Russell T. Hogg

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

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.

Primate enamel evinces long period biological timing and regulation of life history

The factor(s) regulating the combination of traits that define the overall life history matrix of mammalian species, comprising attributes such as brain and body weight, age at sexual maturity, lifespan and others, remains a complete mystery. The principal objectives of the present research are (1) to provide evidence for a key variable effecting life history integration and (2) to provide a model for how one would go about investigating the metabolic mechanisms responsible for this rhythm. We suggest here that a biological rhythm with a period greater than the circadian rhythm is responsible for observed variation in primate life history. Evidence for this rhythm derives from studies of tooth enamel formation. Enamel contains an enigmatic periodicity in its microstructure called the striae of Retzius, which develops at species specific intervals in units of whole days. We refer to this enamel rhythm as the repeat interval (RI). For primates, we identify statistically significant relationships between RI and all common life history traits. Importantly, RI also correlates with basal and specific metabolic rates. With the exception of estrous cyclicity, all relationships share a dependence upon body mass. This dependence on body mass informs us that some aspect of metabolism is responsible for periodic energy allocations at RI timescales, regulating cell proliferation rates and growth, thus controlling the pace, patterning, and co-variation of life history traits. Estrous cyclicity relates to the long period rhythm in a body mass-independent manner. The mass-dependency and -independency of life history relationships with RI periodicity align with hypothalamic-mediated neurosecretory anterior and posterior pituitary outputs. We term this period the Havers-Halberg Oscillation (HHO), in reference to Clopton Havers, a 17th Century hard tissue anatomist, and Franz Halberg, a long-time explorer of long-period rhythms. We propose a mathematical model that may help elucidate the underlying physiological mechanism responsible for the HHO.

Lemur Biorhythms and Life History Evolution

Skeletal histology supports the hypothesis that primate life histories are regulated by a neuroendocrine rhythm, the Havers-Halberg Oscillation (HHO). Interestingly, subfossil lemurs are outliers in HHO scaling relationships that have been discovered for haplorhine primates and other mammals. We present new data to determine whether these species represent the general lemur or strepsirrhine condition and to inform models about neuroendocrine-mediated life history evolution. We gathered the largest sample to date of HHO data from histological sections of primate teeth (including the subfossil lemurs) to assess the relationship of these chronobiological measures with life history-related variables including body mass, brain size, age at first female reproduction, and activity level. For anthropoids, these variables show strong correlations with HHO conforming to predictions, though body mass and endocranial volume are strongly correlated with HHO periodicity in this group. However, lemurs (possibly excepting Daubentonia) do not follow this pattern and show markedly less variability in HHO periodicity and lower correlation coefficients and slopes. Moreover, body mass is uncorrelated, and brain size and activity levels are more strongly correlated with HHO periodicity in these animals. We argue that lemurs evolved this pattern due to selection for risk-averse life histories driven by the unpredictability of the environment in Madagascar. These results reinforce the idea that HHO influences life history evolution differently in response to specific ecological selection regimes.

Life‐History Correlates of Enamel Microstructure in Cebidae (Platyrrhini, Primates)

Previous studies have examined tooth eruption as it relates intrinsically to body mass, brain mass, and other life history variables, and extrinsically to ecological factors (e.g., age at foraging independence, environmental risk aversion, and maternal investment). Different models have been explored wherein each of these variables impacts ontogeny. However, anthropoid and strepsirhine primates exhibit interesting differences in the relationships of these ecological and life history variables with tooth eruption. Moreover, interactions between ecological variables and dental tissue growth have only been explored in the lemurs. This study examines dental microstructure of the New World monkey family, Cebidae, to provide further insight into forces influencing the evolution of primate dental ontogeny. The Cebidae were chosen because they are a diverse group which is distinct in ecology and phylogeny from the better known catarrhines of the Old World. Using phylogenetic generalized least squares analyses (PGLS), we test whether brain mass, body mass, or the three above‐mentioned ecological variables have stronger correlations with enamel growth. Results show that ecological factors have stronger relationships with cebid dental growth rates than brain or body mass. Foraging independence has the most impact on overall enamel growth as it has the strongest correlation with enamel extension rates. However, another estimate of enamel growth, rate of secretion, has the highest correlation with maternal investment. Our results suggest that an overarching ecological model encompassing the three current ecological hypotheses is needed to further understand the evolution of dental ontogeny within primates. Anat Rec,, 2011.

Histology of dental long-period biorhythms in Canis familiaris

Our objective is to assess variation in Havers–Halberg oscillation (HHO) periodicities among domestic dogs (Canis familiaris). The HHO is hypothesized to be a hypothalamic‐generated biorhythm coordinating multiple life history variables including body mass and lifespan. Dogs have a broad mass range spanning two orders of magnitude, but this variation has been shown to result from selection on very few genetic loci, and dogs have low variation in other life history traits. Therefore, we predict that HHO variation will not be correlated to body mass among domestic dogs, as it is in anthropoid primates. To test the prediction, we examined dog HHO periodicity via manifestations in tooth enamel and dentine, quantifying HHO rhythm histologically. HHO rhythm is reflected in teeth as the number of days between secretion of successive striae of Retzius (enamel) and Andresen lines (dentine), a value referred to as Retzius periodicity (RP). We counted ca. 24‐h growth lines between successive Retzius and Andresen lines to determine RP in histological thin‐sections from canine teeth of 19 dogs, representing different breeds and sizes. To test our hypothesis, we regressed RP periodicity against body mass data. Dogs have low RP variation for their body mass range, with a modal periodicity of 5 days and a range of 4–6 days. RP was not significantly correlated with body mass. We conclude that mass variation in dogs does not seem driven by HHO physiology, consistent with findings that IGF1 variants produce dog mass variation. However, low RP (and by extension HHO) variation is consistent with low variation in dog lifespan and gestation, suggesting that dog life history may still be governed by HHO mechanisms even if body mass does not reflect this.