Epigenetic mechanical factors in the evolution of long bone epiphyses

Abstract

In developing vertebrate long bones in which endochondral ossification occurs, it is preceded or accompanied by perichondral ossification. The speed and extent ofperichondral apposition relative to endochondral ossification varies in different taxa. Perichondral ossification dominates early long bone development in extinct basal tetrapods and dinosaurs, extant bony fish, amphibians, and birds. In mammals and lizards, perichondral and endochondral ossification proceed more synchronously. One of the most important epigenetic factors in skeletogenesis is mechanical loading caused by muscle contractions which begin in u t m or in ouo. It has been previously shown that the stress distributions created perinatally in the chondroepiphysis during human skeletal development can influence the appearance of secondary ossification centres. Using finite element computer models representing bones near birth or hatching, we demonstrate that in vertebrates in which perichondral ossification significantly precedes endochondral ossification, the distribution of mechanical stresses in the ossifying cartilage anlagen tends to inhibit the appearance of secondary ossification centres in the ends of long bones. In models representing vertebrates in which endochondral ossification keeps pace with perichondral apposition, the appearance of secondary centres is promoted. The appearance of secondary centres leads to the formation of bony epiphyses and growth plates, which are most common in mammals and extant lizards. We postulate that genotypic factors influencing the relative speed and extent of perichondral and endochondral ossification interact with mechanical epigenetic factors early in development to account for many of the morphological differences observed in vertebrate skeletons.

Postnatal development of the largest subterranean mammal (Bathyergus suillus): Morphology, osteogenesis, and modularity of the appendicular skeleton

“…The effects of prenatal muscle kinesis in Bathyergus, as well as in many other subterranean species are almost completely unknown, and it may have an important impact on the normal development of epiphyses and joints such as the biepicondylar breadth, even when these regions are still chondroepiphyses. 93,94 Similarly, epicondyles are regions directly associated with sites for muscle and tendon attachment, thus receiving direct biomechanical stimulation as compared to regions without it (eg, diaphysis). Differences in load bearing stresses experienced at early perinatal stages also may contribute to the development of such features.…”

Heterochrony and post‐natal growth in mammals – an examination of growth plates in limbs

“…Due to this compression and the movement of the joints, 'pressure epiphyses' are under hydrostatic and shear stresses (Serrano et al, 2011). Arkin & Katz (1956), Carter & Wong (1988), Carter et al (1991Carter et al ( , 1998 found that these stresses decrease the rate of epiphyseal cartilage growth. 'Traction epiphyses' provide attachment for tendons and muscles and are subject to lateral stresses and tension (Parsons, 1904;Serrano et al, 2011).…”

“…The secondary ossification centres are usually tied to the evolution of determinate growth. Calcified and bony epiphyses evolved several times independently in many vertebrate lineages: Teleostei, Anura, Lepidosauria, Theria and possibly Aves (Haines, 1942;Carter et al, 1998). Although bony epiphyses have been reported in some kannemeyeriid dicynodonts, a group of nonmammaliaform synapsids (Walter, 1985), the lack of secondary ossification centres was hypothesized to be the plesiomorphic condition in cynodonts and mammaliaforms (Luo et al, 2007).…”

Anatomy, morphology and evolution of the patella in squamate lizards and tuatara (Sphenodon punctatus)

“…There is reason to expect a patella in Sphenodon. Like the patella, secondary epiphyseal ossification centres have also evolved on repeated occasions, and generally appear to cooccur with sesamoids in many groups (Sarin et al 1999), suggesting that these two features are linked by some yet obscure developmental mechanism (Carter et al 1998). Non-avian dinosaurs, crocodiles, turtles and salamanders lack ossified epiphyses and sesamoids (though they may have cartilaginous sesamoid structures, e.g.…”