Lepidosaurs, currently mainly represented by squamates, are one of the most species-rich tetrapod clades (Uetz et al., 2019), only rivaled by birds in terms of diversity. Evidence points to an explosion in squamate biodiversity 100 million years ago (Ma), in the Cretaceous (Lloyd et al., 2008; Longrich et al., 2012; Mongiardino Koch and Gauthier, 2018), corresponding to the time when flowering plants were diversifying and restructuring terrestrial ecosystems. However, the origin of squamates at least 250 Ma (Jones et al., 2013; Simões et al., 2018) poses two challenges: was that 150 million years (Myr) of poorly documented history real or evidence of a poor fossil record; and when did squamates acquire their current range of ecological adaptations? These uncertainties contrast somewhat with more confident knowledge of the early radiations of birds (Lee et al., 2014; Wang and Lloyd, 2016; Benson et al., 2014) and mammals (Close et al., 2015).

The squamate fossil record is patchy, especially through the Triassic to Early Cretaceous interval (252–100 Ma) when fossils are sparse and incomplete (Cleary et al., 2018). The earliest unambiguously identified squamate fossils date from the Middle and Late Jurassic (174–145 Ma), and among them are forms that can be assigned to major modern clades of squamates, including both lizards and snakes (Evans, 1998; Evans, 2003; Caldwell et al., 2015), but many are isolated jaws and skull bones of difficult identification. Further, their rarity suggests diversity was not high.

The mid-Cretaceous shows an increase in abundance and diversity of squamates (Gauthier et al., 2012), linked to the Cretaceous Terrestrial Revolution (KTR), which triggered an outburst of terrestrial life, including major new clades, such as angiosperms, as well as ferns, hornworts, liverworts among plants, currently highly diverse insect groups, including cockroaches, termites, many groups of beetles, bugs, the wasp, ant, and bee lineage, and the butterfly and moth lineage. These rich new supplies of plants and insects provided food for expanding clades of insect-eaters, including spiders, birds, mammals, and lizards, and even perhaps some dinosaur groups (Lloyd et al., 2008; Doyle, 2008; Benton, 2010; Meredith et al., 2011; Cardinal and Danforth, 2013). It could be plausible to identify this as the time when squamate ecological adaptation expanded, but is this truly the case?

Here, we explore morphospace distribution, disparity (morphological richness), and evolutionary rates of lepidosaurs to understand these important stages in the first three-quarters of squamate history. Species richness is hard to document with confidence in the face of such a patchy fossil record (Cleary et al., 2018), although when combined with phylogenomic data, the relative timing of origins of major modern clades can be identified (Jones et al., 2013; Simões et al., 2018). Sparse fossil data can be used, on the other hand, to document disparity, even though extreme forms may be absent, and the morphospace may be poorly filled. Phylogenetic comparative methods are used here to explore whether the available fossil record before the Late Cretaceous suggests that the importance of the Jurassic in the rise of squamates has been underestimated, hinting at a cryptic diversity hidden behind an impoverished fossil record.

Our dated phylogeny of lepidosaurs (Figure 1, Figure 1—figure supplement 1), based on a morphological tree constrained by phylogenomic evidence (Figure 1—figure supplements 2–4, see Figure 1—figure supplements 5–7 for results of an unconstrained analysis), shows that the clade originated around the Permian-Triassic boundary, and that by the Mid-Triassic it was represented by different extinct groups. The Rhynchocephalia diversified in the Mesozoic, but reverted to a single species subsequently, the living tuatara (Sphenodon punctatus) from New Zealand. The Squamata, on the other hand, show a step of diversification through the Jurassic, as the main modern clades emerged, and then a further diversification in the mid-Cretaceous, perhaps linked to the KTR. The ranges of ages for nodes differ depending on the method used (Figure 1—figure supplement 1), with the Hedman method (Figure 1) yielding the oldest divergence dates for nodes, the MBL (Minimum Branch Length) method yielding the youngest ones, and the equal method being intermediate. According to these results, it was regarded as necessary to consider all three methods of dating when performing the evolutionary rate analyses in order to discard the possibility that results were biased by the selected dating method.

