Salamanders, anurans, and caecilians are highly distinctive from one another in their morphology in both living species and their respective oldest known relatives from the Triassic (Ivachnenko, 1978; Ascarrunz et al., 2016; Pardo et al., 2017a; Schoch et al., 2020; Kligman et al., 2021). As a result, the evolutionary origin(s) of modern amphibians have remained controversial since the late 19^th century (Haeckel, 1866), with a number of extinct tetrapod groups in different ecological types at adult stages having been hypothesized as their purported ancestors, including: amphibamid (terrestrial) and branchiosaurid (terrestrial and aquatic) dissorophoid temnospondyls (Laurin et al., 2004; Fröbisch and Schoch, 2009; Maddin and Anderson, 2012; Pardo et al., 2017b), stereospondylian (semiaquatic/aquatic) temnospondyls (Schoch and Milner, 2014; Pardo et al., 2017a), and several groups of lepospondyls (aquatic, semiaquatic or terrestrial; Marjanović and Laurin, 2013; Marjanović and Laurin, 2019; Jansen and Marjanović, 2021; Laurin et al., 2022). The specialized morphologies in modern amphibians are greatly impacted by ecology and their complex life history strategies (e.g. Wake, 2009), for example, even the earliest anuran Triadobatrachus and the possible caecilian Chinlestegophis from the Triassic display several morphological specializations as their living relatives for aboveground and subterranean terrestrial living settings, respectively. Salamanders (or Caudata, the total group), on the other hand, have a more conservative body plan and more diversified ecological preferences when compared to anurans and caecilians (Deban and Wake, 2000; Bonett and Blair, 2017; Fabre et al., 2020), and have been frequently used as comparative analogues for inferring the paleoecology of extinct tetrapods (Schoch and Fröbisch, 2006; Fröbisch and Schoch, 2009). However, the evolutionary paleoecology in modern amphibians and particularly in early salamanders has received insufficient attention.

Cryptobranchoidea is the sister group of all other crown group salamanders (Urodela) and contains two subclades: Pancryptobrancha (total group cryptobranchids; Vasilyan et al., 2013) and Panhynobia (total group hynobiids; Jia et al., 2021a). The two subclades are united by a set of synapomorphies (Dunn, 1922; Estes, 1981; Jia et al., 2021a), but are different from each other in life history strategies and ecological preferences at their respective adult stage: most pancryptobranchans are neotenic or partially metamorphosed and live in water permanently by retaining larval features (e.g. gill slits), albeit the pancryptobranchan Aviturus from the Paleocene was interpreted as semiaquatic with an unknown life history strategy (Vasilyan and Böhme, 2012; but see Skutschas et al., 2018). In contrast, panhynobians are predominantly metamorphosed, except that the stem hynobiid Regalerpeton from Early Cretaceous (Rong, 2018) and some populations of the living hynobiid Batrachuperus londongensis are neotenic (Jiang et al., 2018). Postmetamorphosed hynobiids have lost larval features and are characterized by an anterolaterally directed palatal ramus of the pterygoid, and are able to live in water (e.g. Paradactylodon), on land (e.g. Hynobius) or are semiaquatic (Ranodon) outside of the breeding season (Kuzmin and Thiesmeier, 2001; Fei et al., 2006; Materials and methods).

Cryptobranchoidea are critical in understanding the paleoecology of early salamanders because the earliest known cryptobranchoids from the Middle Jurassic (Bathonian) have higher disparities in both life history strategies and ecological preferences than stem urodeles, and represent the oldest known crown urodeles, including ‘Kirtlington salamander B’ from the UK, Kiyatriton krasnolutskii from Russia, and Chunerpeton, Neimengtriton, and Jeholotriton from China (Evans and Milner, 1994; Gao et al., 2013; Skutschas, 2015; Jia et al., 2021a). Both Chunerpeton and Jeholotriton are neotenic as confirmed by the presence of external gills and a tall caudal dorsal fin in adult specimens (Gao and Shubin, 2003; Wang and Rose, 2005), whereas Neimengtriton is the oldest metamorphosed and semiaquatic cryptobranchoid (Jia et al., 2021a; see below). The ‘Kirtlington salamander B’ and K. krasnolutskii are both represented by fragmentary materials and their paleoecology unfortunately remains unknown. In contrast, other contemporaries (e.g. Kokartus, Marmorerpeton) from the Middle Jurassic (Bathonian) of UK, Russia, and Kyrgyzstan are all neotenic and aquatic at their adult stage, and have been classified as stem urodeles by the absence of spinal nerve foramina in the atlas that characterizes Urodela (Ivachnenko, 1978; Evans et al., 1988; Skutschas and Krasnolutskii, 2011; Skutschas and Martin, 2011; Skutschas, 2013; Skutschas et al., 2020). The only known pre-Jurassic stem urodele, Triassurus from the Middle/Upper Triassic of Kyrgyzstan, is merely represented by two larval specimens with no clue to its paleoecology at adult stage (Schoch et al., 2020).

