Palaeontological evidence reveals convergent evolution of intervertebral joint types in amniotes

Abstract

the intervertebral disc (iVD) has long been considered unique to mammals. palaeohistological sampling of 17 mostly extinct clades across the amniote tree revealed preservation of different intervertebral soft tissue types (cartilage, probable notochord) seen in extant reptiles. The distribution of the fossilised tissues allowed us to infer the soft part anatomy of the joint. Surprisingly, we also found evidence for an IVD in fossil reptiles, including non-avian dinosaurs, ichthyosaurs, plesiosaurs, and marine crocodiles. Based on the fossil dataset, we traced the evolution of the amniote intervertebral joint through ancestral character state reconstruction. The IVD evolved at least twice, in mammals and in extinct diapsid reptiles. From this reptilian IVD, extant reptile groups and some non-avian dinosaurs independently evolved a synovial ball-and-socket joint. The unique birds dorsal intervertebral joint evolved from this dinosaur joint. The tuatara and some geckos reverted to the ancestral persisting notochord. Morphology of the vertebral column has provided zoologists with key anatomical characters for groups of amniotes 1. This includes the intervertebral disc (IVD), a soft tissue feature, which has been considered to be unique to mammals 2-4. However, although the importance of soft tissue analysis in fossils is clearly recognised today 5-7 , investigations on soft tissue in the vertebral column, namely of joints and intervertebral spaces, have not been done 5. Neither has the evolution of the intervertebral joint been reconstructed using phylogenetic methods such as ancestral state reconstruction (ASR) 8. The intervertebral disc (IVD) is a fibrocartilaginous synarthrotic joint connecting the vertebral centra of mammals. It provides intervertebral flexibility, allowing for a wide range of movements and is involved in shock absorbance and transmission of mechanical forces 9,10. The IVD is thus of eminent biomechanical and clinical importance in the human vertebral column and has been studied from multiple perspectives in biological, medical and veterinary science 11-13. The crucial function of the IVD is to withstand forces acting on the axial skeleton, and gradual failure of IVD function from degenerative processes often leads to pathological symptoms 14. The mammalian IVD is composed of two distinct parts, the nucleus pulposus (NP) and the annulus fibrosus (AF). The NP is the hydrophilic proteoglycan-rich gelatinous core of the IVD. Surrounding the NP is the AF, a lamellate ring of spirally arranged layers of collagen I and fibrocartilage. The joint formed by the IVD is further stabilized by intervertebral ligaments that insert in the periosteal cortex of the adjacent vertebral centra. Due to the lack of soft tissue preservation in fossils, however, the evolutionary origins of the IVD among Amniota (true land animals) have been poorly understood 10. As increasing numbers of fossil amniote specimens

Ontogenetic variation in the skull of Stenopterygius quadriscissus with an emphasis on prenatal development

“…The phylogenetic position of Ichthyosauromorpha has not yet been resolved, although all recent analyses favour a diapsid or even sauropsid position 47 – 49 . Ingroup phylogeny is arguably better resolved with general consensus of the monophyly of the major clades, but little ingroup consensus 50 – 52 .…”

A new Paleogene fossil and a new dataset for waterfowl (Aves: Anseriformes) clarify phylogeny, ecological evolution, and avian evolution at the K-Pg Boundary

“…Opisthocoelous thoracic vertebrae are only known within Neoaves (Mayr and Clarke, 2003;Livezey and Zusi, 2006;Musser and Cracraft, 2019), and amphiplatyan and procoelous vertebrae are only known in non-avian dinosaurs (Livezey and Zusi, 2006). Further study on the function of amphicoelous vertebrae in the context of avian evolution and ecology is needed, especially since birds possess a unique dorsal intervertebral joint (Wintrich et al, 2020); however, the literature on this in fishes and crocodylomorphs suggests that amphicoelous vertebrae provide a more rigid spine (Yakovlev, 1967;Laerm, 1976;Molnar et al, 2015) that can withstand increased stress without deformation that may be caused by powerful movements of musculature (Yakovlev, 1967;Laerm, 1976), allowing for rapid flexure of the spine. Amphicoelous vertebrae have evolved several times in sharks, dipnoans, bony ganoids and teleosts, associating their appearance with improved speed of motion (Yakovlev, 1967).…”

Functional diversity of snake locomotor behaviors: A review of the biological literature for bioinspiration

“…with synovial (fluid-lubricated) articulations that reduce resistance to movement. 241,242 Vertebral shape, including condyle dimensions, has been the subject of only one large-scale comparative investigation in snakes. 216 It found that vertebral shape largely reflected family relationships, with very slight evidence of shape adaptation to particular habitat associations; however, it used only two-dimensional data and preceded the advent of phylogenetic comparative statistical methods by several decades, 243 so studies using more modern methods may reveal previously hidden relationships.…”

“…While lever arms are known for one species, 205 these were calculated relative to the centroid of the vertebral condyle, whose morphology would be expected to have consequences on motion between pairs of vertebrae. We know that adjacent cotyle/condyle pairs form ball‐and‐socket joints (Figure 4) with synovial (fluid‐lubricated) articulations that reduce resistance to movement 241,242 . Vertebral shape, including condyle dimensions, has been the subject of only one large‐scale comparative investigation in snakes 216 .…”