Enamel biorhythms of humans and great apes: the Havers-Halberg Oscillation hypothesis reconsidered

Abstract

The Havers-Halberg Oscillation (HHO) hypothesis links evidence for the timing of a biorhythm retained in permanent tooth enamel (Retzius periodicity) to adult body mass and life history traits across mammals. Potentially, these links provide a way to access life history of fossil species from teeth. Recently we assessed intra-specific predictions of the HHO on human children. We reported Retzius periodicity (RP) corresponded with enamel thickness, and cusp formation time, when calculated from isolated deciduous teeth. We proposed the biorhythm might not remain constant within an individual. Here, we test our findings. RP is compared between deciduous second and permanent first molars within the maxillae of four human children. Following this, we report the first RPs for deciduous teeth from modern great apes (n = 4), and compare these with new data for permanent teeth (n = 18) from these species, as well as with previously published values. We also explore RP in teeth that retain hypoplastic defects. Results show RP changed within the maxilla of each child, from thinner to thicker enameled molars, and from one side of a hypoplastic defect to the other. When considered alongside correlations between RP and cusp formation time, these observations provide further evidence that RP is associated with enamel growth processes and does not always remain constant within an individual. RP of 5 days for great ape deciduous teeth lay below the lowermost range of those from permanent teeth of modern orangutan and gorilla, and within the lowermost range of RPs from chimpanzee permanent teeth. Our data suggest associations between RP and enamel growth processes of humans might extend to great apes. These findings provide a new framework from which to develop the HHO hypothesis, which can incorporate enamel growth along with other physiological systems. Applications of the HHO to fossil teeth should avoid transferring RP between deciduous and permanent enamel, or including hypoplastic teeth.

Keywords: Retzius lines; biorhythms; enamel growth; life history.

Figure 1

Hypoplastic defect and Retzius periodicity (zoom in to see Retzius lines). (a) Human deciduous maxillary second molar mesio‐lingual enamel highlighted in grey. (b) The same region imaged using a polarizing lens. Dashed arrow points to a hypoplastic defect associated with an accentuated marking. Magnification = 4×. (c) Blue arrow points to Retzius lines that formed before the hypoplastic defect. Magnification = 20×. (d) Blue arrow points to Retzius lines that formed after the hypoplastic defect. The stress event did not prevent secretory ameloblasts from recovering, as these cells had a functional Tomes process (separate rods are visible) that deposit enamel at a slightly accelerated rate.

Figure 2

Retzius periodicity in a juvenile orangutan lower second deciduous molar. (a) Retzius lines in cervical enamel. Magnification = 4×. (b) Daily cross‐striations. White arrows point to the first and last cross‐striation between two adjacent Retzius lines (zoom in to see). Magnification = 20×. (c) Large white arrows point to the same two adjacent Retzius lines. Smaller white arrows point to cross‐striations, corresponding to 5 days of enamel secretion. Magnification = 60×.

Figure 3

Scatter plot of dm² Retzius periodicity against Retzius line spacing. There is a significant (P < 0.000) and positive correlation between the two variables.