STABILITY IN THE NUMBER OF CERVICAL VERTEBRAE IS A PROXY FOR HIGH METABOLIC RATE AND EARLY ORGANOGENESIS IN THERAPSIDS AND PTEROSAURS

Nearly all mammals have seven cervical (neck) vertebrae. In contrast, birds and most taxa of reptiles have a highly variable number. Among extant mammalian taxa, the only exceptions are tree sloths and manatees. This stabilizing selection is apparently enforced by deleterious pleiotropic effects associated with coupling between Hox genes that control the development of the axial skeleton and those that control the proliferation of cell lines.

There is a positive correlation between metabolic rate and vulnerability to cancer-causing oxidative DNA damage. The low metabolic rates in manatees and sloths is thought to reduce the incidence and severity of cancer and other free-radical-associated diseases. Thus, a high metabolic rate in some vertebrate groups appears to correspond to strong stabilizing selection in the number of cervical vertebrae. In mammals, the number of cervical vertebrae is determined early in organogenesis, at a time when the cell lines are especially vulnerable. The numbers of vertebrae in more caudal regions of the axial skeleton are determined later. Birds and reptiles have apparently avoided this stabilizing selection by determining the number of their cervical vertebrae later in organogenesis, at a time when the process is less vulnerable to deleterious pleiotropic effects.

In this study we use this stability in the number of cervical vertebrae as a proxy for the presence of a high metabolic rate in pterosaurs and extinct synapsids. Pre-therapsid synapsids have a variable number of cervical vertebrae, whereas all therapsid taxa have seven cervical vertebrae. We conclude that, within the synapsida, a high metabolic rate first appeared in the Late Permian and has been a characteristic feature of therapids and mammals ever since that time.

Among diapsid reptiles, pterosaurs are unique in having a consistent number of cervical vertebrae. They also have seven. The apparent stabilizing selection for seven cervical vertebrae suggests that pterosaurs also had a high metabolic rate. The developmental implication is that, contrary to reptiles with variable numbers of cervical vertebrae, in pterosaurs the determination of the number of cervical vertebrae occurred early in organogensis, at a time when it was under the influence of the same stabilizing selection experienced by therapsids and mammals.