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

www.pnas.org/cgi/doi/10.1073/pnas.1820967116

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