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The dated phylogenetic tree only describes the outline of the origins of squamate biodiversity, but does not map species numbers or, importantly, the range of morphology, and presumably the range of adaptation, reflecting ecological impact, of the group. Using a large morphological dataset (Conrad, 2018), covering 201 species of living and fossil lepidosaurs scored for 836 skeletal morphological characters, we analyzed disparity for lepidosaurs through time and tracked changes to morphospace occupation and major expansions. Stacked temporal morphospaces (Figure 2) show that rhynchocephalians and squamates occupy mutually exclusive morphospaces. Stepping up through time, from bottom to top of the stack, shows how lepidosaur morphospace expanded, not gradually, but marked by a single major step. At first, the total morphospace is small, formed by stem lepidosaurs and rhynchocephalians in the Triassic, and exclusively by rhynchocephalians in the Early Jurassic. Note that the lack of Early Jurassic stem lepidosaurs is artificial because they are found again (and possibly for the last time) in the Middle Jurassic as represented by Marmoretta. Then, with the addition of squamates in the Middle to Late Jurassic bin, morphospace expands to five or six times the area – the limits are established by rhynchocephalians, generalized lizards, anguimorph lizards, and snakes, each occupying a separate area of morphospace. We coin the term Jurassic Morphospace Expansion (JME) for the event related to this sudden increase in morphospace, which is interpreted as evidence of the initial radiation of the total group Squamata. Note that the coincident loss of stem lepidosaurs does not result in a modification of the morphospace hull because of the central position of these taxa. This morphospace configuration remains remarkably stable from the Late Jurassic through to the present, with only subtle increases in morphospace occupation and in the density of points inside the envelope, notably in the mid Cretaceous coinciding with the KTR and the consequent recorded increase in diversity.

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At this point, we should comment on the form-function relationship. It is well understood that form (skeletal morphology) does not always equate to function (Wainwright et al., 2005), with many functions sometimes performed by organisms of apparently similar morphology, or many different morphologies capable of performing a single function. However, here we calibrate the morphospace by mapping living taxa of known function and ecology onto the fossil time slices. This means we can mark (Figures 2 and 3) the rhynchocephalian (cluster 1, in green) pole as dietary generalists with robust jaws and tongue prey prehension like the modern Sphenodon; the generalized lizard (cluster 2, in blue) pole as diverse insect-eaters, like modern skinks; the anguimorph (cluster 3, in yellow) pole as active foragers with tendency to carnivory; and the snake (cluster 4, in violet) pole as limbless predators that feed mainly on other vertebrates and, to a lesser degree, invertebrates. Note that these clusters are loosely based on the ones recovered using the R ‘pamk’ function of the fpc package (see Figure 3—figure supplement 6, Source code 3). Admittedly, this is a simplification because, just as an example, rhynchocephalians contain dietary specialists (durophagous, piscivorous, etc.) and examples of forms adapted to swimming (like pleurosaurs), and the same occurs with specific clades of squamates (e.g., herbivore iguanians). Although a more precise ecomorphological classification would potentially provide more information on the distribution of ecologies through time, it has proven impractical for the current dataset, also in agreement with previous results (e.g., Simões et al., 2020). However, our classification serves the purpose of depicting that the extremes of morphospace had been achieved by the Middle to Late Jurassic (Figures 2 and 3D). Regarding squamates, it is worth noting that the first members of the group sampled in our analyses are Late Jurassic in age, but Middle Jurassic forms are known, just happen to be not included in the current morphological dataset because they are too incomplete.

