Megaevolutionary dynamics and the timing of evolutionary innovation in reptiles

Abstract

The origin of phenotypic diversity among higher clades is one of the most fundamental topics in evolutionary biology. However, due to methodological challenges, few studies have assessed rates of evolution and phenotypic disparity across broad scales of time to understand the evolutionary dynamics behind the origin and early evolution of new clades. Here, we provide a total-evidence dating approach to this problem in diapsid reptiles. We find major chronological gaps between periods of high evolutionary rates (phenotypic and molecular) and expansion in phenotypic disparity in reptile evolution. Importantly, many instances of accelerated phenotypic evolution are detected at the origin of major clades and body plans, but not concurrent with previously proposed periods of adaptive radiation. Furthermore, strongly heterogenic rates of evolution mark the acquisition of similarly adapted functional types, and the origin of snakes is marked by the highest rates of phenotypic evolution in diapsid history.

Sphenodontian phylogeny and the impact of model choice in Bayesian morphological clock estimates of divergence times and evolutionary rates

“…In the empirical case explored here, the available fossil data places the oldest known sphenodontians and squamates in the Middle Triassic (230-242 Mya) [13,34]. Further, recent transcriptomic and total-evidence based studies estimate [13,37,103] or perhaps closer to the Permian-Triassic boundary at 252Mya [104]. Therefore, given current knowledge, it would be expected for the oldest nodes in our tree (marking the divergence of early lepidosauromorph lineages) to be at least within the Permian (not older than 298.9 Mya).…”

“…For instance, there still are several logistical challenges for constructing densely sampled morphological datasets (e.g., specimen accessibility, number of high-quality CT scanned specimens in online repositories) and the vertebrate fossil record is frequently incomplete and sometimes with few phylogenetically informative specimens. Similar examples of higher-level phylogenies with chronologically sparse taxon samplinglow taxon number:age of the tree ratio ratios (< 1, and frequently < 0.5)-include recently published datasets on pterosaurs [118], dinosaurs [119,120], early tetrapods [56], gnathostomes [121], mammals [122], diapsid, and squamate reptiles [13,37], among many others. Notably, many of those datasets comprehend the largest taxonomic sampling for their respective taxonomic groups using morphological data, and increasing taxonomic sampling to considerably higher levels would be simply impossible on the short-to mid-term as some of them already include most or all of the informative fossil taxa available (such as herein).…”

“…The high rates of molecular evolution detected for Sphenodon were measured from mitochondrial sites only [125], which are highly variable (i.e., fast evolving), when compared to nuclear sites in broad scale taxonomic datasets among many vertebrates, including lepidosaurs [13,127,128]. Finally, subsequent studies found much slower molecular rates on the branch leading to Sphenodon based on a larger sample of loci (including nuclear loci) [37] and based on full genomic data [129].…”

“…Sphenodontians are a unique lineage of diapsid reptiles, with an extremely long evolutionary history dating at least as far back as the Middle Triassic at~230Mya [34], but currently represented by a single living species, Sphenodon punctatus, inhabiting small islands off the coast of New Zealand [35]. In contrast, their sister clade, squamates (lizards and snakes), is currently represented by~10,650 extant species [36], indicating both lineages had very different evolutionary histories after their split from a common ancestor at about 260-270 Mya [13,37]. Despite considerable efforts to understand broad scale phylogenetic relationships, divergence times and evolutionary patterns among the various families of squamates (e.g., [13,[38][39][40][41]), there has been comparatively less effort to understand the species level relationships and macroevolutionary patterns in sphenodontians.…”

The making of calibration sausage exemplified by recalibrating the transcriptomic timetree of jawed vertebrates

“…An Early Triassic or perhaps Late Permian maximum age seems reasonable, but, given the rarity of stem-pan-lepidosaurs and of Permian diapsids in general (Carroll's Gap -Marjanović and Laurin, 2013a), I rather propose to use the ecologically similar small amniotes (e.g. Haridy et al, 2017;MacDougall et al, 2019) Simões et al, 2018Simões et al, , 2020, the pan-squamate record as known today goes completely silent (see below under Node 131 for the one or two supposed exceptions) until the dam suddenly breaks in the Bathonian (Middle Jurassic) and representatives of the stem as well as, by current understanding, several parts of the crown appear in several sites in the northern continents and northernmost Gondwana. Second, these early representatives are all isolated and generally incomplete bones that preserve few diagnostic characters; the oldest complete skeletons come from one Tithonian (latest Jurassic) cluster of sites (Conrad, 2017), followed by a few Early Cretaceous ones as well as the oldest partially articulated material other than Megachirella.…”