Neurovascular anatomy of the protostegid turtle Rhinochelys pulchriceps and comparisons of membranous and endosseous labyrinth shape in an extant turtle

Serjoscha W Evers,Paul M Barrett,James M Neenan,Ingmar Werneburg,Gabriel S Ferreira,Roger B J Benson

doi:10.1093/zoolinnean/zlz063

Abstract

AbstractChelonioid turtles are the only surviving group of reptiles that secondarily evolved marine lifestyles during the Mesozoic Early chelonioid evolution is documented by fossils of their stem group, such as protostegids, which yield insights into the evolution of marine adaptation. Neuroanatomical features are commonly used to infer palaeoecology owing to the functional adaptation of the senses of an organism to its environment. We investigated the neuroanatomy and carotid circulation of the early Late Cretaceous protostegid Rhinochelys pulchriceps based on micro-computed tomography data. We show that the trigeminal foramen of turtles is not homologous to that of other reptiles. The endosseous labyrinth of R. pulchriceps has thick semicircular canals and a high aspect ratio. Comparisons among turtles and other reptiles show that the endosseous labyrinth aspect ratio is not a reliable predictor of the degree of aquatic adaptation, contradicting previous hypotheses. We provide the first models of neuroanatomical soft tissues of an extant turtle. Turtle brain morphology is not reflected by the brain cavity, and the endosseous labyrinth provides an incomplete reflection of membranous semicircular duct morphology. Membranous labyrinth geometry is conserved across gnathostomes, which allows approximate reconstruction of the total membranous labyrinth morphology from the endosseous labyrinth despite their poor reflection of duct morphology.

Highlights

We investigated the neuroanatomy and carotid circulation of the early Late Cretaceous protostegid Rhinochelys pulchriceps based on micro-computed tomography data
Turtle brain morphology is not reflected by the brain cavity, and the endosseous labyrinth provides an incomplete reflection of membranous semicircular duct morphology
One of our goals is to examine the osteological correlates for neuroanatomy, such as the endocast of the brain cavity and the structure of the endosseous labyrinth of R. pulchriceps

Summary

Introduction

The increased availability of computed tomography for palaeontological research has facilitated many studies describing the internal cranial anatomy of fossil turtles, including osteology (e.g. Brinkman et al, 2006; Lipka et al, 2006; Sterli et al, 2010; Jones et al, 2012; Bever et al, 2015; Evers et al, 2019), neurosensory anatomy (Walsh et al, 2009; Carabajal et al, 2013, 2017; Willis et al, 2013; Ferreira et al, 2018; Lautenschlager et al, 2018) and vascular anatomy (e.g. Joyce et al, 2018; Myers et al, 2018; Rollot et al, 2018). Neuroanatomical structures can be reconstructed digitally as threedimensional (3D) endocast models when the respective organs are housed in bony cavities of the skull (Witmer et al, 2008; Balanoff et al, 2015; see Fig. 1) These endocasts of the brain cavity represent the brain and cranial nerves (CNs), in addition to the endocast of the endosseous labyrinth of the inner ear, and have been used both qualitatively and quantitatively to interpret the neurological capabilities and palaeoecology of individual turtle taxa Cadena & Parham, 2015; Raselli, 2018; Evers & Benson, 2019; Evers et al, 2019) Despite uncertainties about their exact phylogenetic position with respect to crown-group sea turtles (see Raselli, 2018; Evers & Benson, 2019; Evers et al, 2019), protostegids represent early members of the only turtle lineage that evolved a pelagic lifestyle. Being stem taxa of either Dermochelys coriacea or chelonioids, protostegids provide morphological data on the evolution of marine adaptation in sea turtles

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