decades, researchers have relied on tooth eruption schedules as a proxy for weaning. Unfortunately, more recent investigations of nursing behavior and tooth eruption in wild-living primates have revealed that these parameters do not necessarily occur together (Smith et al., 2013; Godfrey et al., 2003). Observations of nursing behavior aren’t a good proxy for milk transfer either because they tell you nothing about how much milk the infant is actually consuming (Cameron et al., 1999; Cameron, 1998). And toward the end of the weaning process, infants suckle during nighttime co-sleeping (when most primatologists are deservedly recovering from their daytime observations). For living primates, there may be opportunities to measure milk intake from poop samples, but further validation is needed (Reitsema, 2012).

Basically, as anthropologists, we have had a limited number of relatively weak proxies for investigating weaning in the living animals right in front of us, much less going to the fossil record to convincingly deduce when earlier infant weaning evolved in our hominin relatives. Maybe the signatures of early life dietary transitions could be found in teeth?! Many paleoanthropologists began looking for “isotopic biomarkers”–chemical elements laid down as tissue develops–of early life experiences in teeth…but there were some challenges.

A briefest history of elemental analysis in skeletal material

Back in the 1960s, scientists demonstrated that during the fossilization process, elements were readily exchanged between the dirt/rock and skeletons (e.g., Schroeder, 1969). This is known as diagenesis. And these diagenetic effects can obscure the natural accumulation of elements in tissue during the lifetime (biogenesis). Conventional wisdom (persisting today) was most effectively summarized by Johannes Schroeder: “these elements are not dependable for paleo-environmental analysis.”

Since then, new techniques, controls, and instrumentation have re-opened options for investigating dietary shifts in some particularly well-preserved fossils. We can do fancy-pants things like “high-resolution elemental analysis by laser ablation-inductively coupled plasma-mass spectrometry.” Dr. Louise Humphrey and colleagues used these methods to measure strontium, an alkaline earth metal, in the tooth enamel of humans and baboons to indicate dietary changes (Humphrey et al., 2008a, 2008b). Although they used species-typical estimated averages rather than prospectively following individual mother-infant dyads, these studies importantly opened previously abandoned avenues for studying dietary transitions in teeth.

But strontium seemed to have some minor drawbacks. Kohn and Moses, in an elegant experimental study, revealed that strontium was more susceptible to diagenetic alteration than was barium (2013). This meant that strontium had poor resolution over short time scales and would not be as useful to detect discrete time points for weaning transitions.

Back to the story…

We wanted to investigate strontium and barium prospectively in human and monkey enamel in relation to early life diet (Austin et al., 2013). In humans, teeth were collected along with daily journals of infant diet–breastmilk, formula, and solids. My long-term monkey milk study at the Comparative Lactation Lab in Human Evolutionary Biology at Harvard University and the California National Primate Research Center provided teeth, milk samples, and behavioral observations of infant suckling and solid food consumption. (Full disclosure, I am not a tooth histologist nor skilled in elemental analysis. I brought the macaque jazz to this cocktail party.)

We found that we could see the period of exclusive breastfeeding and the weaning process–down to nearly the day–by measuring barium concentrations in tooth enamel!

Using sophisticated analytical chemistry and microscopy techniques at the University of Sydney’s Faculty of Dentistry, the Elemental Bio-imaging Facility (University of Technology, Sydney) and the Dental Hard Tissue Laboratory (Harvard University, Cambridge, MA), we were able to track changes in barium concentration in teeth across time. Similar to the growth rings found in trees, teeth follow an incremental growth pattern that creates daily growth lines in enamel and dentine, which can be viewed and counted under the microscope.

When barium appears in the tooth lines, we know the infant has been born and is consuming milk since barium doesn’t appreciably cross the placenta. The barium levels increased toward peak lactation (as milk consumption increases) and then declined with the known introduction of supplemental solid foods. Importantly, barium levels in the monkey mothers’ milk were consistent with barium levels in monkey infants’ tooth enamel.

We then applied this technique to a single Neanderthal tooth found in Belgium dated to the Middle Paleolithic. The specimen was the wonderfully well-preserved Scladina juvenile. Other scientists have successfully recovered proteins and mitochondrial DNA from this individual (Nielson-Marsh et al., 2009; Orlando et al., 2006). Although these well-preserved features argue against diagenetic alteration, just to be sure we further investigated rare earth elements in the enamel. If diagenesis had appreciably altered the elemental structure of the tooth- creating a diagenetic “overprint” if you will–we would expect these rare earth elements to be enriched in the Neanderthal tooth. There was little evidence for diagenetic modification and none in the areas of the tooth in which we sampled barium (discussed ad nauseum in the supplemental information that accompanies the main paper)(Austin et al. 2013).

