Skeletal development in sloths and the evolution of mammalian vertebral patterning

Abstract

Mammals show a very low level of variation in vertebral count, particularly in the neck. Phenotypes exhibited at various stages during the development of the axial skeleton may play a key role in testing mechanisms recently proposed to explain this conservatism. Here, we provide osteogenetic data that identify developmental criteria with which to recognize cervical vs. noncervical vertebrae in mammals. Except for sloths, all mammals show the late ossification of the caudal-most centra in the neck after other centra and neural arches. In sloths with 8–10 ribless neck vertebrae, the caudal-most neck centra ossify early, matching the pattern observed in cranial thoracic vertebrae of other mammals. Accordingly, we interpret the ribless neck vertebrae of three-toed sloths caudal to V7 as thoracic based on our developmental criterion. Applied to the unusual vertebral phenotype of long-necked sloths, these data support the interpretation that elements of the axial skeleton with origins from distinct mesodermal tissues have repatterned over the course of evolution.

Tetrapod-like axial regionalization in an early ray-finned fish

“…As noted above, Tarrasius sits somewhere on the stem of living actinopterygii, actinopteri and/or neopterygii, nested clades that contain teleosts [28][29][30][31][32][33][34][35]. Under this scenario of shared regional identity, a tetrapod distribution of Hox domains would be ancestral for gnathostomes and osteichthyans by the rules of parsimony [11]. In contrast, axial patterning in model teleosts (figure 2f ) would be derived: the axis of Danio has far fewer trunk vertebrae than Tarrasius and many other bony fishes (figure 2g) [1,18,25].…”

“…Regions are deterministically patterned by expression of specific Hox genes during the development of all examined tetrapod [2][3][4][5][6][7][8]. This strong molecular-morphological relationship has been used to generate developmental hypotheses of body evolution and infer Hox expression from regional identity in fossil and living forms [2,4,[9][10][11][12][13]. Even the origin of the tetrapod body plan has been linked to clade-specific elongation of the trunk and related changes in the placement of nested Hox expression domains [9,13,14].…”

The Mammalian Cervical Vertebrae Blueprint Depends on theT(brachyury) Gene

“…The spontaneous VSD mutation in the bovine T gene is the first in vivo evidence for the hypothesis that the T protein is directly involved in the maintenance of the mammalian seven-cervical vertebra blueprint. It therefore furthers our knowledge of the T-protein function and early mammalian notochord development.KEYWORDS homeotic transformation; genetic defect; brachyury H IGH evolutionary diversification of the vertebral column exists in vertebrates, but the number of cervical vertebrae within mammals has been fixed at seven for .200 million years of evolution since the beginning of the long and wide mammalian radiation (Hautier et al 2010). The reason why all mammals share this fundamental blueprint of cervical vertebrae, compared with a more relaxed rule for the number of posterior vertebrae analogous to other nonmammalian vertebrates, remains unknown.…”

Increased prevalence of abnormal vertebral patterning in fetuses and neonates with trisomy 21

“…Particularly in the cervical region, deviation from the standard number of seven vertebrae is rarely seen, regardless of the length of the neck [1,2]. Several researchers hypothesized that the stability of the cervical vertebral number is the result of developmental constraints or a stabilizing selection against changes in this number [1,3,4].…”