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Ecomorphological diversification in squamates from conserved pattern of cranial integration

Year: 2019
Authors: Akinobu Watanabe, Anne-Claire Fabre, Ryan N. Felice, Jessica A. Maisano, Johannes Mùˆller, Anthony Herrel, and Anjali Goswami
Journal: PNAS
Files: Hypothetical Ancestral Snake, Xenochrophis flavipunctatus, Xenophidion schaeferi, Xenopeltis unicolor, Xenodermus javanicus, Uromacer oxyrhynchus, Ungaliophis continentalis, Tropidophis haetianus, Trimorphodon biscutatus, Trimeresurus gramineus, Trachyboa boulengeri, Thamnophis marcianus, Sonora semiannulata, Sibynophis geminatus, Rena dulcis, Regina grahamae, Python molurus, Pseudoxenodon bambusicola, Psammophis sibilans, Prosymna ambigua, Philodryas olfersii, Pareas hamptoni, Oplurus cyclurus, Natrix natrix, Micrurus fulvius, Lycophidion capense, Loxocemus bicolor, Indotyphlops braminus, Lichanura trivirgata, Laticauda colubrina, Langaha madagascariensis, Lampropeltis getula, Lachesis stenophrys, Imantodes cenchoa, Homalopsis buccata, Heterodon platirhinos, Grayia smythii, Epicrates_cenchria, Enhydris enhydris, Eryx colubrinus, Elaphe dione, Drysdalia coronoides, Dipsas variegata, Diadophis punctatus, Daboia russelli, Cylindrophis ruffus, Coluber constrictor, Causus rhombeatus, Casarea dussumieri, Candoia carinata, Calliophis bivirgata, Calabaria reinhardii, Bothrops asper, Boaedon fuliginosus, Boa constrictor, Bitis arietans, Azemiops feae, Atractaspis irregularis, Aspidites melanocephalus, Aparallactus modestus, Anomochilus leonardi, Anilius scytale, Amphiesma stolatum, Ctenosaura pectinata, Zonosaurus ornatus, Xenosaurus grandis, Xantusia vigilis, Varanus salvator, Uta stansburiana, Urostrophus vantieri, Uroplatus lineatus, Uromastyx aegyptia, Uranoscodon superciliosus, Uma scoparia, Acontias plumbeus, Tupinambis teguixin, Trogonophis wiegmanni, Trachylepis quinquetaeniata, Tiliqua scincoides, Teratoscincus przewalskii, Teius teyou, Takydromus sexlineatus, Strophurus ciliaris, Sphenomorphus solomonis, Sphenodon punctatus, Stenocercus guentheri, Smaug mossambicus, Shinisaurus crocodilurus, Scincus scincus, Scincopus fasciatus, Sceloporus variabilis, Rieppeleon brevicaudatus, Rhineura floridana, Saltuarius cornutus, Rhacodactylus auriculatus, Ptychozoon kuhli, Pristidactylus torquatus, Polychrus marmoratus, Pogona vitticeps, Plica plica, Platysaurus capensis, Phymaturus palluma, Phrynosoma platyrhinos, Pholidobolus montium, Phelsuma lineata, Petrosaurus mearnsi, Oplurus cyclurus, Nucras tesselata, Nephrurus levis, Morunasaurus annularis, Monopeltis capensis, Lygodactylus picturatus, Liolaemus bellii, Lialis burtonis, Lepidophyma flavimaculatum, Leiosaurus catamarcensis, Leiolepis belliana, Leiocephalus barohonensis, Lanthanotus borneensis, Lacerta viridis, Holaspis guentheri, Hemidactylus mabuia, Hemidactylus frenatus, Heloderma horridum, Gymnophthalmus leucomystax, Gonatodes albogularis, Geocalamus acutus, Gekko gecko, Gehyra multilada, Gambelia wislizenii, Gallotia galloti, Feylinia polylepis, Eugongylus rufescens, Eublepharis macularius, Enyalioides laticeps, Draco quinquefasciatus, Elgaria multicarinata, Dipsosaurus dorsalis, Diplometopon zarudnyi, Dibamus novaeguineae, Delma borea, Crotaphytus collaris, Corytophanes cristatus, Cordylosaurus subtessellatus, Conolophus subcristatus, Colobosaura modesta, Coleonyx variegatus, Chirindia swynnertoni, Chamaesaura anguina, Chamaeleo calyptratus, Chalarodon madagascariensis, Celestus enneagrammus, Calotes emma, Callopistes maculatus, Brookesia brygooi, Brachylophus fasciatus, Blanus cinereus, Bipes biporus, Basiliscus_basiliscus, Bachia cophias, Atlantolacerta andreanskyi, Anolis carolinensis, Anniella pulchra, Anelytropsis papillosus, Amphisbaena fuliginosa, Amphiglossus splendidus, Amblyrhynchus cristatus, Alopoglossus copii, Agama agama, Ameiva ameiva, Aeluroscalabotes felina, Acontias percivali, Agkistrodon contortrix, Acrochordus granulatus, Afrotyphlops schlegelii, Afronatrix anoscopus, Hyporhina antiqua, Estesia mongoliensis, Cricosauria typica, Polyglyphanodon sternbergi, Slavoia darevskii, Spathorhynchus fossorium, Plotosaurus bennisonni, Gambelia corona

Factors intrinsic and extrinsic to organisms dictate the course of morphological evolution but are seldom considered together in comparative analyses. Among vertebrates, squamates (lizards and snakes) exhibit remarkable morphological and developmental variations that parallel their incredible ecological spectrum. However, this exceptional diversity also makes systematic quantification and analysis of their morphological evolution challenging. We present a squamate-wide, high-density morphometric analysis of the skull across 181 modern and extinct species to identify the primary drivers of their cranial evolution within a unified, quantitative framework. Diet and habitat preferences, but not reproductive mode, are major influences on skull shape evolution across squamates, with fossorial and aquatic taxa exhibiting convergent and rapid changes in skull shape. In lizards, diet is associated with the shape of the rostrum, reflecting its use in grasping prey, whereas snakes show a correlation between diet and the shape of posterior skull bones important for gape widening. Similarly, we observe the highest rates of evolution and greatest disparity in regions associated with jaw musculature in lizards, whereas those forming the jaw articulation evolve faster in snakes. In addition, high-resolution ancestral cranial reconstructions from these data support a terrestrial, nonfossorial origin for snakes. Despite their disparate evolutionary trends, lizards and snakes unexpectedly share a common pattern of trait integration, with the highest correlations in the occiput, jaw articulation, and palate. We thus demonstrate that highly diverse phenotypes, exemplified by lizards and snakes, can and do arise from differential selection acting on conserved patterns of phenotypic integration.


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