The barium pattern indicated the Neanderthal infant was exclusively breastfed for ~7 months before supplementation with non-milk foods over the following ~7 months. At ~1.2 years of age, there is evidence of an abrupt cessation of weaning. The pattern is the same as found in the macaque separated from its mother during infancy.

The Neanderthal infant survived this early life dietary shift, but the atypical, precipitous decline in barium levels strongly suggests there was some “insult” to the dyad that interrupted the normal, gradual weaning process. Maybe the mother died, became sick, or couldn’t sustain lactation. Maybe she went out foraging while a friend babysat her kid and then there was a flash flood and she was trapped on the other side of the river and in the five days it took the river to subside her milk dried up…there is no way to know. We speculated wildly over e-mail. We were appropriately more circumspect in publication.

The important take away

This one individual cannot be used to infer species-typical weaning patterns of Neanderthals. The precipitous decrease of barium at 1.2 years of age pretty clearly suggests that the Scladina Neanderthal was abruptly weaned in an atypical fashion. Primates aren’t hooded seals. Those guys have four days of mom providing milk and then on day five she abandons the unstable ice pack, returning to the sea from whence she came with hardly a “Go live off your blubber, buddy.” Instead, primates grow slowly, developing their big brains and complex social behavior over a long infancy.

But what we can confirm from these human, macaque, and Neanderthal data is the following. We have a really powerful way to investigate the period of exclusive milk feeding and the weaning process with high precision and resolution. For the first time we have a method to look at individual differences in these parameters in primates “collected” by old school naturalists gathering dust in natural history museums or skeletal material recovered at primate field sites. And we can do this in well-preserved fossil hominins…if colleagues are willing to share. That aggregation of data will allow us to establish the range of variation among individuals within species and from that, a better understanding of life history evolution among species.

References

1. Austin C, Smith TM, Bradman A, Hinde K, Joannes-Boyau R, Bishop D, Hare DJ et al. (2013) Barium distributions in teeth reveal early life dietary transitions in primates. Nature 498:216-219.

2. Cameron EZ (1998) Is suckling behaviour a useful predictor of milk intake? A review. Anim Behav 56:521-532.

3. Cameron EZ, Stafford KJ, Linklater WL, Veltman CJ. (1999) Suckling behaviour does not measure milk intake in horses, Equus caballus. Anim Behav 57:673-678.

4. Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. (2003) “Dental development and primate life histories.” in Primate life histories and socioecology, edited by Peter Kappeler & Michael Pereira, 177-203. Chicago: The University of Chicago Press, 2003.

5.Humphrey LT, Dean MC, Jeffries TE, Penn M. (2008b) Unlocking evidence of early diet from tooth enamel. Proc Natl Acad Sci USA 105:6834–6839.

6. Humphrey LT, Dirks W, Dean MC, Jeffries TE. (2008a) Tracking dietary transitions in weanling baboons (Papio hamadryas anubis) using strontium/calcium ratios in enamel. Folia Primatol (Basel) 79:197–212.

7. Kaplan H, Hill K, Lancaster J, Hurtado AM. (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evolutionary Anthropology Issues: News and Reviews 9: 156-185.

8. Kramer KL & Ellison PT. (2010) Pooled energy budgets: Resituating human energy‐allocation trade-offs. Evolutionary Anthropology: Issues, News, and Reviews 19:136-147.

9. Nielsen-Marsh CM, Stegemann C, Hoffmann R, Smith T, Feeney R, Toussaint M, Harvati K et al. (2009) Extraction and sequencing of human and Neanderthal mature enamel proteins using MALDI-TOF/TOF MS. J Archaeol Sci 36:1758–1763.

10. Orlando L, Darlu P, Toussaint M, Bonjean D, Otte M, Hanni C. (2006) Revisiting Neandertal diversity with a 100,000 year old mtDNA sequence. Curr Biol 16:R400–R402.

11. Reiches MW, Ellison PT, Lipson SF, Sharrock KC, Gardiner E, Duncan LG. (2009) Pooled energy budget and human life history. Am J Human Biol 21:421-429.

12. Reitsema LJ. (2012) Introducing fecal stable isotope analysis in primate weaning studies. Am J Primatol 74:926-939.

13. Schroeder JH. (1969) Experimental dissolution of calcium, magnesium, and strontium from recent biogenic carbonates: a model of diagenesis. Journal of Sedimentary Research 39:1057-1073.

14. Sellen DW (2001) Comparison of infant feeding patterns reported for nonindustrial populations with current recommendations. J Nutr 131: 2707-2715.

15. Sellen DW (2007) Evolution of infant and young child feeding: implications for contemporary public health. Annu Rev Nutr 27:123-148.

16. Smith TM, Machanda Z, Bernard AB, Donovan RM, Papakyrikos AM, Muller MN, Wrangham R. (2013) First molar eruption, weaning, and life history in living wild chimpanzees. Proc Natl Acad Sci USA 110:2787-2791.

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