The origin of squamates revealed by a Middle Triassic lizard from the Italian Alps

Abstract

Modern squamates (lizards, snakes and amphisbaenians) are the world's most diverse group of tetrapods along with birds and have a long evolutionary history, with the oldest known fossils dating from the Middle Jurassic period-168 million years ago. The evolutionary origin of squamates is contentious because of several issues: (1) a fossil gap of approximately 70 million years exists between the oldest known fossils and their estimated origin; (2) limited sampling of squamates in reptile phylogenies; and (3) conflicts between morphological and molecular hypotheses regarding the origin of crown squamates. Here we shed light on these problems by using high-resolution microfocus X-ray computed tomography data from the articulated fossil reptile Megachirella wachtleri (Middle Triassic period, Italian Alps ). We also present a phylogenetic dataset, combining fossils and extant taxa, and morphological and molecular data. We analysed this dataset under different optimality criteria to assess diapsid reptile relationships and the origins of squamates. Our results re-shape the diapsid phylogeny and present evidence that M. wachtleri is the oldest known stem squamate. Megachirella is 75 million years older than the previously known oldest squamate fossils, partially filling the fossil gap in the origin of lizards, and indicates a more gradual acquisition of squamatan features in diapsid evolution than previously thought. For the first time, to our knowledge, morphological and molecular data are in agreement regarding early squamate evolution, with geckoes-and not iguanians-as the earliest crown clade squamates. Divergence time estimates using relaxed combined morphological and molecular clocks show that lepidosaurs and most other diapsids originated before the Permian/Triassic extinction event, indicating that the Triassic was a period of radiation, not origin, for several diapsid lineages.

Evolutionary lability inHoxcluster structure and gene expression inAnolislizards

“…Consequently, individual TE copies accumulate mutations and decay over time. Thus, signals of older activity periods, such as those that occurred during early squamate diversification (up to 250 million years ago; Simoes et al 2018), are either decayed or superseded by more recent TE insertions. Further studies on the relationship between TE activity and rates of speciation in taxa with well-resolved phylogenies are required to test this hypothesis.…”

Lizards possess the most complete tetrapod Hox gene repertoire despite pervasive structural changes in Hox clusters

“…Gene loss, if not caused by structural changes, is a process that can extend over long periods of time. Degraded open reading frames of HoxC1 and -D12 are shared among the seven snake species, which indicates that the onset of degradation occurred in a snake ancestor, living more than 100 mya (Harrington & Reeder, 2017;Simoes et al, 2018). However, for roughly half of the exons, traces of the original sequences remain, albeit with low similarity to intact orthologs.…”

Morphological features of the yolk processing pattern in the eastern fence lizard, Sceloporus undulatus (Phrynosomatidae)

“…Given that lizards and snakes show a similar pattern of yolk processing, this pattern conservatively must be interpreted as ancestral for squamates, and perhaps lepidosaurs, as previously suggested (Elinson et al, ). Because the fossil history of lizards extends back to the Middle Triassic (Simões et al, ), it constitutes an ancient pattern. Among the several questions that deserve consideration is whether the squamate pattern is ancestral for Reptilia, and even for amniotes in general.…”