Megaevolutionary dynamics in reptiles and the role of adaptive radiations in evolutionary innovation

Abstract

13Adaptive radiations are long believed to be responsible for the origin of phenotypic diversity and 14 new body plans among higher clades in the fossil record. However, few studies have assessed 15 rates of phenotypic evolution and disparity across broad scales of time to understand the 16 evolutionary dynamics behind the origin of major clades, or how they relate to rates of molecular 17 evolution. Here, we provide a total evidence approach to this problem using the largest available 18 data set on diapsid reptiles. We find a strong decoupling between phenotypic and molecular rates 19 of evolution, with many periods of accelerated phenotypic evolution or expansion of phenotypic 20 disparity at the origin of major reptile clades and body plans that do not correspond to periods of 21 adaptive radiation. We find heterogeneous rates of evolution during the acquisition of similarly 22 23 evolutionary rates. 24 25 26The classical theory of adaptive radiation predicts that such events are characterized by 27 high rates of phenotypic evolution, in combination with an expansion in phenotypic disparity and 28 taxonomic diversity, as new species rapidly transforming to occupy available adaptive zones 29 during times of ecological opportunity 1,2 . Across geological timescales, lineages undergoing 30 exceptionally fast evolutionary rates would give rise to many new lineages, with some of these 31 fast-evolving lineages potentially going extinct. Once niches are occupied, phenotypic disparity 32 stabilizes and species diversification and evolutionary rates decrease and stabilize at lower 33 levels 1 . It has long been assumed that the aftermath of mass extinctions would provide the ideal 34 ecological opportunities for adaptive radiations 1,3 , such as the diversification of placental 35 mammals after the Cretaceous-Palaeogene mass extinction (KPME), or the appearance of several 36 reptile lineages in the fossil record following the Permian-Triassic mass extinction (PTME) 2,3 . 37Therefore, adaptive radiations have long been hypothesized to be responsible for the origin of 38 most of biological diversity (in both taxonomic and phenotypic terms), especially regarding the 39 origin of higher clades (e.g. families or orders) and new body plans, or what Simpson had 40 originally referred to as "mega-evolutionary" processes 4 . 41Although the concept of adaptive radiations is fundamental to our understanding of 42 evolutionary theory, only recently have quantitative tools been developed to rigorously test its 43 predictions at broad taxonomic and deep time scales in the evolutionary paleobiology. For 44 instance, using both relaxed clocks and phylogenetic comparative methods various studies have 45 3 found high rates of evolution at the origin of major clades, including the early evolution of birds, 46 arthropods, and crown placental mammals 5-7 . Fast evolutionary rates during putative periods of 47 adaptive radiations following mass extinctions have also been recovered, such as the radiation of 48 birds 8 and placental mammals...

Rapid Initial Morphospace Expansion and Delayed Morphological Disparity Peak in the First 100 Million Years of the Archosauromorph Evolutionary Radiation

“…A similar pattern of high evolutionary rates and subsequent deceleration have been found in mammaliamorphs (Close et al, 2015), whereas rather constant rates have been found for lepidosaurs in the Early Jurassic (Simões et al, 2020). The increase of evolutionary rates-which is stronger for the pelvis-recovered here for archosauromorphs during the Middle and Late Jurassic partially matches the results found for lepidosaurs, but the latter show a conspicuous deceleration in the Late Jurassic (Simões et al, 2020). By contrast, mammaliamorphs depict a continuous decrease of rates during the Middle and Late Jurassic (Close et al, 2015).…”

“…The stabilization (cranium) or increase (pelvis) of evolutionary rates since the Toarcian is likely related to the mass extinction event and the diversification of the group as a result of the occupation of empty niches (Benton, 1983;Brusatte et al, 2008a;Brusatte et al, 2008b;Irmis, 2010). A similar pattern of high evolutionary rates and subsequent deceleration have been found in mammaliamorphs (Close et al, 2015), whereas rather constant rates have been found for lepidosaurs in the Early Jurassic (Simões et al, 2020). The increase of evolutionary rates-which is stronger for the pelvis-recovered here for archosauromorphs during the Middle and Late Jurassic partially matches the results found for lepidosaurs, but the latter show a conspicuous deceleration in the Late Jurassic (Simões et al, 2020).…”

The affinities of the Late Triassic Cryptovaranoides and the age of crown squamates

“…We used the Mkv + gamma substitution model [43] (Mk with ascertainment bias correction) for the morphological data of datasets 1 and 2. The molecular partition of the combined evidence dataset (dataset 2) was analysed under the GTR + gamma model and subdivided into four partitions, following the previous partitioning and model test analyses for this dataset [11,35].…”

“…Recent additions and revisions to the early squamate and rhynchocephalian fossil records made possible by the use of new imaging and analytical tools have substantially improved our understanding of squamate origins and the rise of squamates to ecological dominance as rhynchocephalian diversity declined [6][7][8][9][10]. Reconstructing the divergence times of living squamate clades has been greatly aided by the reconciliation of major differences among phylogenies of squamates produced using morphological and molecular data [1,5,7,9,11]. These advances have consistently inferred a Triassic (approx.…”

“…252-202 Ma) age for the origins of the squamate and rhynchocephalian total clades, followed by the diversification of the major clades of crown squamates during the Jurassic (approx. 202-145 Ma) [5,7,[11][12][13][14][15]. This was followed by the radiation of modern squamate families during the middle and Late Cretaceous [16,17] shortly after the Cretaceous Terrestrial Revolution [18], along with the Cretaceous invasion of aquatic environments by mosasaurian squamates [19].…”