Skip to main content
×
×
Home

Miniaturization and morphological evolution in Paleozoic relatives of living amphibians: a quantitative approach

  • Celeste M. Pérez-Ben (a1), Rainer R. Schoch (a2) and Ana M. Báez (a3)
Abstract

Miniaturization has been defined as the evolution of extremely small adult size in a lineage. It does not simply imply the decrease of the body size but also involves structural modifications to maintain functional efficiency at a strongly reduced size. Miniaturization has been proposed as a key factor in the origin of several major tetrapod clades. Current hypotheses propose that the living amphibians (lissamphibians) originated within a clade of Paleozoic dwarfed dissorophoid temnospondyls. Morphological traits shared by these small dissorophoids have been interpreted as resulting from constraints imposed by the extreme size reduction, but these statements were based only on qualitative observations. Herein, we assess quantitatively morphological changes in the skull previously associated with miniaturization in the lissamphibian stem lineage by comparing evolutionary and ontogenetic allometries in dissorophoids. Our results show that these features are not comparable to the morphological consequences of extreme size reduction as documented in extant miniature amphibians, but instead they resemble immature conditions of larger temnospondyls. We conclude that the truncation of the ancestral ontogeny, and not constraints related to miniaturization, might have been the factor that played a major role in the morphological evolution of small dissorophoids. Based on our results, we discuss the putative role of miniaturization in the origin of lissamphibians within Dissorophoidea.

Copyright
References
Hide All
Anderson, J. S. 2007. Incorporating ontogeny into the matrix: a phylogenetic evaluation of developmental evidence for the origin of modern amphibians. Pp. 182227 in J. S. Anderson, and H.-D. Sues, eds. Major transitions in vertebrate evolution. Indiana University Press, Bloomington.
Anderson, J. S., Reisz, R. R., Scott, D., Fröbisch, N. B., and Sumida, S. S.. 2008. A stem batrachian from the Early Permian of Texas and the origin of frogs and salamanders. Nature 453:515518.
Angielczyk, K. D., and Ruta, M.. 2012. The roots of amphibian morphospace: a geometric morphometric analysis of Paleozoic Temnospondyls. Fieldiana Life and Earth Sciences 5:4058.
Ascarrunz, E., Rage, J.-C., Legreneur, P., and Laurin, M.. 2016. Triadobatrachus massinoti, the earliest known lissamphibian (Vertebrata: Tetrapoda) re-examined by μCT scan, and the evolution of trunk length in batrachians. Contributions to Zoology 85:201234.
Atchley, W. R., and Hall, B. K.. 1991. A model for development and evolution of complex morphological structures. Biological Reviews 66:101157.
Bauchot, R. 1978. Encephalization in vertebrates. Brain, Behavior, and Evolution 15:118.
Blomberg, S. P., Lefevre, J. G., Wells, J. A., and Waterhouse, M.. 2012. Independent contrasts and PGLS regression estimators are equivalent. Systematic Biology 61:382391.
Bolt, J. R. 1969. Lissamphibian origins: possible protolissamphibian from the Lower Permian of Oklahoma. Science 166:888891.
Bolt, J. R. 1979. Amphibamus grandiceps as a juvenile dissorophoid: evidence and implications. Pp. 529563 in M. H. Nitecki, ed. Mazon Creek fossils. Academic, New York.
Bolt, J. R. 1991. Lissamphibian origins. Pp. 194221 in H.-P. Schultze, and L. Trueb, eds. Origins of the higher groups of tetrapods: Controversy and consensus. Comstock Publishing, Ithaca, N.Y.
Bourget, H., and Anderson, J. S.. 2011. A new Amphibamid (Temnospondyli: Dissorophoidea) from the Early Permian of Texas. Journal of Vertebrate Paleontology 31:3249.
Bolt, J. R., and Lombard, R. E.. 1985. Evolution of the tympanic ear and the origin of frogs. Biological Journal of the Linnean Society 24:8399.
Boy, J. A. 1972. Die Branchiosaurier (Amphibia) des saarpfälzischen Rotliegenden (Unter–Perm, SW–Deutschland). Abhandlungen des hessisches Landes-Amtes für Bodenforschung 65:1137.
Boy, J. A. 1974. Die Larven der rhachitomen Amphibien (Amphibia: Temnospondyli; Karbon–Trias). Paläontologische Zeitschrift 48:236268.
Boy, J. A. 1986. Studien über die Branchiosauridae (Amphibia: Temnospondyli) 1. Neue und wenig bekannte Arten aus dem mitteleuropäischen Rotliegenden (?oberstes Karbon bis unteres Perm). Paläontologische Zeitschrift 60:131166.
