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Evolution of the Sauropterygian Labyrinth with Increasingly Pelagic Lifestyles

2017; Elsevier BV; Volume: 27; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2017.10.069

1879-0445

James M. Neenan, Tobias Reich, Serjoscha Evers, Patrick S. Druckenmiller, Dennis F. A. E. Voeten, Jonah N. Choiniere, Paul M. Barrett, Stephanie E. Pierce, Roger Benson,

Evolution and Paleontology Studies

Sauropterygia, a successful clade of marine reptiles abundant in aquatic ecosystems of the Mesozoic, inhabited nearshore to pelagic habitats over >180 million years of evolutionary history [1Motani R. The evolution of marine reptiles.Evol. Educ. Outreach. 2009; 2: 224-235Crossref Scopus (106) Google Scholar]. Aquatic vertebrates experience strong buoyancy forces that allow movement in a three-dimensional environment, resulting in structural convergences such as flippers and fish-like bauplans [2Motani R. Evolution of fish-shaped reptiles (Reptilia: Ichthyopterygia) in their physical environments and constraints.Annu. Rev. Earth Planet. Sci. 2005; 33: 395-420Crossref Scopus (121) Google Scholar, 3Kelley N.P. Pyenson N.D. Vertebrate evolution. Evolutionary innovation and ecology in marine tetrapods from the Triassic to the Anthropocene.Science. 2015; 348: aaa3716Crossref PubMed Scopus (91) Google Scholar], as well as convergences in the sensory systems. We used computed tomographic scans of 19 sauropterygian species to determine how the transition to pelagic lifestyles influenced the evolution of the endosseous labyrinth, which houses the vestibular sensory organ of balance and orientation [4Sipla J.S. Spoor F. The physics and physiology of balance.in: Thewissen J.G.M. Nummela S. Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates. University of California Press, 2008: 227-232Crossref Google Scholar]. Semicircular canal geometries underwent distinct changes during the transition from nearshore Triassic sauropterygians to the later, pelagic plesiosaurs. Triassic sauropterygians have dorsoventrally compact, anteroposteriorly elongate labyrinths, resembling those of crocodylians. In contrast, plesiosaurs have compact, bulbous labyrinths, sharing some features with those of sea turtles. Differences in relative labyrinth size among sauropterygians correspond to locomotory differences: bottom-walking [5Scheyer T.M. Neenan J.M. Renesto S. Saller F. Hagdorn H. Furrer H. Rieppel O. Tintori A. Revised paleoecology of placodonts – with a comment on ‘The shallow marine placodont Cyamodus of the central European Germanic Basin: its evolution, paleobiogeography and paleoecology’ by C.G. Diedrich (Historical Biology, iFirst article, 2011, 1–19).Hist. Biol. 2012; 24: 257-267Google Scholar, 6Klein N. Houssaye A. Neenan J.M. Scheyer T.M. Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia).Contrib. Zool. 2015; 84: 59-84Google Scholar] placodonts have proportionally larger labyrinths than actively swimming taxa (i.e., all other sauropterygians). Furthermore, independent evolutionary origins of short-necked, large-headed “pliosauromorph” body proportions among plesiosaurs coincide with reductions of labyrinth size, paralleling the evolutionary history of cetaceans [7Spoor F. Bajpai S. Hussain S.T. Kumar K. Thewissen J.G.M. Vestibular evidence for the evolution of aquatic behaviour in early cetaceans.Nature. 2002; 417: 163-166Crossref PubMed Scopus (171) Google Scholar]. Sauropterygian labyrinth evolution is therefore correlated closely with both locomotory style and body proportions, and these changes are consistent with isolated observations made previously in other marine tetrapods. Our study presents the first virtual reconstructions of plesiosaur endosseous labyrinths and the first large-scale, quantitative study detailing the effects of increasingly aquatic lifestyles on labyrinth morphology among marine reptiles.