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The illustrated morphospaces (Figures 2, 3A and B, Figure 2—figure supplement 2, Figure 3—figure supplement 1) represent the first two major axes of variation, and there could be additional morphospace expansions along the other main axes: this is not the case (Figure 2—figure supplements 3 and 5; Figure 3—figure supplements 2 and 3). Further, the story does not change when the post-Cretaceous time bin is divided into Paleogene and Neogene time slices (Figure 2—figure supplements 2; 4 and 6). In a plot of total disparity (i.e., the sum of variances [SoVs] across all morphospace axes) of lepidosaurs through geological time (Figure 4A), the two peaks of elevated disparity (Middle–Late Jurassic and mid–Late Cretaceous) are clear. These summary data also confirm the much higher total disparity of squamates than rhynchocephalians (Figure 4—figure supplement 1) and among the former, a higher disparity of snakes and anguimorphs (and less clearly mosasaurs) than the remaining main groups of squamates among which dibamids, lacertids, and the extinct group of ardeosaurs (sensu lato) are the ones with the lowest disparity (Figure 4—figure supplement 2).

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The ‘two-peak’ pattern is also identified through a study of evolutionary rates among lepidosaurs (Figure 4B). Maximum-likelihood analyses of rates of morphological character evolution clearly show that the highest rates occur in the Late Jurassic (coinciding with the peak in disparity and roughly coinciding with the observed expansion of morphospace), and there is a lower peak in the mid-Cretaceous (see Figure 4—figure supplements 5–7). The high peak is for squamates (see Figure 4—figure supplements 8–10 for squamates), not rhynchocephalians (see Figure 4—figure supplements 11–13), and in our opinion all three observations (morphospace expansion, increase of disparity, and fast evolutionary rates) are linked and support the existence of the JME event. Rhynchocephalians showed their highest rates of evolution in the Triassic, and those rates declined substantially through time. On the other hand, squamates show a further step-up in rates during the Neogene, the past 23 Myr. The peak in evolutionary rates towards the present is particularly acute when using the MBL method, in what we regard as an artifact due to the condensing of divergence dates towards the present. These evolutionary rates are not the result of choosing a specific phylogenetic context – the black line represents summed rates for all lepidosaurs using the phylogenomic constrained trees, and the dashed gray line the rates from unconstrained morphological trees, with iguanians and fossorial species in traditional positions. This alternative version yields a similar general result, where the Late Jurassic peak is again clearly recovered (see Figure 4—figure supplements 14–22). In both cases, most parsimonious trees (MPTs) were randomly selected and dated five times according to each of the three dating methods, and evolutionary rates were calculated for each of the resulting dated trees. The curve shown represents average evolutionary rates among those calculated using the randomly selected MPT’s and the equal method (see Figure 4—figure supplements 5–22 for results according to all methods). The Late Jurassic peak in evolutionary rates is thus also robust to changes in the particular (randomly selected) point inside the stratigraphical range of a given fossil, and to different methods of dating the trees, including ‘equal’ and ‘Hedman’ methodologies, but not the ‘MBL’ method (but see the discussion for a possible explanation).

In exploring the nature of the ‘early burst’ in squamate disparity, we wanted to understand how the different clades occupied morphospace. Such an early establishment of squamate morphospace has never been documented in the few studies dealing with early radiations of squamates (e.g., Simões et al., 2020). Our finding that morphospace dimensions were established as early as the Middle or Late Jurassic is a counterintuitive result because it substantially predates the apparent increase in species richness that is usually tied to the KTR. Also, the high morphological rates recovered by a similar approach in Simões et al., 2020 applied to a different dataset of lepidosaurs plus a wide array of other diapsids (Simões et al., 2018) are in their case not correlated to a high disparity. In the latter study, morphospace was not plotted through time, so our time series (Figure 2) or chronophylomorphospace (Figure 3D) have no counterpart in their results.

It is also interesting to observe so little addition to squamate morphospace after its establishment; the great expansion in species numbers up to 10,000 today has happened partly by minor expansions of the total morphospace envelope, but mainly by packing ever more species inside the existing morphospace area. Although we would expect that a more fine-tuned grouping of ecomorphotypes would reveal minor changes in the specific portions of occupied morphospace, it is unlikely that such improvement in resolution would change the recovered outer limits of morphospace.