To date, seven other basal cryptobranchoids have been reported from the Upper Jurassic to Lower Cretaceous of northern China: Laccotriton, Liaoxitriton, Linglongtriton, Nuominerpeton, Pangerpeton, Regalerpeton, and Sinerpeton, most of which are represented by articulated specimens and have been recently recovered as stem hynobiids or hynobiid-like taxa (see Gao et al., 2013; Jia and Gao, 2016; Jia and Gao, 2019; Jia et al., 2021a). Besides the neotenic Regalerpeton as aforementioned, habitat preferences of these metamorphosed taxa and paleoecological disparity patterns of Cryptobranchoidea remain largely unexplored mainly due to yet established osteological indicators for ecology (see Discussion). The configuration of vomerine teeth has long been identified as useful for the classification of living cryptobranchoids (Zhao and Hu, 1984) and was recently claimed to be ecologically informative (Jia et al., 2021b), but such statements have not received rigorous tests with inclusion of fossil taxa.

Our series of studies on living and fossil cryptobranchoids noticed that besides the vomerine teeth, the palate varies in shape and proportion, and could potentially serve as an indicator for paleoecological reconstruction (Jiang et al., 2018; Jia et al., 2019; Jia et al., 2021b; Figure 1 and Figure 1—figure supplements 1–23). To test these hypotheses and to address the constraints underlying the morphological disparity of the palate, here we conducted a 2D landmark-based geometric morphometric analysis on the palate of all living and most aforementioned fossil genera of cryptobranchoids, stem, and other basal crown urodeles based primarily on micro-CT scanned specimens. We statistically investigated disparity patterns within the morphospace of the palate with respect to ecological preferences, life history strategies, and taxonomic affiliations. Based on a time-calibrated cladogram we established for fossil and living cryptobranchoids (Jetz and Pyron, 2018; Jia et al., 2021a), we further quantified the evolutionary rate of the palate and reconstructed the ancestral states for ecological preferences, life history strategies, palate shape, and vomerine tooth configurations of the respective last common ancestor of Panhynobia, Pancryptobrancha, Cryptobranchoidea, Urodela, and Caudata. We demonstrate that the palate is a reliable proxy in ecological reconstructions for early salamanders, and the morphospace of the palate is predominantly shaped by ecological constraints and also displays a stepwise evolutionary pattern.

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In ventral view of the palate, the anteromedial fenestra is present between the vomer and the upper jaw in most early salamanders and is only absent in living cryptobranchids (Figure 1—figure supplements 1–23). The paired vomers medially articulate with each other in most taxa and posteriorly overlap to different extents, the anterior part of the cultriform process of the parasphenoid and/or the orbitosphenoid. The teeth are closely packed as a continuous tooth row positioned along the anterolateral periphery of the vomer in cryptobranchids but have diversified configurations in other taxa. The parasphenoid is a sword-like, azygous bony plate with its anterior part articulating dorsally with the orbitosphenoid and its posterior part flooring the otic capsule.

