The Origin and Early Evolution of Sauria: Reassessing the Permian Saurian Fossil Record and the Timing of the Crocodile-Lizard Divergence

Abstract

Sauria is the crown-group of Diapsida and is subdivided into Lepidosauromorpha and Archosauromorpha, comprising a high percentage of the diversity of living and fossil tetrapods. The split between lepidosauromorphs and archosauromorphs (the crocodile-lizard, or bird-lizard, divergence) is considered one of the key calibration points for molecular analyses of tetrapod phylogeny. Saurians have a very rich Mesozoic and Cenozoic fossil record, but their late Paleozoic (Permian) record is problematic. Several Permian specimens have been referred to Sauria, but the phylogenetic affinity of some of these records remains questionable. We reexamine and review all of these specimens here, providing new data on early saurian evolution including osteohistology, and present a new morphological phylogenetic dataset. We support previous studies that find that no valid Permian record for Lepidosauromorpha, and we also reject some of the previous referrals of Permian specimens to Archosauromorpha. The most informative Permian archosauromorph is Protorosaurus speneri from the middle Late Permian of Western Europe. A historically problematic specimen from the Late Permian of Tanzania is redescribed and reidentified as a new genus and species of basal archosauromorph: Aenigmastropheus parringtoni. The supposed protorosaur Eorasaurus olsoni from the Late Permian of Russia is recovered among Archosauriformes and may be the oldest known member of the group but the phylogenetic support for this position is low. The assignment of Archosaurus rossicus from the latest Permian of Russia to the archosauromorph clade Proterosuchidae is supported. Our revision suggests a minimum fossil calibration date for the crocodile-lizard split of 254.7 Ma. The occurrences of basal archosauromorphs in the northern (30°N) and southern (55°S) parts of Pangea imply a wider paleobiogeographic distribution for the group during the Late Permian than previously appreciated. Early archosauromorph growth strategies appear to be more diverse than previously suggested based on new data on the osteohistology of Aenigmastropheus.

Preliminary observations on the bone histology of the Middle Triassic pseudosuchian archosaurBatrachotomus kupferzellensisreveal fast growth with laminar fibrolamellar bone tissue

“…Data on archosauromorphs, archosauriforms, and pseudosuchian archosaurs, however, are still rare (and less well understood) but so far show a variety of bone tissues and vascular systems, resulting in a mixture of bone tissue patterns (Botha-Brink and Smith, 2011). The primary bone tissue type of non-ornithodiran archosauromorphs can be characterized (with a few exceptions, see below) as lamellar-zonal bone tissue type/LZB (Ricql es et al, 2003(Ricql es et al, , 2008Botha-Brink and Smith, 2011;Werning and Irmis, 2011;Ezcurra et al, 2014;Mukherjee, 2015;Veiga et al, 2015;Werning and Nesbitt, 2016). Differences with modern reptiles that also grow with LZB are mainly related to vascularity (density and organization) and a higher organization of tissue.…”

Supplemental Material for 'Postcranial osteology of Azendohsaurus madagaskarensis (?Middle to Upper Triassic, Isalo Group, Madagascar) and its systematic position among stem archosaur reptiles. (Bulletin of the American Museum of Natural History, no. 398)'

“…This is well supported, given that Archosauriformes, represented by Archosaurus rossicus, diverged from the rest of Archosauromorpha by the end of the Permian (Tatarinov, 1960;Ezcurra et al, 2014). This divergence indicates that all successive outgroups to Archosauriformes (e.g., Rhynchosauria, Tanystropheidae) were also present by that time.…”

“…OF ARCHOSAUROMORPHA All recent phylogenetic analyses concur that the origin and lineage diversification of early archosauromorphs occurred prior to the end of the Permian (e.g., Dilkes, 1998;Muller, 2004;Butler et al, 2011;Ezcurra et al, 2014). This is well supported, given that Archosauriformes, represented by Archosaurus rossicus, diverged from the rest of Archosauromorpha by the end of the Permian (Tatarinov, 1960;Ezcurra et al, 2014).…”

“…These include: (1) a small tuber located on the ventrolateral surface of the prezygapophyseal stalk in the middle to posterior cervical vertebrae; (2) a well-defined fossa at the base of the neural spine, just posterior to the prezygapophyses in the second sacral vertebra; (3) the lateral side of the calcaneal tuber expanded laterally and ventrally, with the ventral expansion being clearly visible in proximal view; (4) deep fossae between well-developed laminae in the posterior cervical vertebrae (autapomorphy among non-archosaurian archosauromorphs, but these structures are found in some crowngroup archosaurs and Aenigmastropheus parrintoni [Ezcurra et al, 2014]); (5) hyposphene-hypantra intervertebral articulations in the posterior cervical, anterior trunk, and sacral vertebrae (autapomorphy among nonarchosaurian archosauromorphs, but these structures are found in some crown-group archosaurs); (6) proximal projection on the proximal surface of metatarsal IV; and (7) an oval and proximodistally oriented tuber on the lateral surface of the scapula that nearly contacts the edge of the glenoid fossa.…”

Arctosaurus osborni, a Late Triassic archosauromorph reptile from the Canadian Arctic Archipelago

“…Referral to Archosauromorpha is supported by three features (Ezcurra et al 2014): the (in lateral view) parallelogramshaped centrum, the anterior articular surface of which is set dorsal to the posterior one; the well-developed posterior centrodiapophyseal ridge; and the positioning of the zygapophyses close to each other medially. In addition, NMING:F14878 has two features that Nesbitt et al (2015) hypothesized as shared derived character states for the archosauromorph clade Allokotosauria: the apparently anterodorsally canted neural spine (character state 116-1; Nesbitt et al 2015) and the posteriorly pointed epipophyses on the dorsal surface of the postzygapophyses (character state 119-1; Nesbitt et al 2015).…”