Lamellar Bone is an Incremental Tissue Reconciling Enamel Rhythms, Body Size, and Organismal Life History

Abstract

Mammalian enamel formation is periodic, including fluctuations attributable to the daily biological clock as well as longer-period oscillations that enigmatically correlate with body mass. Because the scaling of bone mass to body mass is an axiom of vertebrate hard tissue biology, we consider that long-period enamel formation rhythms may reflect corresponding and heretofore unrecognized rhythms in bone growth. The principal aim of this study is to seek a rhythm in bone growth demonstrably related to enamel oscillatory development. Our analytical approach is based in morphology, using a variety of hard tissue microscopy techniques. We first ascertain the relationship among longperiod enamel rhythms, the striae of Retzius, and body mass using a large sample of mammalian taxa. In addition, we test whether osteocyte lacuna density (a surrogate for rates of cell proliferation) in bone is correlated with mammalian body mass. Finally, using fluorescently labeled developing bone tissues, we investigate whether the bone lamella, a fundamental microanatomical unit of bone, relates to rhythmic enamel growth increments. Our results confirm a positive correlation between long-period enamel rhythms and body mass and a negative correlation between osteocyte density and body mass. We also confirm that lamellar bone is an incremental tissue, one lamella formed in the species-

Enamel-Calibrated Lamellar Bone Reveals Long Period Growth Rate Variability in Humans

“…Previously we observed a circa 28-day rhythm in lamellar bone growth from an early human ancestor [Bromage et al, 2009], a result that we also obtained in preliminary analyses of a human female of Anglo-Celtic origin living in Melbourne, Australia (results not reported here). In the present study of humans of Bantu origin, for the first time we have observed striking lamellar growth rate rhythms revealing heretofore unknown cycles at various length scales.…”

“…Species variability in the RI reflects a statistically significant and positive relationship with body size explained by the discovery that the period responsible for RI formation is one and the same as that required to form one increment of bone, i.e. the lamella, which is the fundamental -if not archetypal -unit of bone [Bromage et al, 2009]. Lamellae of known formation time nevertheless vary in width and thus provide time-calibrated growth rate variability.…”

“…Fortunately, the possibility now exists to assign a time scale to lamellar bone using calibrated enamel increments that, in mammalian teeth, exhibit incremental features representing successive forming fronts of enamel at varying time scales [Bromage et al, 2009]. There exists a daily period which, by light microscopy, is recognized as a 'cross striation', and there is a long period, i.e.…”

The Havers-Halberg oscillation regulates primate tissue and organ masses across the life-history continuum

“…The pattern of body sizedependent and -independent characteristics aligns with hypothalamic controls over anterior and posterior pituitary function, respectively, suggesting that long period biological timing is fundamental to a metabolism-mediated regulation of primate life history (Bromage et al, 2012). Given this key role, we termed this period the Havers-Halberg oscillation (HHO) (Bromage et al, 2009), in reference to Clopton Havers, a 17th Century hard tissue anatomist (Havers, 1691), and Franz Halberg, a long-time explorer of long-period rhythms (Halberg et al, 1965).…”

“…In the search for proximate mechanisms, it has been shown that long period biological timing, as deduced from the enamel formation rhythms evident in its microanatomy, varies predictably with body size (Bromage et al, 2009). Although it is well known that the enamel structure of primates (and many other mammals) manifests as a daily developmental event, a previously enigmatic long period rhythm is also visible, known as the stria of Retzius.…”