Morphospace and shape disparity patterns of the palate in early salamanders

The palate is symmetric about the mid-sagittal plane of the skull with symmetric shape components accounting for 96.15% of the total shape variation in 70 specimens, and the left-right asymmetry accounting for the remaining 3.85%. The shape and the size of the palate with the latter represented by the centroid size (CS), are significantly correlated as revealed by the standard multivariate regression between log (CS) (independent variable) and symmetric shape components (dependent variable) across 70 specimens (R² = 9.3331%; p<0.001; F = 6.9977; Z = 3.918) and 34 species (R² = 13.276%; p<0.001; F = 4.8985; Z = 3.1691). However, when phylogenetic relationships of the 34 species were factored in, the association between size and shape of the palate is no longer significant as shown in the evolutionary allometry analysis (p=0.1583). Such inconsistency between standard and evolutionary allometry analyses is related to the fact that the CS of the palate has a strong phylogenetic signal (Blomberg’s K = 0.997, p=0.001, Z = 4.1921) and, hence, the CS accounts for an even smaller amount of shape variations of the palate (R² = 4.494%; F = 1.5059; Z = 1.0141) when evolutionary history among species was counterbalanced in the evolutionary allometry analysis. To eliminate impacts from both asymmetry and allometry on the spatial patterns of the palate, residuals from the multivariate regression of symmetric shape components on log (CS) were retained for downstream statistical analyses.

To visualize the spatial patterns of the palate in the morphospace, on the basis of the size-corrected (allometry-free) 24-landmark dataset, we conducted a standard principal component analysis (PCA) across 70 specimens; and we also conducted three other types of PCA across 34 species with the time-calibrated cladogram and ancestral internal nodes projected into the morphospace (Figure 2—figure supplements 1–3), including: a phylomorphospace analysis (PA), phylogenetic principal component analysis (Phylo-PCA) and a phylogenetically-aligned components analysis (PaCA). The first three PC axes in each of the four PCAs collectively measure up to about 70% of total shape variances (Supplementary file 1A). Within the phylomorphospace defined by principal components (PCs) 1–2 (Figure 2B and Figure 2—figure supplement 1b), aquatic and terrestrial living species of Cryptobranchoidea are generally located along the positive and negative interval of the PC 2 axis (21.35%), respectively. Most taxa are ecologically exclusive at the genus level, except that Liua and Paradactylodon are the only two living hynobiid genera with species occupying both the aquatic (Liua shihi and Paradactylodon mustersi) and terrestrial (Liua tsinpaensis and Paradactylodon persicus) zones. The living semiaquatic hynobiid Ranodon sibiricus occupies at a location intermediate between the aquatic and terrestrial zones. Shape changes of the palate relative to the mean shape of all terminal and internal taxa along the positive values of PC 2 (aquatic zone) involve an anteromedial extension of the vomer and therefore a reduction of the anteromedial fenestra, a shrinkage of the anterolateral and posterolateral borders of the vomer and the width of the cultriform process of the parasphenoid, and an anterior extension of the parasphenoid. In contrast, the negative values of PC 2 (terrestrial zone) characterize a shrinkage of the anteromedial border of the vomer and therefore a posterolaterally expanding anteromedial fenestra, a laterally widening retrochoanal process of the vomer and the cultriform process of the parasphenoid, and an anteroposteriorly shortening parasphenoid. On the other hand, basalmost crown urodeles (e.g. Beiyanerpeton, Chunerpeton, and Pangerpeton) and karaurids are largely separated from living taxa along the PC 1 axis (37.49%), with stem hynobiids widely scattered in the phylomorphospace and lying within either the aquatic (Liaoxitriton) or terrestrial (Linglongtriton and Nuominerpeton) zone. The only known aquatic stem hynobiid Regalerpeton is situated at a region of the aquatic zone occupied by other aquatic fossil taxa (e.g. Beiyanerpeton and Chunerpeton), whereas the semiaquatic stem hynobiid Neimengtriton occupies a location closer to terrestrial than either aquatic zone or the semiaquatic zone of extant hynobiids. From the largest to the smallest value of PC 1, both the vomer and the parasphenoid have an anteroposterior extension and the cultriform process of the parasphenoid changes from an anteriorly widened plate with an indented anterior edge into a bilaterally narrowed plate with a pointed anterior edge.