The total morphospace (Figures 2 and 3A) confirms the central location of stem lepidosaurs, and that rhynchocephalians and squamates explored distinct morphospace throughout their evolution (see their spread along PCO2). Martínez et al., 2021 reported that rhynchocephalians seem to present a lower proportion of morphological traits not shared with other diapsids than squamates do, which they interpreted as supporting the traditional view of rhynchocephalians as retaining a more plesiomorphic morphotype than squamates. Although our dataset is not comparable in the sense that it does not contain such a wide array of non-lepidosaurian diapsids, our morphospace, showing stem lepidosaurs in an intermediate position between squamates and rhynchocephalians, does not seem to support a plesiomorphic morphology for the latter. Our results are in line with current reinterpretations of many supposedly plesiomorphic traits of rhynchocephalians as actually derived in the context of Lepidosauromorpha. Regarding the distribution of squamates groups in particular, in our 2D phylomorphospace (Figure 3B) the squamate clades that lie furthest from the centroid are anguimorphs and marine mosasaurs (forming cluster 3) as well as amphisbaenians (worm lizards), dibamids (blind skinks), and snakes (forming cluster 4, associated with the limbless morphotype). A more detailed distribution of clades through the morphospace is represented in Figure 3—figure supplement 4.

Simões et al., 2020 reported a comparable morphospace for lepidosaurs, where rhynchocephalians and squamates do not overlap in morphospace, and squamates are mainly divided into limbed (lizards) and limbless (snakes and amphisbaenians) taxa. However, their large sample of non-lepidosaur diapsids forced a relatively low sample of lepidosaurs (in comparison to our study) that resulted in a loss of resolution for lepidosaur and squamate morphospace. It is worth noting that our morphospace is also similar to the one recovered by Watanabe et al., 2019 as based on skull geometric morphometrics, in identifying a cluster of snakes (and other limbless taxa like amphisbaenians and dibamids), anguimorphs, and mosasaurs at another pole, and a poor differentiation between other lizard groups (what we regard as ‘generalized lizards’).

The 3D phylomorphospace (Figure 3C, Supplementary files 4 and 5) shows how additional variation along PCO3 reveals the separation of several lizard morphotypes. This morphospace is easier to interpret in the 3D interactive plot (Supplementary file 5), which more clearly separates amphisbaenians and dibamids from snakes, the latter occupying an intermediate position between the two former clades and anguimorphs along PCO3. The inclusion of PCO3 slightly improves separation among ‘generalized lizards,’ although some clades persist as mixed groups in morphospace (e.g., scincids and gekkotans). However, PCO3 separates limbed (e.g., Eumeces and Acontias) from limbless (Typhlacontias and Feylinia) scincids. There is also a superposition between iguanians and the portion of anguimorphs that is closer to the middle part PCO3, which seem to represent less specialized anguimorphs (e.g., Elgaria) than those at the edge (varanid-like forms). In our opinion, all available studies (including ours) fail in fine-tuning ecomorphological groups of squamates, hinting at a problem that seems to be shared to both types of source data (discrete morphological characters and morphometric data). Ours is, however, the first study to track lepidosauromorph morphospace changes through time.

The chronophylomorphospace (Figure 3D) highlights the Mid–Late Jurassic expansion of morphospace, linked with the first radiation of the novel ‘snake-like’ morphology (see also Appendix 3—figure 1), but also that of clearly predatory forms as represented by Dorsetisaurus. In our interpretation, the first event (JME) is tracking the initial radiation of total group Squamata, when the clade radiated into its main components, as revealed by the branching timing of the dated trees, the primary expansions seen in morphospace plots, the Late Jurassic peak in disparity, and the Late Jurassic peak in evolutionary rates. This is particularly true for the trees dated using the Hedman and equal methods, but in the case of the MBL method the signal is overprinted by the high concentration of short branches close to the present time, which result in artificially higher rates for that period, and relatively lower Mesozoic peaks. Besides the MJE, a second event, which fits well with the timing of the KTR, would be coincident with the radiation of the constituent crown groups of Squamata as revealed by a limited expansion and infilling of morphospace plus the record of coincident peaks of disparity and evolutionary rates. Whether this second event represents an actual event of diversification among squamates or is the result of a greatly improved fossil record remains unclear.

