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Walk before you jump: new insights on early frog locomotion from the oldest known salientian

  • Andrés I. Lires (a1), Ignacio M. Soto (a1) and Raúl O. Gómez (a2)
Abstract

Understanding the evolution of a Bauplan starts with discriminating phylogenetic signal from adaptation and the latter from exaptation in the observed biodiversity. Whether traits have predated, accompanied, or followed evolution of particular functions is the basic inference to establish the type of explanations required to determine morphological evolution. To accomplish this, we focus in a particular group of vertebrates, the anurans. Frogs and toads have a unique Bauplan among vertebrates, with a set of postcranial features that have been considered adaptations to jumping locomotion since their evolutionary origin. This interpretation is frequently stated but rarely tested in scientific literature. We test this assumption reconstructing the locomotor capabilities of the earliest known salientian, Triadobatrachus massinoti. This extinct taxon exhibits a mosaic of features that have traditionally been considered as representing an intermediate stage in the evolution of the anuran Bauplan, some of which were also linked to jumping skills. We considered T. massinoti in an explicit evolutionary framework by means of multivariate analyses and comparative phylogenetic methods. We used length measurements of major limb bones of 188 extant limbed amphibians (frogs and salamanders) and lizards as a morphological proxy of observed locomotor behavior. Our findings show that limb data correlate with locomotion, regardless of phylogenetic relatedness, and indicate that salamander-like lateral undulatory movements were the main mode of locomotion of T. massinoti. These results contrast with recent hypotheses and indicate that derived postcranial features that T. massinoti shared with anurans might have been later co-opted as exaptations in jumping frogs.

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AmphibiaWeb. 2015. Information on amphibian biology and conservation. http://amphibiaweb.org, accessed 23 September 2015.
Ashley-Ross, M. A., Lundin, R., and Johnson, K. L.. 2009. Kinematics of level terrestrial and underwater walking in the California newt, Taricha torosa . Journal of Experimental Zoology 311:240257.
Báez, A. M., and Basso, N. G.. 1996. The earliest known frogs of the Jurassic of South America: review and cladistic appraisal of their relationships. Münchner Geowissenschaftliche Abhandlungen 30:131158.
Barr, W. A., and Scott, R. S.. 2014. Phylogenetic comparative methods complement discriminant function analysis in ecomorphology. American Journal of Physical Anthropology 153:663674.
Davis, E. B., and McHorse, B. K.. 2013. A method for improved identification of postcrania from mammalian fossil assemblages: multivariate discriminant function analysis of camelid astragali. Palaeontologia Electronica 16:27A. http://palaeo-electronica.org/content/2013/539-discriminant-id-of-postcrania.
Dong, L., Roček, Z., Wang, Y., and Jones, M. E. H.. 2013. Anurans from the Lower Cretaceous Jehol Group of western Liaoning, China. PLoS ONE 8:e69723.
Duellman, W. E. 1992. Reproductive strategies of frogs. Scientific American 267(1), 8087.
Emerson, S. B. 1976. Burrowing in frogs. Journal of Morphology 149:437458.
Emerson, S. B. 1978. Allometry and jumping in frogs: helping the twain to meet. Evolution 32:551564.
Emerson, S. B. 1979. The ilio-sacral articulation in frogs: form and function. Biological Journal of the Linnean Society 11:153168.
Emerson, S. B. 1988. Convergence and morphological constraint in frogs: variation in postcranial morphology. Fieldiana Zoology 43:119.
Emerson, S. B., and De Jongh, H. J.. 1980. Muscle activity at the ilio-sacral articulation of frogs. Journal of Morphology 166:129144.
Emerson, S. B., Travis, J., and Koehl, M. A.. 1990. Functional complexes and additivity in performance: a test case with “flying” frogs. Evolution 44:21532157.
Enriquez-Urzelai, U., Montori, A., Llorente, G. A., and Kaliontzopoulou, A.. 2015. Locomotor mode and the evolution of the hindlimb in western Mediterranean anurans. Evolutionary Biology 42:199209.
Essner, R. Jr., Suffian, D. J., Bishop, P. J., and Reilly, S. M.. 2010. Landing in basal frogs: evidence of saltational patterns in the evolution of anuran locomotion. Naturwissenschaften 97:935939.
Estes, R., and Reig, O. A.. 1973. The early fossil record of frogs: a review of the evidence. Pp. 1163 in J. L. Vial, ed. Evolutionary biology of the anurans: contemporary research on major problems. University of Missouri Press, Columbia.