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The evolutionary history among species has a moderate but significant contribution in the formation of the spatial patterns in the phylomorphospace (phylogenetic signal: observed K_mult = 0.4154, p=0.001, Z = 4.9856). When the multivariate shape data of the palate were maximally aligned with phylogenetic signal (Figure 2C and Figure 2—figure supplement 1c), fossil taxa can be roughly divided from living taxa along PaCA-C 1. Both crown and stem taxa of Panhynobia are more compactly clustered than that seen in the phylomorphospace created by PA, and are distinct from the Pancryptobrancha and the region occupied by karaurids, basal cryptobranchoids and salamandroids; but taxa in different types of ecological preference are mixed together. By contrast, when the phylogenetic signals of the palate were eliminated by the Phylo-PCA (Figure 2D and Figure 2—figure supplement 1d), the overall spatial patterns among species are essentially preserved, albeit slightly rotated clockwise, as observed in the phylomorphospace. In this phylogeny-free morphospace, the last common ancestors of Pancryptobrancha and of Hynobiidae lie within the aquatic zone and are tightly associated with living cryptobranchids and the stem urodele Kokartus, respectively. In contrast, the last common ancestors of Panhynobia, Cryptobranchoidea, Urodela, and Caudata lie within the terrestrial zone and are adjacent to three highly derived living hynobiids, respectively, Pseudohynobius shuichengensis, Pseudohynobius jinfo, and Liua tsinpaensis.

Our pairwise comparison (Supplementary file 1B–E) and phylogenetic Procrustes ANOVA reinforce that the shape of the palate is significantly different among groups of species that are classified by ecological preference (R² = 28.079%; p=0.001; F = 4.3740; Z = 3.4838) and life history strategy (R² = 6.797%; p=0.006; F = 3.1766; Z = 2.4673), but not by taxonomic affiliations, neither at the genus (R² = 68.711%; p=0.248; F = 1.2549; Z = 0.78492) nor family (R² = 12.858%; p=0.581; F = 0.8263; Z = –0.21234) level. With regard to the life history strategy, living cryptobranchids are separated from all Mesozoic neotenic taxa including Beiyanerpeton, Chunerpeton, karaurids, and Regalerpeton by the vast majority of the metamorphosed taxa, which occupy most of the morphospace of the palate (Figure 2—figure supplement 4). The single living neotenic hynobiid B. londongensis is situated between the two neotenic groups as aforementioned and lies alongside its metamorphosed conspecifics and those all collectively overlap with other aquatic hynobiids. When the seven-landmark-dataset for the right vomer was analyzed following the same procedure, the purported semiaquatic basal pancryptobranchan Aviturus is nested within the terrestrial zone along with living metamorphosed taxa (Figure 2—figure supplement 5).

Evolutionary rates of the palate

The palate exhibits considerable differences in morphological disparity and evolutionary rates across regions represented by the 24-landmark points as calculated under a Brownian motion evolutionary model (Figure 3; Supplementary file 1B–H). The vomer evolves about two times faster than the parasphenoid, and such a pattern is also supported by the fact that the vomer has a higher phylogenetic signal (K_mult = 0.6407) than that of the palate (K_mult = 0.4154). The posterior border of the vomer and the medial-most part of the choanal notch are the fastest and the slowest evolving parts in the palate, respectively. In the parasphenoid, however, the highest evolutionary rates are concentrated on the anterior end, posterior end and the lateral alae, and the lowest evolutionary rates are located at the posterior contact between the cultriform process and the orbitosphenoid and the junction area where the cultriform process merges with the lateral alae.

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Species in different ecological (p=0.002, Z = 2.6284) and taxonomic (p=0.035, Z = 1.7594) groups vary greatly in evolutionary rate of the palate (Supplementary file 1H). Namely, aquatic and terrestrial taxa are comparable with each other in the evolutionary rate of the palate, the vomer and the parasphenoid, and both of them evolve at a rate that is less than half of that in semiaquatic taxa championed by Neimengtriton. Stem hynobiids have the highest evolutionary rates, followed successively by basal cryptobranchoids, pancryptobranchans, crown hynobiids, and non-cryptobranchoid basal salamanders. Neotenic and metamorphosed taxa are not significantly different from each other in evolutionary rates (p=0.843, Z = –1.1341).

