Evolution of the Mammalian Neck from Developmental, Morpho-Functional, and Paleontological Perspectives

Abstract

The mammalian neck adopts a variety of postures during daily life and generates numerous head trajectories. Despite its functional diversity, the neck is constrained to seven cervical vertebrae in (almost) all mammals. Given this low number, an unexpectedly high degree of modularity of the mammalian neck has more recently been uncovered. This work aims to review neck modularity in mammals from a developmental, morpho-functional, and paleontological perspective and how high functional diversity evolved in the mammalian neck after the occurrence of meristic limitations. The fixed number of cervical vertebrae and the developmental modularity of the mammalian neck are closely linked to anterior Hox genes expression and strong developmental integration between the neck and other body regions. In addition, basic neck biomechanics promote morpho-functional modularity due to preferred motion axes in the cranio-cervical and cervico-thoracic junction. These developmental and biomechanical determinants result in the characteristic and highly conserved shape variation among the vertebrae that delimits morphological modules. The step-wise acquisition of these unique cervical traits can be traced in the fossil record. The increasing functional specialization of neck modules, however, did not evolve all at once but started much earlier in the upper than in the lower neck. Overall, the strongly conserved modularity in the mammalian neck represents an evolutionary trade-off between the meristic constraints and functional diversity. Although a morpho-functional partition of the neck is common among amniotes, the degree of modularity and the way neck disparity is realized is unique in mammals.

Phenotypic integration in the carnivoran backbone and the evolution of functional differentiation in metameric structures

“…Moreover, this high integration from C02–C07 could not be explained by the functional roles in which these vertebrae are involved, because although the mid‐cervical vertebrae (C03–C05) are involved in axial rotation, the anterior and posterior cervicals do contribute to sagittal movements (Graf et al. 1995; Arnold 2020).…”

Pushing the boundary? Testing the “functional elongation hypothesis” of the giraffe's neck

“…2017; Böhmer 2017; Jones et al. 2018; Arnold 2020). C7 and T1 of the giraffe show striking morphological differences to their respective counterparts in other cetartiodactyl species.…”

“…Using geometric morphometrics, subtle shape differences between vertebrae can be quantified (Arnold et al 2016;Randau et al 2017;Böhmer 2017;Jones et al 2018;Arnold 2020). C7 and T1 of the giraffe show striking morphological differences to their respective counterparts in other cetartiodactyl species.…”

A comparative morphological study of the sixth and seventh spinous processes of the cervical vertebrae in extinct and extant species of Equus.

“…The number of cervical vertebrae in mammals became fixed more than 200 million years ago (mya); the canonical number of seven cervicals is well established by palaeontological evidence (Buchholtz et al 2012;Arnold 2020). The mammalian cervical spine, considered as a morphologically static feature (Arnold et al 2017), typically includes dorsally positioned spinous processes on some or all of the 2nd to 7th cervical vertebrae (Zsoldos and Licka 2015;Arnold 2020).…”

“…The number of cervical vertebrae in mammals became fixed more than 200 million years ago (mya); the canonical number of seven cervicals is well established by palaeontological evidence (Buchholtz et al 2012;Arnold 2020). The mammalian cervical spine, considered as a morphologically static feature (Arnold et al 2017), typically includes dorsally positioned spinous processes on some or all of the 2nd to 7th cervical vertebrae (Zsoldos and Licka 2015;Arnold 2020). The North American Eocene perissodactyl A comparative morphological study of the spinous processes of the sixth and seventh cervical vertebrae in extinct and extant species of Equus Hyracotherium (Buchholtz et al 2012;MacFadden 1992) bears blade-like spinous processes on the 4th to 7th cervical vertebrae (Wood et al 2011) (Fig.…”