Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T18:33:45.708Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  21 March 2016

Andrés I. Lires ,
Ignacio M. Soto  and
Raúl O. Gómez
Andrés I. Lires
Affiliation:
IEGEBA (CONICET/UBA)–Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Buenos Aires C1428EGA, Argentina. E-mail: [email protected], [email protected]
Ignacio M. Soto
Affiliation:
IEGEBA (CONICET/UBA)–Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Buenos Aires C1428EGA, Argentina. E-mail: [email protected], [email protected]
Raúl O. Gómez
Affiliation:
CONICET–Laboratorio de Paleontología Evolutiva de Vertebrados, Departamento de Ciencias Geológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Buenos Aires C1428EGA, Argentina. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Type
Articles
Information
Paleobiology , Volume 42 , Issue 4 , November 2016 , pp. 612 - 623
Copyright
Copyright © 2016 The Paleontological Society. All rights reserved 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

AmphibiaWeb. 2015. Information on amphibian biology and conservation. http://amphibiaweb.org, accessed 23 September 2015.Google Scholar
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 311:240–257.Google Scholar
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 30:131–158.Google Scholar
Barr, W. A., and Scott, R. S.. 2014. Phylogenetic comparative methods complement discriminant function analysis in ecomorphology. American Journal of Physical Anthropology 153:663–674.Google Scholar
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.Google Scholar
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.Google Scholar
Duellman, W. E. 1992. Reproductive strategies of frogs. Scientific American 267(1), 80–87.Google Scholar
Emerson, S. B. 1976. Burrowing in frogs. Journal of Morphology 149:437–458.Google Scholar
Emerson, S. B. 1978. Allometry and jumping in frogs: helping the twain to meet. Evolution 32:551–564.Google Scholar
Emerson, S. B. 1979. The ilio-sacral articulation in frogs: form and function. Biological Journal of the Linnean Society 11:153–168.CrossRefGoogle Scholar
Emerson, S. B. 1988. Convergence and morphological constraint in frogs: variation in postcranial morphology. Fieldiana Zoology 43:1–19.Google Scholar
Emerson, S. B., and De Jongh, H. J.. 1980. Muscle activity at the ilio-sacral articulation of frogs. Journal of Morphology 166:129–144.CrossRefGoogle ScholarPubMed
Emerson, S. B., Travis, J., and Koehl, M. A.. 1990. Functional complexes and additivity in performance: a test case with “flying” frogs. Evolution 44:2153–2157.Google Scholar
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 42:199–209.Google Scholar
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 97:935–939.Google Scholar
Estes, R., and Reig, O. A.. 1973. The early fossil record of frogs: a review of the evidence. Pp. 11–63 in J. L. Vial, ed. Evolutionary biology of the anurans: contemporary research on major problems. University of Missouri Press, Columbia.Google Scholar
Evans, S. E., and Borsuk-Białynicka, M.. 1998. A stem-group frog from the Early Triassic of Poland. Acta Palaeontologica Polonica 43:573–580.Google Scholar
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 41:308–326.Google Scholar
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.Google Scholar
Gans, C., and Parsons, T. S.. 1966. On the origin of the jumping mechanisms in frogs. Evolution 20:92–99.Google Scholar
Gao, K. Q., and Chen, Q.. 2004. A new frog (Amphibia: Anura) from the Lower Cretaceous of western Liaoning, China. Cretaceous Research 25:761–769.Google Scholar
Gao, K. Q., and Wang, Y.. 2001. Mesozoic anurans from Liaoning Province, China, and phylogenetic relationships of archaeobatrachian anuran clades. Journal of Vertebrate Paleontology 21:460–476.Google Scholar
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 30:1684–1696.Google Scholar
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 22:1088–1097.Google Scholar
Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society Series B 326:119–157.Google Scholar
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 277:417–424.Google Scholar
Griffiths, I. 1956. Status of Protobatrachus massinoti . Nature 177:342–343.Google Scholar
Griffiths, I. 1963. The phylogeny of the Salientia. Biological Reviews 38:241–292.Google Scholar
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 82:1–25.Google Scholar
Hecht, M. K. 1962. A reevaluation of the early history of the frogs: Part I. Systematic Biology 11:39–44.Google Scholar
Jenkins, F. A., and Shubin, N. H.. 1998. Prosalirus bitis and the anuran caudopelvic mechanism. Journal of Vertebrate Paleontology 18:495–510.Google Scholar
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 26:929–943.Google Scholar
