Deep time perspective on turtle neck evolution: chasing the Hox code by vertebral morphology

Abstract

The unparalleled ability of turtle neck retraction is possible in three different modes, which characterize stem turtles, living side-necked (Pleurodira), and hidden-necked (Cryptodira) turtles, respectively. Despite the conservatism in vertebral count among turtles, there is significant functional and morphological regionalization in the cervical vertebral column. Since Hox genes play a fundamental role in determining the differentiation in vertebra morphology and based on our reconstruction of evolutionary genetics in deep time, we hypothesize genetic differences among the turtle groups and between turtles and other land vertebrates. We correlated anterior Hox gene expression and the quantifiable shape of the vertebrae to investigate the morphological modularity in the neck across living and extinct turtles. This permitted the reconstruction of the hypothetical ancestral Hox code pattern of the whole turtle clade. The scenario of the evolution of axial patterning in turtles indicates shifts in the spatial expression of HoxA-5 in relation to the reduction of cervical ribs in modern turtles and of HoxB-5 linked with a lower morphological differentiation between the anterior cervical vertebrae observed in cryptodirans. By comparison with the mammalian pattern, we illustrate how the fixed count of eight cervical vertebrae in turtles resulted from the emergence of the unique turtle shell.

<b><i>Hox</i></b> Genes in Reptile Development, Epigenetic Regulation, and Teratogenesis

“…Interestingly, in the same study, Böhmer and Werneburg [2017] reported that in crocodiles, Hoxa5 is expressed at CV9, whereas in P. sinensis , it is expressed at CV2. This anterior expression in the turtle seems to be related to the absence of free cervical ribs, which allows the turtle to retract the head and neck inside the shell.…”

“…More recently, Böhmer and Werneburg [2017] suggested that expression of Hoxc6 (at the cervicothoracic transition) corresponds to the lack of ventral ribs in turtles, since it is expressed in prevertebrae and future carapacial dermis, but not in the somatopleure (region in which ventral ribs are missing). The authors also suggested that Hoxa7 was recruited for a turtle-specific function because most turtles possess a highly retractile neck that requires specialization at CV8.…”

“…According to Böhmer and Werneburg [2017], the first Hox gene expressed in the vertebral cervical column of archosaurs was Hoxb5 , showing the anterior expression boundary at the axis (cervical vertebra 2 [CV2]). However, in the turtle, the anterior expression boundary of Hoxb5 is at the atlas (CV1).…”

Patterns of morphological evolution in the skull of turtles: contributions from digital paleontology, neuroanatomy and biomechanics

“…Olivier Rieppel (2013) The shell, the toothless jaws with beaks and the clumsy and slow locomotion, even from the outside, make turtles "one of nature's most immediately recognizable life forms" (Adler 2007). From "the inside", they may look even more different: their unfenestrated skulls (unique among extant reptiles; Ferreira & Werneburg 2019; Chapter 2 of this thesis), their extremely mobile necks (Werneburg et al 2015a), the anatomical composition of the carapace and plastron (Nagashima et al 2009), their scapular and pelvic girdles inside the thoracic cage (Lyson & Joyce 2012), and their highly conserved cervical and trunk vertebral count (Böhmer & Werneburg 2017) are but a few of the morphological modifications of turtles that makes them one of the most intriguing vertebrate groups from a macroevolutionary perspective. At the same time that their very unique morphology leaves no room for doubts on their monophyly, it also makes it difficult to establish homologies with other reptiles (Carroll 2013), hampering the assessment of the group's origin and making the phylogenetic origin of turtles one of the oldest debates in vertebrate paleontology, lasting for more than 200 years (Rieppel 2013(Rieppel , 2017.…”

“…Its appearance completely reorganized the ancestral reptilian body plan in this lineage, not only modifying the ribs and dorsal vertebrae, but also completely reorganizing the whole turtle body. The musculoskeletal alterations related to the encapsulation of the scapular girdle and extensive reorganization of musculature related to the limb muscles (explained by the hypothesis of folding of the lateral body wall ;Nagashima et al 2009Nagashima et al , 2012Kuratani et al 2011), the division of function between the hypaxial muscles and the dorsal ribs that led to the development of their unique ventilatory system , the constraint on the number of cervical and thoracic vertebrae (Böhmer & Werneburg 2017), and even modifications on the skull, such as the emarginations (Werneburg 2015), mode of palatoquadrate fixation (Werneburg & Maier 2019), and the skull architecture (Chapter 5 of this Thesis) are thought to be related to the emergence of the turtle shell. A detailed review of the skull morphology, development and its modifications from a reptilian body plan are discussed in Chapter 2 of this thesis.…”