Among modern amphibians, anurans, and caecilians undergo metamorphosis or direct development, and the adults of most species are terrestrial. In contrast, salamanders have their ecological preference decoupled from life history strategy, especially in metamorphosed taxa such as living and extinct hynobiids where postmetamorphosed adults live in water, on land or are semiaquatic (Fei et al., 2006; Jia and Gao, 2016; Jia et al., 2021a). The discrepancy in ecological preference between salamanders on one hand and anurans and caecilians on the other hand is unhelpful in understanding the evolutionary paleoecology in the early lissamphibians given that salamanders and anurans are sister-groups. Previous studies on fossil salamanders generally focus on the taxonomy, whereas the paleoecology and the evolutionary history of the ecological decoupling particularly in metamorphosed taxa had received insufficient attention, which is to some extent explained by the insufficient taphonomic analyses on fossil sites with salamander discoveries, such as the Daohugou fossil locality (Wang et al., 2019). The main obstacles are (1) sufficient and reliable ecological indicators in the bony skeleton have not yet been established for extant cryptobranchoids and early salamanders (Xiong et al., 2016; Jia et al., 2021b), and (2) soft anatomical structures (e.g. labial fold and caudal fin) and stomach contents that are ecologically informative, as commonly seen in lacustrine deposits of certain neotenic species (Dong et al., 2011), are rarely preserved in metamorphosed individuals. Here, we quantitively investigate the paleoecological turnover in the earliest known salamanders based on the shape and non-shape variables of the palate. Our results shed light on the interactions between morphology and paleoecology, and the underlying mechanisms governing ecomorphological diversity among early salamanders along the rise of modern amphibians.

As shown in the phylomorphospace, the shape of the palate in early salamanders is heavily impacted by convergence resulting from ecological disparity, as extant cryptobranchoids and fossil taxa in different ecological preferences occupy distinctive zones in the morphospace. Such spatial patterns remain essentially unaltered after phylogenetic signals are eliminated by the Phylo-PCA, along the first axis of which aquatic and terrestrial taxa regardless of their phylogenetic closeness are separated from each other, confirming our hypothesis that the shape of the palate is a reliable ecological indicator in early salamanders as reported in living salamanders (Fabre et al., 2020). As shown above, non-shape covariates of the palate particularly with regard to the VTR are also ecologically informative. The palate in aquatic species is characterized by a reduction of the anteromedial fenestra, a shrinkage of the vomer laterally and anteroposteriorly with fewer vomerine teeth, a high ratio of the outer to the inner branch of the VTR, a narrow VTR, and an elongated parasphenoid. On the other hand, the palate in terrestrial species is characterized by a posterolateral expansion of the anteromedial fenestra, an anteroposteriorly elongated vomer and a widened retrochoanal process with more vomerine teeth, a low ratio of the outer to inner branch of the VTR, a widened VTR, and an anteroposteriorly shortened parasphenoid. The palate in extant semiaquatic taxa is transitional in both the morphospace and many non-shape covariates between aquatic and terrestrial taxa as mentioned above, whereas the palate of the only known fossil semiaquatic salamander, Neimengtriton (Middle Jurassic) is configured more like that of terrestrial taxa as argued in the original study (Jia et al., 2021a), indicating that Neimengtriton is probably more adapted to terrestrial environments despite being semiaquatic. The respective last common ancestors for Caudata, Urodela, Cryptobranchoidea, and Panhynobia, the basal cryptobranchoid Pangerpeton (Late Jurassic) and the stem hynobiids Linglongtriton (Late Jurassic) and Nuominerpeton (Early Cretaceous) are terrestrial, whereas other stem hynobiids Liaoxitriton and Regalerpeton (Early Cretaceous) and the respective last common ancestors for Hynobiidae and Pancryptobrancha are aquatic, demonstrating that ecological shifts occurred frequently in the evolution of early salamanders. The Paleocene pancryptobranchan Aviturus is likely metamorphosed and terrestrial based on the shape and non-shape variables of the vomer, but this hypothesis awaits to be tested by the discovery of a more completely preserved palate.