Our study offers a new perspective on the early evolution of the major clade Squamata and the other groups of lepidosauromorphs. It benefits from current phylogenomic evidence on phylogeny, as well as fossil data on the timings of events and the expansion of skeletal morphologies and disparity. Our results show that, although the first assemblages of lizards (and possibly snakes) in the Middle–Late Jurassic are not particularly diverse or abundant, the basic structure of the present morphospace distribution had already been achieved (Figures 2 and 3D, Appendix 3—figure 1). This is independent of the interpretation of the affinities of a given taxon because the points in morphospace do not change with changes in topology (only the branches uniting them in phylomorphospaces). Finding support for this early burst of disparity and associated rapid evolutionary rates was rather unexpected, especially so long before the KTR – a reported key driver of squamate evolution (Gauthier et al., 2012) – and before a good fossil record is documented.

Further, we confirm that these distributions in morphospace, marking broad ecological and functional groupings, were remarkably stable for the subsequent 150 Myr, through to the present day (Figure 2, Figure 2—figure supplements 1–6). In other words, the range of adaptations in the current huge diversity of squamate species tracks back very deep in Earth history, some 60 Myr before the KTR. The only observable changes from then on correspond to a slight expansion of the edges of the occupied morphospace, and a notable increase in the density of points filling this morphospace. We acknowledge, however, that the recovered structure represents a simplification that only corresponds to groups according to general bauplans (e.g., limbed vs. limbless morphotypes) and, to a lesser degree, adaptations achieved by specific clades like, for example, anguimorphs. It is thus not possible to track finer ecomorphologies like, for example, adaptations of snakes to different environments (marine, fossorial, or ground-dwelling), which would likely add some variability in the form of shifts in the occupied morphospace through time. Although this is possibly related, in part, to the use of a phylogenetic morphological matrix that was constructed to capture the deep phylogenetic relationships of the constituent groups inside Squamata, it is worth noting that our morphospace is not too different from one recovered from a geometric morphometrics approach (Watanabe et al., 2019), suggesting that this poor resolution is not entirely explained by this procedural choice.

As a final note on squamate morphospace distribution and evolutionary rates, the results presented here also differ from recently published studies dealing with dentition shape, jaw size disparity (as informed by geometric morphometrics Herrera-Flores et al., 2021a), and body size as a continuous character (Herrera-Flores et al., 2021b). In the latter, even though the divergence times for most clades were in line with our results (they applied the Hedman method to their dataset), their results on evolutionary rates greatly differ from the ones presented here. Our study here yields consistently higher rates for squamates than rhynchocephalians, when the opposite trend was recovered in reference (Herrera-Flores et al., 2021b). Moreover, our results show a trend of decreasing evolutionary rates for rhynchocephalians through time, whereas the opposite was recovered by Herrera-Flores et al., 2021b through the Mesozoic, with a marked increase across the Jurassic–Cretaceous boundary. We regard these striking differences as related to the radically different sources of information used in both studies. Although differences in body size can be used to track shifts in evolution and, accordingly, to hint at macroevolutionary patterns, they do not need to be necessarily related to the same processes explored here. Both mentioned studies (Herrera-Flores et al., 2021b; Herrera-Flores et al., 2021a) dealt with particular aspects of lepidosaur evolution (body size and dentition/diet), whereas the results presented here are derived from an approach that considered many different ecomorphological aspects (as many as can be reflected in a morphological matrix that includes osteological characters for the entire skeleton, as well as soft-tissue characters). In addition, the focus on Mesozoic taxa in the aforementioned studies make the results obtained here, which include a good representation of extant taxa, difficult to compare.

