Bone Rhythms Correspond to Enamel Periods and Reflect Life History

Dental and skeletal tissues share the characteristic that each is formed by cells that secrete an organic matrix, which is subsequently mineralized.  Mammalian enamel is a periodic incremental tissue, characterized to include a circadian rhythm visible as daily cross striations or varicosities and, in some mammals such as humans, to exhibit a near weekly incremental rhythm recognized as striae of Retzius.  These chronobiological rhythms have not been previously identified in bone. 

Objectives: Our aim is to discover whether dental incremental periodicities have corresponding rhythms in bone and, if so, to define their functional role in organismal life history.  Our hypothesis is that a hypothalamic autonomic clock is responsible for, amongst other life history features, the pace of development, bone/body mass, feeding behavior, and reproduction. 

Methods: Fluorescence, polarized, and scanning electron microscopy of histological thin sections derived from vitally labeled mammalian bones and teeth provided time-calibrated incremental microanatomy.  To evaluate their association with organismal life history, observed incremental rhythms were related to body size, a principal character governing taxon-specific life history.  

Results: With focus on living primates and extinct human ancestors, striae of Retzius were observed to vary continuously based on a daily rhythm, corresponding to body size; short repeat intervals (e.g. two daily cross striations between adjacent striae) correspond to small body size, and longer repeat intervals relating to larger body size (median eight-day repeat in modern humans).  The fundamental microanatomical unit of bone, the lamella, corresponded in duration to striae of Retzius, and thus a time-dependency related to body size during growth.  The relationship between osteocyte density in lamellar bone - a proxy for bone cell proliferation and formation rate - and body size is also confirmed. 

Conclusion: Bone is an incremental tissue, the lamellae of which correspond to a long term rhythm related to body size.  This rhythm is hypothesized to relate to leptin-mediated central control of bone/body mass via the autonomic nervous system.  Striae of Retzius are secondary to this systemic physiological control.  The evolution of organismal life history appears to result from natural selection operating on a hypothalamic autonomic clock.