Two related species of salamanders were found living on opposite sides of a mountain

Ecological preferences and life history strategies have enormous impacts on the evolution and phenotypic diversity of salamanders, but the yet established reliable ecological indicators from bony skeletons hinder investigations into the paleobiology of early salamanders. Here, we statistically demonstrate by using time-calibrated cladograms and geometric morphometric analysis on 71 specimens in 36 species, that both the shape of the palate and many non-shape covariates particularly associated with vomerine teeth are ecologically informative in early stem- and basal crown-group salamanders. Disparity patterns within the morphospace of the palate in ecological preferences, life history strategies, and taxonomic affiliations were analyzed in detail, and evolutionary rates and ancestral states of the palate were reconstructed. Our results show that the palate is heavily impacted by convergence constrained by feeding mechanisms and also exhibits clear stepwise evolutionary patterns with alternative phenotypic configurations to cope with similar functional demand. Salamanders are diversified ecologically before the Middle Jurassic and achieved all their present ecological preferences in the Early Cretaceous. Our results reveal that the last common ancestor of all salamanders share with other modern amphibians a unified biphasic ecological preference, and metamorphosis is significant in the expansion of ecomorphospace of the palate in early salamanders.

This paper is a valuable contribution to evolutionary ecomorphology in extant and extinct tetrapods, and of interest to vertebrate paleontologists and other evolutionary biologists interested in the early evolution of amphibians. Using geometric morphometric analysis, the authors demonstrate that both the shape of the palate and several non-shape variables [particularly associated with vomerine teeth] are ecologically informative in early stem- and basal crown-group salamanders. The study also reveals that metamorphosis is significant in the expansion of ecomorphospace of the palate in early salamanders.

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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 19th 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.

[A] The vomer [gold] and parasphenoid [purple] of the palate in ventral view of the skull in living hynobiid Pseudohynobius flavomaculatus. [B] Dorsal view of the palate showing the articulation patterns with the paired orbitosphenoid [whitish]. [C] Enlarged view of the palate in ventral view with red circles corresponding to the 24 landmarks used for the geometric morphometric analysis. [D] Palatal configurations of early salamanders in ventral view, with color-coded life history strategies [square block] and ecological preferences [line] plotted on the time-calibrated tree modified from Jetz and Pyron, 2018 and Jia et al., 2021a.

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.