It is important to consider whether results could represent bias in the fossil record. It is well understood that the Mesozoic fossil record of squamates is patchy, including some very poorly sampled time intervals (Cleary et al., 2018; Evans, 2003). As a counter to this concern, we note that the occupied total squamate morphospace in the Middle–Late Jurassic is just slightly smaller than that for the Late Cretaceous or the Paleogene to extant time bin (Figure 2), even though the two latter have yielded much higher sample sizes of specimens (Appendix 1—figure 5) that are also anatomically more complete (Appendix 1—figures 1–4). In particular, note that the morphospaces through geological time, from the Middle Jurassic onwards, are not much smaller than the morphospaces occupied by the represented sample among 10,000-strong extant squamates. Therefore, we have either identified more or less the correct extent of morphospace for the Middle to Late Jurassic, despite the poor fossil record at that time, or that with much richer finds from that time interval occupied morphospace was even larger than we identify here. This would then enhance our interpretation of an early burst in squamate morphology and function. We posit that our conclusions regarding morphospace expansion are not affected by sampling; we predict that new fossil finds in the future will mostly fit inside the demarcated area of occupied morphospace.

Our interpretation here of the long-term stable morphospace occupation by squamates is compelling because the apparent increase in species richness through time, even if partially influenced by bias in the fossil record (Cleary et al., 2018), is not linked to a great increase in occupied morphospace. The observed expansion in occupied morphospace and rapid evolutionary rates coincides not only with the first presence of squamates in the fossil record, but also with the time when many crown groups are first recorded (e.g., scincoids, anguimorphs, and likely gekkotans and snakes), in the Middle–Late Jurassic (Evans, 2003; Caldwell et al., 2015; Estes, 1983; Evans, 2008; Figure 1). The Jurassic expansion of squamates is further supported by (1) the fact that all three main squamate morphological groups in morphospace (clusters 2–4) are already present in the Middle–Late Jurassic bin (Figure 2); (2) bootstrapped and rarefied measures of disparity through time (Figure 4A) present a peak roughly corresponding to the Late Jurassic for all lepidosaurs and for squamates alone; and (3) the evolutionary rates calculations also show peak in the Late Jurassic (Figure 4B).

This explosive adaptive radiation of squamates in the Middle–Late Jurassic situates the dates of origin of major clades in line with current phylogenomic analyses (Mulcahy et al., 2012; Zheng and Wiens, 2016; Pyron, 2017; Burbrink et al., 2020), mostly into the Jurassic, except for some groups in the Hedman trees, the divergence ages of which are even older, placed in the Triassic. It is worth noting that other key tetrapod groups also radiated ecologically in the Jurassic, namely, illustrated by the rapid diversification of paravians, the clade including birds and related small, feathered theropods with elongate wing-like arms (Lee et al., 2014; Puttick et al., 2014; Brusatte et al., 2015) and the expansion of early mammalian clades (Close et al., 2015). This predates the second ecological expansion of these three major clades, accounting for more than 95% of the modern biodiversity of tetrapods, which happened in the mid-Cretaceous in association with the KTR (Lloyd et al., 2008; Doyle, 2008; Benton, 2010; Meredith et al., 2011; Cardinal and Danforth, 2013), when diversity, and probably also abundance, exploded in line with the new food resources on land. Squamates remained at low diversity through the Triassic (where unambiguous fossils are yet to be recovered, but supposed to be present), Jurassic, and Early Cretaceous (Jones et al., 2013; Caldwell et al., 2015; Evans, 2008), and species richness seems to have risen massively during the KTR some 100 Ma, but the morphological expansion had already happened some 60 Myr earlier, in the Middle to Late Jurassic. This seems to fit an already identified pattern where the main diapsid groups present a long chronological lag between the initial phenotypic radiation of the group and its subsequent taxonomic diversification (Simões et al., 2020; Close et al., 2019) or, alternatively, it is related to a failure of an impoverished fossil record to reveal the true diversity achieved in pre-Late Cretaceous times.