Evans, S. E., and Borsuk-Białynicka, M.. 1998. A stem-group frog from the Early Triassic of Poland. Acta Palaeontologica Polonica 43:573580.
Fabrezi, M., Manzano, A. S., Abdala, V., and Lobo, F.. 2014. Anuran locomotion: ontogeny and morphological variation of a distinctive set of muscles. Evolutionary Biology 41:308326.
Frost, D. R. 2015. Amphibian species of the world: an online reference. Version 6.0. http://research.amnh.org/vz/herpetology/amphibia/index.html, accessed 8 June 2015.
Gans, C., and Parsons, T. S.. 1966. On the origin of the jumping mechanisms in frogs. Evolution 20:9299.
Gao, K. Q., and Chen, Q.. 2004. A new frog (Amphibia: Anura) from the Lower Cretaceous of western Liaoning, China. Cretaceous Research 25:761769.
Gao, K. Q., and Wang, Y.. 2001. Mesozoic anurans from Liaoning Province, China, and phylogenetic relationships of archaeobatrachian anuran clades. Journal of Vertebrate Paleontology 21:460476.
Gardner, J. D., Roček, Z., Přikryl, T., Eaton, J. G., Blob, R. W., and Sankey, J. T.. 2010. Comparative morphology of the ilium of anurans and urodeles (Lissamphibia) and a re-assessment of the anuran affinities of Nezpercius dodsoni (Blob et al. 2001). Journal of Vertebrate Paleontology 30:16841696.
Gomes, F. R., Rezende, E L., Grizante, M. B., and Navas, C. A.. 2009. The evolution of jumping performance in anurans: morphological correlates and ecological implications. Journal of Evolutionary Biology 22:10881097.
Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society Series B 326:119157.
Grey, L. A., O’Reilly, J. C., and Nishikawa, K. C.. 1997. Evolution of forelimb movement patterns for prey manipulation in anurans. Journal of Experimental Zoology 277:417424.
Griffiths, I. 1956. Status of Protobatrachus massinoti . Nature 177:342343.
Griffiths, I. 1963. The phylogeny of the Salientia. Biological Reviews 38:241292.
Handrigan, G. R., and Wassersug, R. J.. 2007. The anuran Bauplan: a review of the adaptive, developmental, and genetic underpinnings of frog and tadpole morphology. Biological Reviews 82:125.
Hecht, M. K. 1962. A reevaluation of the early history of the frogs: Part I. Systematic Biology 11:3944.
Jenkins, F. A., and Shubin, N. H.. 1998. Prosalirus bitis and the anuran caudopelvic mechanism. Journal of Vertebrate Paleontology 18:495510.
Jorgensen, M. E., and Reilly, S. M.. 2013. Phylogenetic patterns of skeletal morphometrics and pelvic traits in relation to locomotor mode in frogs. Journal of Evolutionary Biology 26:929943.
Jungers, W. L., Falsetti, A. B., and Wall, C. E.. 1995. Shape, relative size, and size-adjustments in morphometrics. Yearbook of Physical Anthropology 38:137161.
Karakasiliotis, K., Schilling, N., Cabelguen, J. M., and Ijspeert, A. J.. 2013. Where are we in understanding salamander locomotion: biological and robotic perspectives on kinematics. Biological Cybernetics 107:529544.
Lachenbruch, P. A., and Mickey, M. R.. 1968. Estimation of error rates in discriminant analysis. Technometrics 10:111.
Maddison, W. P., and Maddison, D. R.. 2011. Mesquite: a modular system for evolutionary analysis, Version 2.75. http://mesquiteproject.org.
Maglia, A. M., Pugener, L. A., and Mueller, J. M.. 2007. Skeletal morphology and postmetamorphic ontogeny of Acris crepitans (Anura: Hylidae): a case of miniaturization in frogs. Journal of Morphology 268:194223.
Marjanović, D., and Witzmann, F.. 2015. An extremely peramorphic newt (Urodela: Salamandridae: Pleurodelini) from the Latest Oligocene of Germany, and a new phylogenetic analysis of extant and extinct salamandrids. PLoS ONE 10:e0137068.
Martins, E. P., and Hansen, T. F.. 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist 149:646667.
Mosimann, J. E., and James, F. C.. 1979. New statistical methods for allometry with application to Florida red-winged blackbirds. Evolution 33:444459.
Nauwelaerts, S., and Aerts, P.. 2002. Two distinct gait types in swimming frogs. Journal of Zoology 258:183188.
Nauwelaerts, S., and Aerts, P.. 2006. Take-off and landing forces in jumping frogs. Journal of Experimental Biology 209:6677.
