Long Bone Histology of Sauropterygia from the Lower Muschelkalk of the Germanic Basin Provides Unexpected Implications for Phylogeny

Abstract

BackgroundSauropterygia is an abundant and successful group of Triassic marine reptiles. Phylogenetic relationships of Triassic Sauropterygia have always been unstable and recently questioned. Although specimens occur in high numbers, the main problems are rareness of diagnostic material from the Germanic Basin and uniformity of postcranial morphology of eosauropterygians. In the current paper, morphotypes of humeri along with their corresponding bone histologies for Lower to Middle Muschelkalk sauropterygians are described and interpreted for the first time in a phylogenetic context.Methodology/Principal Findings Nothosaurus shows a typical plesiomorphic lamellar-zonal bone type, but varying growth patterns and the occurrence of a new humerus morphotype point to a higher taxonomic diversity than was known. In contrast to the enormous morphological variability of eosauropterygian humeri not assigned to Nothosaurus, their long bone histology is relatively uniform and can be divided into two histotypes. Unexpectedly, both of these histotypes reveal abundant fibrolamellar bone throughout the cortex. This pushes the origin of fibrolamellar bone in Sauropterygia back from the Cretaceous to the early Middle Triassic (early Anisian). Histotype A is assigned to Cymatosaurus, a basal member of the Pistosauroidea, which includes the plesiosaurs as derived members. Histotype B is related to the pachypleurosaur Anarosaurus. Contrary to these new finds, the stratigraphically younger pachypleurosaur Neusticosaurus shows the plesiomorphic lamellar-zonal bone type and an incomplete endochondral ossification, like Nothosaurus.Conclusions/SignificanceHistological results hypothetically discussed in a phylogenetical context have a large impact on the current phylogenetic hypothesis of Sauropterygia, leaving the pachypleurosaurs polyphyletic. On the basis of histological data, Neusticosaurus would be related to Nothosaurus, whereas Anarosaurus would follow the pistosaur clade. Furthermore, the presence of fibrolamellar bone, which is accompanied with increased growth rates and presumably even with increased metabolic rates, already in Anarosaurus and Cymatosaurus can explain the success of the Pistosauroidea, the only sauropterygian group to survive into the Jurassic and give rise to the pelagic plesiosaur radiation.

Growth patterns, sexual dimorphism, and maturation modeled in Pachypleurosauria from Middle Triassic of central Europe (Diapsida: Sauropterygia)

“…Also, contrary to the other pachypleurosaurs, the bone tissue type of Anarosaurus is summarized as incipient fibrolamellar bone (Klein, 2010), and indicates a higher growth rate than the other taxa show. Some remodeling of the inner cortex in the form of scattered erosion cavities can occur in taxa of the Neusticosaurus-Serpianosaurus clade.…”

“…The downside is that taxonomical assignment of isolated bones beyond group level is often difficult (e.g., see Rieppel, 2000;Klein et al, 2015aKlein et al, , b, 2016. Triassic Sauropterygia have been in the focus of several histological and/or microanatomical studies (Klein, 2010;Krahl et al, 2013;Klein et al, 2015a. The growth record was analyzed histologically and by growth curve modeling for Placodontia (Klein et al, 2015b) and Simosaurus (Klein and Griebeler, 2016).…”

“…Bone histological studies of midshaft regions in long bones (humeri and femora) of pachypleurosaur taxa (Sander, 1990;Klein, 2010Klein, , 2012Hugi et al, 2011) revealed important information on their life history: Serpianosaurus reached sexual maturity in its 2nd or 3rd year of life, and the oldest individual died in its 14th year (Hugi et al, 2011). Neusticosaurus pusillus and N. peyeri reached sexual maturity at an age between 3 and 4 and died between 7 and 10 years (Sander, 1990).…”

“…The onset of sexual maturity started in N. edwardsii between the 4th and 7th year, and it reached ages older than 15 years (Hugi et al, 2011). Anarosaurus shows a much faster growth rate due to growing with a different bone tissue and vascular pattern when compared to Neusticosaurus and Serpianosaurus (Klein, 2010). It also displays stratification of its cortex by growth marks but skeletochronology has not been analyzed in detail yet.…”

“…Based on their morphology these humeri most likely represent Dactylosaurus (Nopcsa, 1928;Sues and Caroll, 1985;Rieppel and Lin, 1995;Rieppel, 2000). The humeri from Winterswijk all belong to Anarosaurus heterodontus (Rieppel and Lin, 1995;Rieppel, 2000;Klein, 2009Klein, , 2012 and have been partly studied before (Klein, 2010(Klein, , 2012. Humeri from the Lower Lettenkeuper (aff.…”