Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths

Abstract

Mammalian cervical count has been fixed at seven for more than 200 million years. The rare exceptions to this evolutionary constraint have intrigued anatomists since the time of Cuvier, but the developmental processes that generate them are unknown. Here we evaluate competing hypotheses for the evolutionary origin of cervical variants in Bradypus and Choloepus, tree sloths that have broken the seven cervical vertebrae barrier independently and in opposite directions. Transitional and mediolaterally disjunct anatomy characterizes the cervicothoracic vertebral boundary in each genus, although polarities are reversed. The thoracolumbar, lumbosacral, and sacrocaudal boundaries are also disrupted, and are more extreme in individuals with more extreme cervical counts. Hypotheses of homologous, homeotic, meristic, or associational transformations of traditional vertebral column anatomy are not supported by these data. We identify global homeotic repatterning of abaxial relative to primaxial mesodermal derivatives as the origin of the anomalous cervical counts of tree sloths. This interpretation emphasizes the strong resistance of the "rule of seven" to evolutionary change, as morphological stasis has been maintained primaxially coincident with the generation of a functionally longer (Bradypus) or shorter (Choloepus) neck.