What was happening in the Middle Jurassic that could have triggered squamate morphological diversity? (1) The supercontinent Pangaea began to split into precursors of the modern continents; (2) temperatures rose sharply for a short time; (3) gymnosperm plants diversified; and (4) various insect groups (e.g., mayflies, crickets, cockroaches, bugs, cicadas) diversified. All these factors may have had a role in driving some aspects of the early burst of squamate disparity, and they all require further investigation. This early radiation of squamates had been previously inferred (Evans, 1998; Evans, 2003) on the basis of a crude interpretation of the fossil record and tree topologies. However, it is the first time this issue has been approached with quantitative methods involving such an array of diverse points of view (phylogeny, dating, fossil record, morphospace, disparity, and evolutionary rates). Moreover, most of the Jurassic forms are very difficult to classify, and many of them have been reinterpreted since this was proposed (e.g., Marmoretta, see Griffiths et al., 2021). Our methods, however, do not necessarily rely on the achieved identification of each fossil because they feed on the morphological information stored in the character matrix, and not the specific topology derived from its analysis. Thus, the method used accounts for possible shifts in the phylogenetic position recovered for each form.

In their later evolution in the Mesozoic, all living clades of squamates diversified rapidly through the KTR. In addition, new and short-lived squamate groups arose in the Late Cretaceous, such as the terrestrial borioteiioids and the marine mosasaurs and relatives, but they disappeared, together with non-avian dinosaurs and other groups of diapsids at the end of the Cretaceous. The non-survival of such groups emphasizes the importance of the origin of the key modern clades in the Middle Jurassic and the establishment of their key ecomorphological adaptations – these then proved robust to various crises, including the end-Cretaceous mass extinction. Our integrative study here, incorporating current phylogenomic analyses of relationships of squamate clades with current fossil data, and novel computational methods in disparity and evolutionary rates, provides a synthetic narrative of the origin of one-third of modern tetrapod biodiversity, the Squamata.

Although morphological matrices might not be ideal for macroevolutionary inferences because they were specifically built for inferring phylogenetic relationships, they are handy in that they represent readily available sources of information, and they allow the mixture of taxa for which ecology is known (extant taxa) and taxa for which it can only be inferred (fossils). Moreover, results actually show that some ecomorphological signal is present in such datasets. Although the recovery of a limbless cluster of taxa might seem trivial, in fact it shows that the ecomorphological signal is overprinting the phylogenetic signal in that case because otherwise snakes and amphisbaenians would cluster with their respective closer clades (anguimorphs and iguanians for the former, lacertids for the latter). There are many other examples of this convergence in morphospace that can be interpreted as related to ecological niche convergence, for example, xantusiids and gekkotans, two groups that are not closely related phylogenetically but greatly overlap in our morphospace. The tight clustering of multiple groups close to the centroid does not help in interpretation, but the overall morphospace distribution shares many similarities with the niche plots reported by reference (Pianka et al., 2017) according to extant taxa scored for five niche dimensions. Their Figure 4 perfectly shows that a mixture of niche conservatism (phylogenetically close taxa tend to occupy similar niches) and niche convergence (distantly related species with similar ecomorphology tend to cluster together) occurs. Although represented taxa are not completely comparable (Pianka et al.’s dataset includes only lizards, lacking snakes and amphisbaenians among squamates, and also rhynchocephalians), and even the lizards sampled are different at the genus or species levels, similarities between our morphospace plot and their niche plot for extant groups include (1) anguimorphans are in both cases the most differentiated group, far from a much more populated cluster of taxa around the centroid that includes most of the rest of lizards; (2) this centered cluster includes scincoids, lacertoids, gekkotans, and some iguanians in our plot, whereas in Pianka’s plot gekkotans and most iguanians overlap outside this cluster, in the opposite direction of anguimorphans along PC1; and (3) small teiids overlap lacertids in both cases, but large teiids (Dracaena and Tupinambis in our case, Tupinambis in the Pianka et al.’s plot) are closer to anguimorphs.

Macroevolutionary studies can be strongly influenced by an array of potential biases that sometimes compromise results to variable degrees. Several potential issues have been identified through the design, development, and review of this study, ranging from sampling to methodological and interpretative factors. Moreover, methods are quickly evolving and can be quickly displaced by more refined approaches or criticized in their use or misuse. We have made an effort to consider as many variables as possible by assessing multiple potential resolutions for the phylogenies (constrained vs. unconstrained), specific changes in topology (by randomly selecting multiple MPTs), dating (by using three different methods, and randomly dating each fossil tip multiple times, accounting for geological range uncertainty), and by using multiple metrics and time bins when necessary. Other factors, like the possibility that our results are biased by the nature of the fossil record and how it conditions effective sampling across different time bins, are difficult to circumvent. We think, however, that if the poor fossil record is affecting results, it is most probably undermining the effect of the JME because (1) we have not been able to include any of the known Middle Jurassic squamate fossils and (2) the Late Jurassic contains a low number of samples compared to the Early and Late Cretaceous.

