title: 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 long-period 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-specific time dependency of striae of Retzius formation. We conclude by contextualizing our morphological research with a current understanding of autonomic regulatory control of the skeleton and body mass, suggesting a central contribution to the coordination of organismal life history and body mass.
authors.affiliation: Departments of Biomaterials and Biomimetics and Basic Science and Craniofacial Biology, New York University College of Dentistry, New York, NY 10010, USA. tim.bromage@nyu.edu
authors.forename: Timothy G
authors.initials: TG
authors.lastname: Bromage
authors.forename: Rodrigo S
authors.initials: RS
authors.lastname: Lacruz
authors.forename: Russell
authors.initials: R
authors.lastname: Hogg
authors.forename: Haviva M
authors.initials: HM
authors.lastname: Goldman
authors.forename: Shannon C
authors.initials: SC
authors.lastname: McFarlin
authors.forename: Johanna
authors.initials: J
authors.lastname: Warshaw
authors.forename: Wendy
authors.initials: W
authors.lastname: Dirks
authors.forename: Alejandro
authors.initials: A
authors.lastname: Perez-Ochoa
authors.forename: Igor
authors.initials: I
authors.lastname: Smolyar
authors.forename: Donald H
authors.initials: DH
authors.lastname: Enlow
authors.forename: Alan
authors.initials: A
authors.lastname: Boyde
mesh_terms: D000818:Animals; D005075:Biological Evolution; D015992:Body Mass Index; D015519:Bone Density / Q000502:physiology; D001846:Bone Development / Q000502:physiology*; D001842:Bone and Bones / Q000166:cytology / Q000502:physiology*; D049109:Cell Proliferation; D003743:Dental Enamel / Q000166:cytology / Q000254:growth & development*; D015186:Hominidae / Q000033:anatomy & histology / Q000254:growth & development; D006801:Humans; D008136:Longevity / Q000502:physiology; D008322:Mammals / Q000033:anatomy & histology / Q000254:growth & development*; D010011:Osteocytes / Q000166:cytology / Q000502:physiology; D010507:Periodicity; D010802:Phylogeny; D011323:Primates / Q000033:anatomy & histology / Q000254:growth & development; D051381:Rats; D013045:Species Specificity; D014070:Tooth / Q000166:cytology / Q000254:growth & development*