Extreme Selection in Humans Against Homeotic Transformations of Cervical Vertebrae

Abstract

Why do all mammals, except for sloths and manatees, have exactly seven cervical vertebrae? In other vertebrates and other regions, the vertebral number varies considerably. We investigated whether natural selection constrains the number of cervical vertebrae in humans. To this end, we determined the incidence of cervical ribs and other homeotic vertebral changes in radiographs of deceased human fetuses and infants, and analyzed several existing datasets on the incidence in infants and adults. Our data show that homeotic transformations that change the number of cervical vertebrae are extremely common in humans, but are strongly selected against: almost all individuals die before reproduction. Selection is most probably indirect, caused by a strong coupling of such changes with major congenital abnormalities. Changes in the number of thoracic vertebrae appear to be subject to weaker selection, in good correspondence with the weaker evolutionary constraint on these numbers. Our analysis highlights the role of prenatal selection in the conservation of our common body plan.

MIPoD: A Hypothesis‐Testing Framework for Microevolutionary Inference from Patterns of Divergence

“…Vertebral number is remarkably constant in many vertebrate groups, apparently because deviation away from a modal number can have profoundly deleterious consequences (Galis et al 2006). However, vertebral number in snakes is conspicuously variable among species, with means ranging from 100 to 300 total vertebrae.…”

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

“…In the general population or in patients without anomalies, a low prevalence of absent or rudimentary 12th thoracic ribs (0.4-6.6%) and cervical ribs (0.2-6.2%) is reported [5,8,9,[17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34]. Bots et al [17] found a higher prevalence of agenesis of the 12th thoracic ribs (12.6%) and cervical ribs (37.7%) in fetuses with a gestational age ranging between 10 and 21 weeks that were electively aborted, but medical data concerning these pregnancies and the mothers were missing.…”

“…If a rib on the most cranial or most caudal thoracic vertebra had a length of less than half of the rib of the adjacent thoracic vertebra, it was considered rudimentary. Enlarged transverse processes were considered rudimentary cervical ribs if the length of the transverse process of the seventh cervical vertebra was more than the transverse process of the first thoracic vertebra [5,16,17]. Karyotype was analyzed using fluorescent in situ hybridization (FISH).…”

“…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]. The fact that selection against variations in caudally located parts of the vertebral column is less prominent and thoracolumbar and lumbosacral shifts are more common in the general population, could be a reflection of the craniocaudal direction in which the vertebral column is formed [3,5]. Formation of the cervical region of the vertebral column starts earlier in embryogenesis than the formation of the thoracic and lumbar regions.…”

“…Formation of the cervical region of the vertebral column starts earlier in embryogenesis than the formation of the thoracic and lumbar regions. It has been suggested that the interactivity between the developing organ systems and the patterning of the embryonic axes is higher during early organogenesis than during later stages [5,6]. This can lead to a higher vulnerability to disruptions in embryonic development during the early stage in which the cervical vertebral column is formed, compared with the stages in which the thoracic and lumbar regions of the vertebral column are formed [7].…”