Among other studies that have emphasized the importance of the KTR in squamate evolution is Lafuma et al., 2021. In a study of origins and losses of tooth complexity across the clade, they found that tooth complexity first increased in the Late Jurassic, although it is regarded as marginal until the KTR. This increase in tooth complexity is apparent when its distribution through the Jurassic and Cretaceous is analyzed, but the possibility that the change in the quality of the fossil record might be enhancing the much more complete sample occurring in the Late Cretaceous is not discussed. Further, lumping the diverse morphologies of unicuspid teeth into a single category is potentially problematic if carnivores and insectivores are to be considered as distinct styles of predators. Another interesting but ignored result of that study is that, besides presenting a Cretaceous turnover (speciation/extinction) peak coinciding with the KTR, there is a previous peak mostly coinciding with the Jurassic–Cretaceous boundary. In any case, it seems that there is a shared pattern to our results, where innovations are initially explored in the Jurassic and then fully exploited in the Cretaceous, coinciding with the KTR.

To the uncertainty generated by the incomplete fossils that can only be scored for a minor portion of the morphological characters, we face the added problem of unscorable characters. In a morphological matrix of characters for lepidosaurs, this is not a minor issue because there is a long list of characters that cannot be scored for multiple groups, for example, characters related to limbs in limbless taxa, or characters related to structures only found in the snake skull. Even though the use of inapplicable characters has been discouraged (Gerber and Ruta, 2019), we think that simply removing them from the analyses is not the best solution, just as it would not be for a phylogenetic analysis.

Finally, results that directly depend on the estimation of time-calibrated branch lengths, such as the calculation of evolutionary rates, should be treated as preliminary because they must be validated under the use of more robust methods of time calibration, such as those that incorporate molecular data alongside the fossil record, as well as employ more realistic models of diversification such as the fossilized birth–death prior. In this sense, an ongoing study (work in progress) aims to analyze the present matrix and other datasets by using Bayesian tip dating under relaxed morphological clocks as described in Zhang and Wang, 2019. This allows us to calculate phylogeny and estimate divergence times and evolutionary rates while accounting for their uncertainties, and allow the use of both morphological and combined (morphological plus molecular data) matrices. This additional study should help clarify if the signal recovered in this work is reliable, or on the contrary it is biased by the chosen methodology. Meanwhile, the results presented here question the alternative view that regards the great diversification of squamates as occurring in the mid-Cretaceous, coinciding with the KTR. The first half of the Mesozoic has a great potential for unveiling the key milestones in the evolutionary history of lepidosauromorphs in general, but also of squamates in particular. Current reanalyses of classic material and the description of new specimens and taxa are already displacing the focus from the Late Cretaceous to the first half of the Mesozoic and are expected to provide insights on the issue presented here.

All data generated or analysed during this study are included in the manuscript and supporting files. More specifically, all necessary files (Nexus files and source tables) are included in the Source code 1–4.

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Author details

1. Arnau Bolet

   1. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain
   2. School of Earth Sciences, University of Bristol, Bristol, United Kingdom

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Visualization, Writing - original draft, Writing – review and editing

   For correspondence

   arnau.bolet@icp.cat

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4416-4560

2. Thomas L Stubbs

   School of Earth Sciences, University of Bristol, Bristol, United Kingdom

   Contribution

   Methodology, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7358-1051

3. Jorge A Herrera-Flores

   School of Earth Sciences, University of Bristol, Bristol, United Kingdom

   Contribution

   Conceptualization, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9660-4161

4. Michael J Benton

   School of Earth Sciences, University of Bristol, Bristol, United Kingdom

   Contribution

   Conceptualization, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4323-1824

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