Jungers, W. L., Falsetti, A. B., and Wall, C. E.. 1995. Shape, relative size, and size-adjustments in morphometrics. Yearbook of Physical Anthropology 38:137–161.CrossRefGoogle Scholar
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 107:529–544.Google Scholar
Lachenbruch, P. A., and Mickey, M. R.. 1968. Estimation of error rates in discriminant analysis. Technometrics 10:1–11.Google Scholar
Maddison, W. P., and Maddison, D. R.. 2011. Mesquite: a modular system for evolutionary analysis, Version 2.75. http://mesquiteproject.org.Google Scholar
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 268:194–223.Google Scholar
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.Google Scholar
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 149:646–667.Google Scholar
Mosimann, J. E., and James, F. C.. 1979. New statistical methods for allometry with application to Florida red-winged blackbirds. Evolution 33:444–459.Google Scholar
Nauwelaerts, S., and Aerts, P.. 2002. Two distinct gait types in swimming frogs. Journal of Zoology 258:183–188.Google Scholar
Nauwelaerts, S., and Aerts, P.. 2006. Take-off and landing forces in jumping frogs. Journal of Experimental Biology 209:66–77.Google Scholar
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 40:123–135.Google Scholar
Piveteau, J. 1936. Une forme ancestrale des Amphibiens Anoures dans le Trias inférieur de Madagascar. Comptes Rendus de l’Académie des Sciences 102:1607–1608.Google Scholar
Piveteau, J. 1937. Paléontologie de Madagascar. Un amphibien du Trias inférieur: essai sur l’origine et l’évolution des amphibiens anoures. Annales de Paléontologie. 26:135–177.Google Scholar
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 214:100–139.Google Scholar
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 270:52–69.Google Scholar
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 61:543–583.Google Scholar
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.Google Scholar
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.Google Scholar
Rage, J. C., and Roček, Z.. 1986. Triadobatrachus revisited. Pp. 255–258 in Z. Roček, ed. Studies in herpetology. Charles University Press, Prague.Google Scholar
Rage, J. C., and Roček, Z.. 1989. Redescription of Triadobatrachus massinoti (Piveteau, 1936) an anuran amphibian from the early Triassic. Palaeontographica A 206:1–16.Google Scholar
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 272:149–168.Google Scholar
Roček, Z. 2000. Mesozoic anurans. Pp. 1295–1331. in H. Heatwole, and R. L. Carroll, eds. Amphibian biology. Surrey Beatty, Chipping Norton, Australia.Google Scholar
Roček, Z., and Rage, J. C.. 2000. Proanuran stages (Triadobatrachus, Czatkobatrachus). Pp. 1283–1294. in H. Heatwole, and R. L. Carroll, eds. Amphibian biology. Surrey Beatty, Chipping Norton, Australia.Google Scholar
Ročková, H., and Roček, Z.. 2005. Development of the pelvis and posterior part of the vertebral column in the Anura. Journal of Anatomy 206:17–35.Google Scholar
Rohlf, F. J. 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143–2160.Google Scholar
Rohlf, F. J. 2004. NTSYSpc: numerical taxonomy and multivariate analysis system, Version 2.11. Exeter, Setauket, N.Y.Google Scholar
Shubin, N. H., and Jenkins, F. A. Jr. 1995. An Early Jurassic jumping frog. Nature 377:49–52.Google Scholar
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 5:77–89.Google Scholar
StatSoft. 2007. STATISTICA (data analysis software system), Version 8.0. httm://www.statsoft.com.Google Scholar
Symonds, M. R., and Blomberg, S. P.. 2014. A primer on phylogenetic generalised least squares. Pp. 105–130 in L. Z. Garamszegi, ed. Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin.Google Scholar
Taigen, T. L., Emerson, S. B., and Pough, F. H.. 1982. Ecological correlates of anuran exercise physiology. Oecologia 52:49–56.Google Scholar
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 19:185–198.Google Scholar
Venables, W. N., and Ripley, B. D.. 2002. Modern applied statistics with S, 4th ed. Springer, New York.Google Scholar
Weisbecker, V., and Mitgutsch, C.. 2010. A large-scale survey of heterochrony in anuran cranial ossification patterns. Journal of Zoological Systematics and Evolutionary Research 48:332–347.Google Scholar
Wells, K. D. 2007. The ecology and behavior of amphibians, 1st ed. University of Chicago Press, Chicago.Google Scholar
Zug, R. G. 1972. Anuran locomotion: structure and function. I. Preliminary observations on relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia 4:613–624.Google Scholar
Zug, R. G. 1978. Anuran locomotion-structure and function II: Jumping performance of semiaquatic, terrestrial, and arboreal frogs. Smithsonian Contributions to Zoology 276:1–32.Google Scholar