Endochondral ossification and the evolution of limb proportions. (29th January 2020)

• Record Type: Journal Article
• Authors: Rolian, Campbell
• Is Part Of: Wiley interdisciplinary reviews. Volume 9:Number 4(2020)
• Page Start: n/a
• Page End: n/a
• Publication Date: 2020-01-29
• Subjects: chondrocytes -- endochondral ossification -- growth plates -- limb proportions -- skeletal allometry; Developmental biology -- Periodicals; 571.805
• DOI: 10.1002/wdev.373
• Languages: English
• ISSNs: 1759-7684

Abstract

Abstract: Mammals have remarkably diverse limb proportions hypothesized to have evolved adaptively in the context of locomotion and other behaviors. Mechanistically, evolutionary diversity in limb proportions is the result of differential limb bone growth. Longitudinal limb bone growth is driven by the process of endochondral ossification, under the control of the growth plates. In growth plates, chondrocytes undergo a tightly orchestrated life cycle of proliferation, matrix production, hypertrophy, and cell death/transdifferentiation. This life cycle is highly conserved, both among the long bones of an individual, and among homologous bones of distantly related taxa, leading to a finite number of complementary cell mechanisms that can generate heritable phenotype variation in limb bone size and shape. The most important of these mechanisms are chondrocyte population size in chondrogenesis and in individual growth plates, proliferation rates, and hypertrophic chondrocyte size. Comparative evidence in mammals and birds suggests the existence of developmental biases that favor evolutionary changes in some of these cellular mechanisms over others in driving limb allometry. Specifically, chondrocyte population size may evolve more readily in response to selection than hypertrophic chondrocyte size, and extreme hypertrophy may be a rarer evolutionary phenomenon associated with highly specialized modes of locomotion in mammals (e.g., powered flight, ricochetal bipedal hopping). Physical and physiological constraints at multiple levels of biological organization may also have influenced the cell developmental mechanisms that have evolved to produce the highly diverse limb proportions in extant mammals. This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Comparative Development and Evolution > Regulation of Organ Diversity Comparative Development and Evolution > Organ System Comparisons Between Species Abstract : Contributions of chondrogenesis and endochondral ossification to adult limb proportions in two mammals with different modes of locomotion, the house mouse (top, Mus musculus ) and Seba's short‐tailed bat (bottom, Carollia perspicillata ). In early development, embryos are similar in size, though the bat hand plate (blue) is already larger than in the mouse. At matching fetal stages, the bat has a markedly longer third metacarpal (MC3, blue). The rapid fetal and postnatal elongation of the bat's MC3 is then driven by its growth plate chondrocytes, which are (a) more numerous, (b) dividing more frequently (black cells), and (c) hypertrophying to a much greater extent than in the mouse. Species differences in these three cellular parameters are the main drivers of diversity in mammalian limb bone size and shape. Bat embryo/fetus redrawn from Cretekos et al. (2005), adult bat skeleton redrawn from Cooper et al. (2012), with permission.