Abstract
The patterns of bone modeling and mineral mobilization (skeletal homeostasis) among mammals other than humans and laboratory rodents are still poorly known. In this study we assessed the pattern of bone formation and bone resorption in the femur of a wild population of Cape dune molerats, Bathyergus suillus (n = 41) (Bathyergidae), a solitary subterranean mammal with a marked extended longevity among rodents, and which also lives in a naturally deficient state of vitamin D. In order to determine ontogenetic and sex effects on histomorphometric parameters of transversal undecalcified bone sections, two-way ANOVA, linear mixed-effects model and regression statistical analyses were performed. During ontogeny, B. suillus increased their cross sectional area, cortical area and cortical thickness, and most importantly, they showed scarce endosteal bone resorption which resulted in a retained medullary cavity size during ontogeny. This resulted in a positively imbalanced bone modeling, where bone formation considerably surpasses bone loss by almost 100-fold in adulthood. This differs markedly from other terrestrial mammals with relatively thin cortical walls. Regarding bone loss and remodeling, three main processes involving intracortical resorption were observed: modeling-related bone loss in early postnatal growth; secondary osteon formation occurring in both sexes; and subendosteal secondary reconstruction observed only in females. The latter is accompanied by females having six-fold more relative bone loss than males, which is evidenced by the development of enlarged resorption cavities (RCs) distributed circumferentially around the medullary cavity. Males have smaller, more circular and randomly distributed RCs. In general, our data indicate no age-related decline in mineral content in B. suillus, and provides strong support for a pattern of sexual dimorphism in skeletal homeostasis, similar to that occurring in humans and other mammals, with females losing more bone throughout aging as compared to males due to reproductive factors. Interestingly as well, despite the high mechanical loads experienced during burrow construction, bone remodeling in B. suillus is kept at very low levels throughout their lifespan, and dense Haversian tissue never forms. This study represents the first comprehensive assessment of skeletal homeostasis in a subterranean mammal, and it enables a better understanding of the complex processes governing the acquisition and maintenance of bone properties in this species with extraordinary fossorial adaptations.
Highlights
An important goal in bone research is to understand the interrelationship between mineral homeostasis and bone modeling dynamics
Box plots presented in this study show the following legend: (1) the dark horizontal line in the middle of the boxes is the median; (2) the boxes indicate the 25th and 75th percentile of the cases; (3) the T-bars that extend from the boxes are the whiskers, which represent 1.5 times the height of the box when data is available for bottom and top boxes; if no value exist in any of these ranges, it will represent the minimum or maximum values, respectively; (4) the points are outliers, and are defined as values that do not fall within the whiskers
This study shows that despite having subterranean lifestyles, with limited exposure to sunlight, Cape dune molerats (CDMs) have highly mineralized cortical walls with no evidence of bone diseases generally associated with vitamin D deficiency
Summary
An important goal in bone research is to understand the interrelationship between mineral homeostasis and bone modeling dynamics (i.e., uncoupled bone formation and resorption). The interaction between these processes and specific adaptations (e.g., reproductive and/or biomechanical) are relevant to understand how bone structure is maintained with aging (Yingling & Taylor, 2008; Lanyon, Sugiyama & Price, 2009; Macica et al, 2016). The patterns of mineral mobilization (skeletal homeostasis) and bone modeling in mammals have largely focused on humans, non-human primates and rodents (Duque & Watanabe, 2011; Allen & Burr, 2014). The rapid expansion of the medullary cavity typically observed during early ontogeny of surface-dwelling (terrestrial) mammals restricts the analysis of skeletal homeostatic dynamics, since most of the early deposited bone tissues are resorbed (Castanet, 2006)
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