Morphological adaptations in the palate and perhaps in other cranial features (e.g. hyobranchial apparatus; see Jia et al., 2021b) to aquatic and terrestrial living settings are likely constrained by feeding mechanisms (Regal, 1966; Reilly and Lauder, 1990). In extant cryptobranchoids, terrestrial species grasp prey items with their jaws and/or by their tongue protruding from the mouth; the captured prey is then transported from the snout into the esophagus with the assistance of several cyclical movements of tongue and hyobranchial apparatus that press and reposition the prey against the palate (Deban and Wake, 2000; Wake and Deban, 2000). Such feeding mechanisms in terrestrial cryptobranchoids demand a sticky tongue moisturized by the intermaxillary or internasal gland that is housed above an expanded anteromedial fenestra, a wide snout contributed by lateral expansions of the vomer, many vomerine teeth to efficiently hold the prey in place, and a shortened parasphenoid to reduce the distance of intraoral transportation. The posteriorly elongated inner branch of the VTR as represented by derived terrestrial hynobiids Hynobius and Salamandrella would serve as toothed surfaces that can further facilitate tongue manipulations and transportations of small prey items posteriorly as in more sophisticated terrestrial feeders (e.g. salamandrids and plethodontids; Regal, 1966). By contrast, aquatic salamander species capture their prey primarily by suction feeding in which the prey is carried into the biting range of the jaws by water currents created by retraction and expansion of the buccal walls, and giant salamanders can even perform asymmetrical strikes in water via unilateral jaw and hyobranchial movements (Gillis and Lauder, 1994). Intraoral transport of the prey is more efficient in aquatic than in terrestrial species; and it typically involves repeating the same procedure as in the initial suction strike and is occasionally assisted by tongue manipulations against the palate (Regal, 1966). The limited usage of the tongue in aquatic prey capture diminishes the need for moisturization from the intermaxillary or internasal gland which, in turn, may lead to reduction and closure of the anteromedial fenestra as seen in aquatic species. An anteroposterior expansion of the parasphenoid increases buccal volume, and the shrinkage of the vomer along both the mediolateral and anteroposterior dimensions reduces snout size; both features act in concert to boost the success of feeding attempts by creating a high negative buccal pressure. A narrow VTR with few teeth, most of which are located on the outer branch, likely serves to reduce hindering the influx of water and prey.

Whichever mode of prey capture and intraoral transportation cryptobranchoids perform, the palate undergoes a similar mechanical stress distribution pattern as found in species with different types of ecological preference and life history strategy (Fortuny et al., 2015: Andrias davidianus; Zhou et al., 2017: Salamandrella keyserlingii). Such findings reinforce that alternative morphological configurations of certain features in the palate cope well with similar functional demands, but do not necessarily indicate that other feeding-related features of the palate and other regions of the cranium would also exhibit such extensive convergence. For example, the ceratohyal has been argued to be ecologically informative in extant cryptobranchoids, as the ceratohyal is consistently ossified at its posterior end in aquatic species but remains cartilaginous in terrestrial taxa (Xiong et al., 2016; Jia et al., 2021b); however, the ceratohyal remains cartilaginous in all known early fossil stem and crown urodeles, and ossifications of the ceratohyal must represent a derived feature independently evolved in crown cryptobranchoids (Jia et al., 2021b). Interestingly, the palate of extant cryptobranchoids as shown in biomechanical analyses (Fortuny et al., 2015; Zhou et al., 2017) has the highest stress level concentrated in the most posterior part of the vomer and its sutural area with the parasphenoid and orbitosphenoid, which surprisingly correspond to the place with the highest evolutionary rate in the palate as revealed by our study. Here, we recognize a clear stepwise evolutionary pattern at the vomer-parasphenoid-orbitosphenoid sutural area in early salamanders (Figure 4). In stem (Karaurus and Kokartus) and many basal crown (Beiyanerpeton, Chunerpeton, Jeholotriton, Neimengtriton, Pangerpeton, and Qinglongtriton) urodeles from the Jurassic and the reconstructed respective last common ancestors for Panhynobia, Cryptobranchoidea, Urodela, and Caudata, the vomer has a limited contact with the parasphenoid, the cultriform process of the parasphenoid is anteriorly expanded bilaterally, and the orbitosphenoid has no anteroventral processes (see below) or in the case of Qinglongtriton remains completely cartilaginous. In three stem hynobiids (Liaoxitriton, Nuominerpeton, and Regalerpeton) and the reconstructed ancestors for Hynobiidae and Pancryptobrancha from the Cretaceous and another stem hynobiid Linglongtriton from the Late Jurassic, the vomer has an increased contact with the parasphenoid, the cultriform process of the parasphenoid is anteriorly constricted, and the orbitosphenoid lacks the anteroventral process. In living cryptobranchoids, the vomer is in more extensive contact with the parasphenoid and orbitosphenoid (Trueb, 1993: Cryptobranchus; Kuzmin and Thiesmeier, 2001: Ranodon; Jiang et al., 2018: Batrachuperus; Jia et al., 2021b: Pseudohynobius), the cultriform process of the parasphenoid is anteriorly constricted bilaterally, and the orbitosphenoid has a thick anteroventral process ossified from neighboring cartilages in the nasal capsule that projects medially and firmly overlaps the cultriform process of the parasphenoid. If similar biomechanical stress patterns existed in early salamanders, the stress and strain applying to the vomer/parasphenoid sutural area would be equally offset by either a wide and thin cultriform process of the parasphenoid with limited support from the vomer and the absence of anteroventral process of the orbitosphenoid as seen in Jurassic taxa, or a narrow cultriform process thickened by more extensive overlapping with the vomer as seen in Cretaceous and living taxa, and by ossification of the anteroventral process of the orbitosphenoid as seen solely in living taxa.