Boy, J. A. 1987. Studien über die Branchiosauridae (Amphibia: Temnospondyli; Ober-Karbon-Unter-Perm) 2. Systematische Übersicht. Neues Jahrbuch für Geologie und Paläeontologie Abhandlungen 174:75104.
Boy, J. A. 1995. Über die Micromelerpetontidae (Amphibia: Temnospondyli). 2. Micromelerpeton ulmetense n. sp. und Micromelerpeton (?) boyi Heyler. Neues Jahrbuch für Geologie und Paläeontologie Abhandlungen 223:241274.
Boy, J. A., and Sues, H.-D.. 2000. Branchiosaurs: larvae, metamorphosis and heterochrony in temnospondyls and seymouriamorphs. Pp. 11501197 in H. Heatwole, and R. L. Carroll, eds. Amphibian biology, Vol. 4. Palaeontology. Surrey Beatty, Chipping Norton, NSW, Australia.
Carroll, R. L. 1964. Early evolution of the dissorophid amphibians. Bulletin of the Museum of Comparative Zoology 131:163250.
Carroll, R. L. 1970. Quantitative aspects of the amphibian-reptilian transition. Forma et functio 3:165178.
Carroll, R. L. 1990. A tiny microsaur from the Lower Permian of Texas: size constraints in Palaeozoic tetrapods. Palaeontology 33:893909.
Carroll, R. L. 2001. The origin and early radiation of terrestrial vertebrates. Journal of Paleontology 75:12021213.
Carroll, R. L. 2009. The rise of amphibians: 365 million years of evolution. Johns Hopkins University Press, Baltimore, Md.
Carroll, R. L., and Holmes, R.. 1980. The skull and jaw musculature as guides to the ancestry of salamanders. Zoological Journal of the Linnean Society 68:140.
Clack, J. A., and Milner, A. R.. 2010. Morphology and systematics of the Pennsylvanian amphibian Platyrhinops lyelli (Amphibia: Temnospondyli). Earth and Environmental Science Transactions of the Royal Society of Edinburgh 100:275295.
Daly, E. 1994. The Amphibamidae (Amphibia: Temnospondyli), with a description of a new genus from the Upper Pennsylvanian of Kansas. University of Kansas Museum of Natural History, Miscellaneous Publications 85:159.
Dilkes, D. W. 1990. A new trematopsid amphibian (Temnospondyli: Dissorophoidea) from the Lower Permian of Texas. Journal of Vertebrate Paleontology 10:222243.
Dilkes, D. W., and Reisz, R. R.. 1987. Trematops milleri Williston, 1909 identified as a junior synonym of Acheloma cumminsi Cope, 1882, with a revision of the genus. American Museum Novitates 2902:112.
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:115.
Fröbisch, N. B., and Reisz, R. R.. 2008. A new Lower Permian amphibamid (Dissorophoidea, Temnospondyli) from the fissure fill deposits near Richards Spur, Oklahoma. Journal of Vertebrate Paleontology 28:10151030.
Fröbisch, N. B., and Reisz, R. R.. 2012. A new species of dissorophid (Cacops woehri) from the Lower Permian Dolese quarry, near Richards Spur, Oklahoma. Journal of Vertebrate Paleontology 32:3544.
Fröbisch, N. B., and Schoch, R. R.. 2009. Testing the impact of miniaturization on phylogeny: Paleozoic dissorophoid amphibians. Systematic Biology 58:312327.
Garland, T. Jr., Bennett, A. F., and Rezende, E. L.. 2005. Phylogenetic approaches in comparative physiology. Journal of Experimental Biology 208:30153035.
Garland, T. Jr., Harvey, P. H., and Ives, A. R.. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:1832.
Hanken, J. 1983. Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia, Plethodontidae). II. The fate of the brain and sense organs and their role in skull morphogenesis and evolution. Journal of Morphology 177:255268.
Hanken, J. 1984. Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia: Plethodontidae). I. Osteological variation. Biological Journal of the Linnean Society 23:5575.
Hanken, J. 1985. Morphological novelty in the limb skeleton accompanies miniaturization in salamanders. Science 229:871874.
Hanken, J. 1993. Adaptation of bone growth to miniaturization of body size. Pp. 79104 in B. K. Hall, ed. Bone. CRC Press, Boca Raton, Fl.
Hanken, J., and Wake, D. B.. 1993. Miniaturization of body size: organismal consequences and evolutionary significance. Annual Review of Ecology and Systematics 24:501519.
Huxley, J. S. 1932. Problems of Relative Growth. John Hopkins University Press, Baltimore, Md.
Jenkins, F. A. Jr., Walsh, D. M., and Carroll, R. L.. 2007. Anatomy of Eocaecilia micropodia, a limbed caecilian of the Early Jurassic. Bulletin of the Museum of Comparative Zoology 158:285365.
