4.3 Article

Bone remodeling in the longest living rodent, the naked mole-rat: Interelement variation and the effects of reproduction

Journal

JOURNAL OF ANATOMY
Volume 239, Issue 1, Pages 81-100

Publisher

WILEY
DOI: 10.1111/joa.13404

Keywords

Bone resorption; Female breeder; Haversian systems; Heterocephalus glaber; Secondary osteons; Secondary reconstruction

Funding

  1. Becas Chile, the Government of Chile (CONICYT) [72160463]
  2. National Research Foundation (NRF) (South Africa) [117716]
  3. SARChI chair of Mammalian Behavioural Ecology and Physiology from the DST-NRF South Africa [64756]

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The bone remodeling pattern of naked mole-rats, known for their low metabolic rates and long lifespans, was assessed in a study. Results showed slow bone turnover, with differences in remodeling between reproductive and non-reproductive individuals. This variation in skeletal homeostasis, especially in stylopodial elements, sheds light on the skeletal dynamics of mammals with low metabolic rates.
The pattern of bone remodeling of one of the most peculiar mammals in the world, the naked mole-rat (NMR), was assessed. NMRs are known for their long lifespans among rodents and for having low metabolic rates. We assessed long-term in vivo bone labeling of subordinate individuals, as well as the patterns of bone resorption and bone remodeling in a large sample including reproductive and non-reproductive individuals (n = 70). Over 268 undecalcified thin cross-sections from the midshaft of humerus, ulna, femur and tibia were analyzed with confocal fluorescence and polarized light microscopy. Fluorochrome analysis revealed low osteogenesis, scarce bone resorption and infrequent formation of secondary osteons (Haversian systems) (i.e., slow bone turnover), thus most likely reflecting the low metabolic rates of this species. Secondary osteons occurred regardless of reproductive status. However, considerable differences in the degree of bone remodeling were found between breeders and non-breeders. Pre-reproductive stages (subordinates) exhibited quite stable skeletal homeostasis and bone structure, although the attainment of sexual maturity and beginning of reproductive cycles in female breeders triggered a series of anabolic and catabolic processes that up-regulate bone turnover, most likely associated with the increased metabolic rates of reproduction. Furthermore, bone remodeling was more frequently found in stylopodial elements compared to zeugopodial elements. Despite the limited bone remodeling observed in NMRs, the variation in the pattern of skeletal homeostasis (interelement variation) reported here represents an important aspect to understand the skeletal dynamics of a small mammal with low metabolic rates. Given the relevance of the remodeling process among mammals, this study also permitted the comparison of such process with the well-documented histomorphology of extinct therapsids (i.e., mammalian precursors), thus evidencing that bone remodeling and its endocortical compartmentalization represent ancestral features among the lineage that gave rise to mammals. It is concluded that other factors associated with development (and not uniquely related to biomechanical loading) can also have an important role in the development of bone remodeling.

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