Figure 4

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It is worth emphasizing that the phenotypic diversity of the palate is variously affected by neoteny and metamorphosis. Neoteny is notable in producing convergent characters through truncation of normal developmental trajectories and its indirect role associated with constraints from the aquatic environment (Wiens et al., 2005). Most early stem and crown urodeles are neotenic (e.g. Chunerpeton and Kokartus) and their phenotypic diversity of the palate is truly confined to a restricted area in the spatial-temporal morphospace. However, extant neotenic cryptobranchids and the hynobiid B. londongensis bear an increased phenotypic diversity of the palate as compared to fossil neotenic taxa, and are separated from one another within the morphospace with the neotenic B. londongensis even overlapping with its metamorphosed conspecifics, indicating that constraints imposed by ecology have more influence than neoteny in the morphogenesis of the palate. The ecomorphospace of the palate is indeed greatly and rapidly expanded by metamorphosed taxa represented by basal cryptobranchoids and most stem hynobiids as these taxa have the highest evolutionary rate in the palate (Supplementary file 1H). The last common ancestors of Caudata, Urodela, and Cryptobranchoidea are reconstructed to be metamorphosed and terrestrial as evidenced by the shape and non-shape variables of the palate. Disparities of ecological preference among metamorphosed taxa must have taken place before the Middle Jurassic (Bathonian), because one of the oldest known crown urodeles, Neimengtriton, is metamorphosed and semiaquatic as evidenced by the presence of a low but pliable dorsal caudal fin at adult stage. Most of the current scope in the phenotypic diversity of the palate possessed by modern cryptobranchoids were achieved by Early Cretaceous. Our results rigorously show that the shape of the palate and many non-shape covariates particularly associated with vomerine teeth are reliable ecological indicators for paleoecology of early salamanders, and we demonstrate that metamorphosis with biphasic ecological preference (aquatic larvae + terrestrial adults) is not only the ancestral lifestyle in salamanders but also significant for the rise and diversification of modern amphibians.

All data needed to evaluate the conclusions are included in the manuscript and the Supplementary file 1. Details of specimens, CT parameters and raw landmark coordinates and centroid sizes are available in three CSV files in the online Dryad repository (https://doi.org/10.5061/dryad.c59zw3r8x). Source codes for R and SAS used in this study are available at GitHub (https://github.com/SalamanderGeomorph/Salamander_Palate, copy archived at swh:1:rev:8cbdd82025b0bf987bb6211239a2e7dc56c615d5).

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Author details

1. Jia Jia

   1. School of Earth and Space Sciences, Peking University, Beijing, China
   2. State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS), Nanjing, China
   3. Department of Comparative Biology and Experimental Medicine, University of Calgary, Calgary, Canada

   Contribution

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

   For correspondence

   jia.jia@ucalgary.ca

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8243-0156

2. Guangzhao Li

   Department of Microbiology, Immunology, and Tropical Medicine, The George Washington University, Washington D.C., United States

   Contribution

   Formal analysis, Methodology, Software, Validation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5007-8338

3. Ke-Qin Gao

   School of Earth and Space Sciences, Peking University, Beijing, China

   Contribution

   Data curation, Funding acquisition, Resources, Writing – review and editing

   For correspondence

   kqgao@pku.edu.cn

   Competing interests

   No competing interests declared

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