Kimmel, C. B., Sidlauskas, B., and Clack, J. A.. 2009. Linked morphological changes during palate evolution in early tetrapods. Journal of Anatomy 215:91109.
Kowalewski, M., and Novack-Gottshall, P. M.. 2010. Resampling methods in paleontology. Quantitative Methods in Paleobiology. Short Courses in Paleontology 16:1954.
Laurin, M., and Reisz, R. R.. 1997. A new perspective on tetrapod phylogeny. Pp. 959 in S. S. Sumida, and K. L. Martin, eds. Amniote origins. Academic, New York.
Lee, M. S. Y., Cau, A., Naish, D., and Dyke, G. J.. 2014. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345:562566.
Lombard, R. E., and Wake, D. B.. 1977. Tongue evolution in the lungless salamanders, family Plethodontidae. II. Function and evolutionary diversity. Journal of Morphology 153:3980.
Maddin, H. C., and Anderson, J. S.. 2012. Evolution of the amphibian ear with implications for lissamphibian phylogeny: insight gained from the caecilian inner ear. Fieldiana Life and Earth Sciences 5:5976.
Maddin, H. C., Reisz, R. R., and Anderson, J. S.. 2010. Evolutionary development of the neurocranium in Dissorophoidea (Tetrapoda: Temnospondyli), an integrative approach. Evolution and Development 12:393403.
Maddin, H. C., Jenkins, F. A. Jr., and Anderson, J. S.. 2012. The braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the origin of caecilians. PLoS ONE 7:e50743.
Marjanovic, D., and Laurin, M.. 2013. The origin(s) of extant amphibians: a review with emphasis on the “lepospondyl hypothesis.” Geodiversitas 35:207272.
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.
Milner, A. R. 1982. Small temnospondyl amphibians from the middle Pennsylvanian of Illinois. Palaeontology 25:635664.
Milner, A. R. 1988. The relationships and origin of living amphibians. Pp. 59102 in M. J. Benton, ed. The phylogeny and classification of the tetrapods. Clarendon, Oxford, U.K.
Milner, A. R. 1993. The Paleozoic relatives of lissamphibians. Herpetological Monographs 7:827.
Organ, C., Struble, M., Canoville, A., de Buffrénil, V., and Laurin, M.. 2016. Macroevolution of genome size in sarcopterygiaens during the water–land transition. Comptes Rendus Palevol 15:6573.
Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., and Pearse, W.. 2013. caper: comparative analyses of phylogenetics and evolution in R. R package, Version 0.5.2. http://CRAN.R–project.org/package=caper
Paradis, E., Claude, J., and Strimmer, K.. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289290.
Polley, B., and Reisz, R. R.. 2011. A new Lower Permian trematopid (Temnospondyli: Dissorophoidea) from Richards Spur, Oklahoma. Zoological Journal of the Linnean Society 161:789815.
Reisz, R. R., Schoch, R. R., and Anderson, J. S.. 2009. The armored dissorophid Cacops from the Early Permian of Oklahoma and the exploitation of the terrestrial realm by amphibians. Naturwissenschaften 96:789796.
Rieppel, O. 1996. Miniaturization in tetrapods: consequences for skull morphology. Pp. 4761 in P. J. Miller, ed. Miniature vertebrates: the implications of small body size. Clarendon, Oxford, U.K.
Roček, Z., and Rage, J. C.. 2000. Anatomical transformations in the transitions from temnospondyl to proanuran stages. Pp. 12741282 in H. Heatwole, and R. L. Carroll, eds. Amphibian biology, Vol. 4. Palaeontology. Surrey Beatty, Chipping Norton, NSW, Australia.
Ruta, M., Coates, M. I., and Quicke, D. L. J.. 2003. Early tetrapod relationships revisited. Biological Reviews 78:251345.
Rohlf, F. J. 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:21432160.
Sanchez, S., De Ricqlès, A., Schoch, R. R., and Steyer, J. S.. 2010. Developmental plasticity of limb bone microstructural organization in Apateon: histological evidence of paedomorphic conditions in branchiosaurs. Evolution and Development 12:315328.
Schoch, R. R. 1992. Comparative ontogeny of early Permian branchiosaurid amphibians. Developmental stages. Palaeontographica Abteilung A 222:4383.
Schoch, R. R. 1995. Heterochrony in the development of the amphibian head. Pp. 107124 in K. J. McNamara, ed. Evolutionary change and heterochrony. Wiley, Chichester, U.K.
Schoch, R. R. 2002. The early formation of the skull in extant and Paleozoic amphibians. Paleobiology 28:278296.
Schoch, R. R. 2009. Evolution of life cycles in early amphibians. Annual Review of Earth and Planetary Sciences 37:135162.
Schoch, R. R. 2012a. Character distribution and phylogeny of the dissorophid temnospondyls. Fossil Record 15:119135.