O’Reilly, J. C., Summers, A. P., and Ritter, D. A.. 2000. The evolution of the functional role of trunk muscles during locomotion in adult amphibians. American Zoologist 40:123135.
Piveteau, J. 1936. Une forme ancestrale des Amphibiens Anoures dans le Trias inférieur de Madagascar. Comptes Rendus de l’Académie des Sciences 102:16071608.
Piveteau, J. 1937. Paléontologie de Madagascar. Un amphibien du Trias inférieur: essai sur l’origine et l’évolution des amphibiens anoures. Annales de Paléontologie. 26:135177.
Přikryl, T., Aerts, P., Havelková, P., Herrel, A., and Roček, Z.. 2009. Pelvic and thigh musculature in frogs (Anura) and origin of anuran jumping locomotion. Journal of Anatomy 214:100139.
Pugener, L. A., and Maglia, A. M.. 2009. Skeletal morphogenesis of the vertebral column of the miniature hylid frog Acris crepitans, with comments on anomalies. Journal of Morphology 270:5269.
Pyron, R. A., and Wiens, J. J.. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61:543583.
Pyron, R. A., Burbrink, F. T., and Wiens, J. J.. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13:93.
R Development Core Team. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org.
Rage, J. C., and Roček, Z.. 1986. Triadobatrachus revisited. Pp. 255258 in Z. Roček, ed. Studies in herpetology. Charles University Press, Prague.
Rage, J. C., and Roček, Z.. 1989. Redescription of Triadobatrachus massinoti (Piveteau, 1936) an anuran amphibian from the early Triassic. Palaeontographica A 206:116.
Reilly, S. M., and Jorgensen, M. E.. 2011. The evolution of jumping in frogs: morphological evidence for the basal anuran locomotor condition and the radiation of locomotor systems in crown group anurans. Journal of Morphology 272:149168.
Roček, Z. 2000. Mesozoic anurans. Pp. 12951331. in H. Heatwole, and R. L. Carroll, eds. Amphibian biology. Surrey Beatty, Chipping Norton, Australia.
Roček, Z., and Rage, J. C.. 2000. Proanuran stages (Triadobatrachus, Czatkobatrachus). Pp. 12831294. in H. Heatwole, and R. L. Carroll, eds. Amphibian biology. Surrey Beatty, Chipping Norton, Australia.
Ročková, H., and Roček, Z.. 2005. Development of the pelvis and posterior part of the vertebral column in the Anura. Journal of Anatomy 206:1735.
Rohlf, F. J. 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:21432160.
Rohlf, F. J. 2004. NTSYSpc: numerical taxonomy and multivariate analysis system, Version 2.11. Exeter, Setauket, N.Y.
Shubin, N. H., and Jenkins, F. A. Jr. 1995. An Early Jurassic jumping frog. Nature 377:4952.
Sigurdsen, T., Green, D. M., and Bishop, P. J.. 2012. Did Triadobatrachus Jump? Morphology and evolution of the anuran forelimb in relation to locomotion in early salientians. Fieldiana Life and Earth Sciences 5:7789.
StatSoft. 2007. STATISTICA (data analysis software system), Version 8.0. httm://www.statsoft.com.
Symonds, M. R., and Blomberg, S. P.. 2014. A primer on phylogenetic generalised least squares. Pp. 105130 in L. Z. Garamszegi, ed. Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin.
Taigen, T. L., Emerson, S. B., and Pough, F. H.. 1982. Ecological correlates of anuran exercise physiology. Oecologia 52:4956.
Toledo, N., Bargo, M. S., Cassini, G. H., and Vizcaíno, S. F.. 2012. The forelimb of early Miocene sloths (Mammalia, Xenarthra, Folivora): morphometrics and functional implications for substrate preferences. Journal of Mammalian Evolution 19:185198.
Venables, W. N., and Ripley, B. D.. 2002. Modern applied statistics with S, 4th ed. Springer, New York.
Weisbecker, V., and Mitgutsch, C.. 2010. A large-scale survey of heterochrony in anuran cranial ossification patterns. Journal of Zoological Systematics and Evolutionary Research 48:332347.
Wells, K. D. 2007. The ecology and behavior of amphibians, 1st ed. University of Chicago Press, Chicago.
Zug, R. G. 1972. Anuran locomotion: structure and function. I. Preliminary observations on relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia 4:613624.
Zug, R. G. 1978. Anuran locomotion-structure and function II: Jumping performance of semiaquatic, terrestrial, and arboreal frogs. Smithsonian Contributions to Zoology 276:132.
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