Schoch, R. R. 2012b. How body size and development biased the direction of evolution in early amphibians. Historical Biology 25:155165.
Schoch, R. R. 2014a. Amphibian skull evolution: the developmental and functional context of simplification, bone loss and heterotopy. Journal of Experimental Zoology B 322:619630.
Schoch, R. R. 2014b. Life cycles, plasticity and palaeoecology in temnospondyl amphibians. Palaeontology 57:517529.
Schoch, R. R., and Fröbisch, N. B.. 2006. Metamorphosis and neoteny: alternative pathways in an extinct amphibian clade. Evolution 60:14671475.
Schoch, R. R., and Milner, A. R.. 2004. Structure and implications of theories on the origins of lissamphibians. Pp. 345377 in G. Arratia, and M. V. H. Wilson, eds. Recent advances in the origin and early radiation of vertebrates. Dr. Friederich Pfeil, Munich, Germany.
Schoch, R. R., and Milner, A. R.. 2008. The intrarelationships and evolutionary history of the temnospondyl family Branchiosauridae. Journal of Systematic Palaeontology 6:409431.
Schoch, R. R., and Milner, A. R.. 2014. Handbook of paleoherpetology—Temnospondyli I. Dr. Friedrich Pfeil, Munich, Germany.
Schoch, R. R., and Rubidge, B. S.. 2005. The amphibamid Micropholis from the Lystrosaurus Assemblage Zone of South Africa. Journal of Vertebrate Paleontology 25:502522.
Schoch, R. R., and Sues, H.-D.. 2013. A new dissorophid temnospondyl from the Lower Permian of north-central Texas. Comptes Rendus Palevol 12:437445.
Sessions, S. K. 2008. Evolutionary cytogenetics in salamanders. Chromosome Research 16:183201.
Sigurdsen, T., and Bolt, J. R.. 2010. The Lower Permian amphibamid Doleserpeton (Temnospondyli: Dissorophoidea), the interrelationships of amphibamids, and the origin of modern amphibians. Journal of Vertebrate Paleontology 30:13601377.
Skutschas, P., and Martin, T.. 2011. Cranial anatomy of the stem salamander Kokartus honorarius (Amphibia: Caudata) from the Middle Jurassic of Kyrgyztan. Zoological Journal of the Linnean Society 161:816838.
Trueb, L., and Alberch, P.. 1985. Miniaturization and the anuran skull: a case study of heterochrony. Pp. 113121 in H. R. Duncker, and G. Fleischer, eds. Functional morphology of vertebrates. Gustav Fischer, Stuttgart, Germany.
Trueb, L., and Cloutier, R.. 1991. A phylogenetic investigation of the inter– and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). Pp. 223313 in H.-P. Schultze, and L. Trueb, eds. Origins of the higher groups of tetrapods. Controversy and consensus. Comstock Publishing, Ithaca, N.Y.
Vallin, G., and Laurin, M.. 2004. Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny and lifestyle of the first amphibians. Journal of Vertebrate Paleontology 24:5672.
Wake, M. H. 1986. The morphology of Idiocranium russeli (Amphibia: Gymnophiona), with comments on miniaturization through heterochrony. Journal of Morphology 189:116.
Werneburg, R. 1986. Die Stegocephalen (Amphibia) der Goldlauterer Schichten (Unterrotliegendes, Perm) des Thüringer Waldes. Teil 1. Apateon flagrifer (Whittard). Freiberger Forschungshefte C 410:88101.
Werneburg, R. 1988. Die Stegocephalender Goldauterer Schichten (Unterrotliegendes, Unterperm). Teil II: Apateon kontheri n. sp., Melanerpeton eisfeldi n. sp. Des Thüringer Waldes und andere. Freiberger Forschungshefte C 427:729.
Werneburg, R. 1989. Die Amphibienfauna der Manebacher Schichten (Unterrotliegendes, Unterperm) des Thüringer Waldes. Veröffentlichungen des Naturhistorischen Museums Schleusingen 4:5568.
Werneburg, R. 2001. Apateon dracyiensis—eine frühe Pionierform der Branchiosaurier aus dem Europaischen Rotliegend. Teil 1: Morphologie. Veröffentlichungen des Naturhistorischen Museums Schleusingen 16:1736.
Witzmann, F., and Pfretzschner, H.-U.. 2003. Larval ontogeny of Micromelerpeton credneri (Temnospondyli, Dissorophoidea). Journal of Vertebrate Paleontology 23:750768.
Witzmann, F., Scholz, H., and Ruta, M.. 2009. Morphospace occupation of temnospondyl growth series: a geometric morphometric approach. Alcheringa 33:237255.
Yeh, J. 2002. The effect of miniaturized body size on skeletal morphology in frogs. Evolution 56:628641.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Paleobiology
  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed