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

Published online by Cambridge University Press:  23 January 2018

Celeste M. Pérez-Ben ,
Rainer R. Schoch  and
Ana M. Báez
Celeste M. Pérez-Ben
Affiliation:
Konrad Lorenz Institute, Klosterneuburg, Niederösterreich 3400, Austria, and Staaliches Museum für Naturkunde, Stuttgart, Baden-Württemberg 70191, Germany. E-mail: [email protected].
Rainer R. Schoch
Affiliation:
Staaliches Museum für Naturkunde, Stuttgart, Baden-Württemberg 70191, Germany.
Ana M. Báez
Affiliation:
CONICET, Departamento de Ciencias Geológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires 1428, Argentina.
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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.

Type
Articles
Information
Paleobiology , Volume 44 , Issue 1 , February 2018 , pp. 58 - 75
Copyright
Copyright © 2018 The Paleontological Society. All rights reserved 

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References

Literature Cited

Anderson, J. S. 2007. Incorporating ontogeny into the matrix: a phylogenetic evaluation of developmental evidence for the origin of modern amphibians. Pp. 182–227 in J. S. Anderson, and H.-D. Sues, eds. Major transitions in vertebrate evolution. Indiana University Press, Bloomington.Google Scholar
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 453:515–518.CrossRefGoogle ScholarPubMed
Angielczyk, K. D., and Ruta, M.. 2012. The roots of amphibian morphospace: a geometric morphometric analysis of Paleozoic Temnospondyls. Fieldiana Life and Earth Sciences 5:40–58.Google Scholar
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 85:201–234.Google Scholar
Atchley, W. R., and Hall, B. K.. 1991. A model for development and evolution of complex morphological structures. Biological Reviews 66:101–157.Google Scholar
Bauchot, R. 1978. Encephalization in vertebrates. Brain, Behavior, and Evolution 15:1–18.Google Scholar
Blomberg, S. P., Lefevre, J. G., Wells, J. A., and Waterhouse, M.. 2012. Independent contrasts and PGLS regression estimators are equivalent. Systematic Biology 61:382–391.Google Scholar
Bolt, J. R. 1969. Lissamphibian origins: possible protolissamphibian from the Lower Permian of Oklahoma. Science 166:888–891.Google Scholar
Bolt, J. R. 1979. Amphibamus grandiceps as a juvenile dissorophoid: evidence and implications. Pp. 529–563 in M. H. Nitecki, ed. Mazon Creek fossils. Academic, New York.Google Scholar
Bolt, J. R. 1991. Lissamphibian origins. Pp. 194–221 in H.-P. Schultze, and L. Trueb, eds. Origins of the higher groups of tetrapods: Controversy and consensus. Comstock Publishing, Ithaca, N.Y.Google Scholar
Bourget, H., and Anderson, J. S.. 2011. A new Amphibamid (Temnospondyli: Dissorophoidea) from the Early Permian of Texas. Journal of Vertebrate Paleontology 31:32–49.Google Scholar
Bolt, J. R., and Lombard, R. E.. 1985. Evolution of the tympanic ear and the origin of frogs. Biological Journal of the Linnean Society 24:83–99.CrossRefGoogle Scholar
Boy, J. A. 1972. Die Branchiosaurier (Amphibia) des saarpfälzischen Rotliegenden (Unter–Perm, SW–Deutschland). Abhandlungen des hessisches Landes-Amtes für Bodenforschung 65:1–137.Google Scholar
Boy, J. A. 1974. Die Larven der rhachitomen Amphibien (Amphibia: Temnospondyli; Karbon–Trias). Paläontologische Zeitschrift 48:236–268.Google Scholar
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 60:131–166.Google Scholar
Boy, J. A. 1987. Studien über die Branchiosauridae (Amphibia: Temnospondyli; Ober-Karbon-Unter-Perm) 2. Systematische Übersicht. Neues Jahrbuch für Geologie und Paläeontologie Abhandlungen 174:75–104.Google Scholar
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 223:241–274.Google Scholar
Boy, J. A., and Sues, H.-D.. 2000. Branchiosaurs: larvae, metamorphosis and heterochrony in temnospondyls and seymouriamorphs. Pp. 1150–1197 in H. Heatwole, and R. L. Carroll, eds. Amphibian biology, Vol. 4. Palaeontology. Surrey Beatty, Chipping Norton, NSW, Australia.Google Scholar
Carroll, R. L. 1964. Early evolution of the dissorophid amphibians. Bulletin of the Museum of Comparative Zoology 131:163–250.Google Scholar
Carroll, R. L. 1970. Quantitative aspects of the amphibian-reptilian transition. Forma et functio 3:165–178.Google Scholar
Carroll, R. L. 1990. A tiny microsaur from the Lower Permian of Texas: size constraints in Palaeozoic tetrapods. Palaeontology 33:893–909.Google Scholar
Carroll, R. L. 2001. The origin and early radiation of terrestrial vertebrates. Journal of Paleontology 75:1202–1213.2.0.CO;2>CrossRefGoogle Scholar
Carroll, R. L. 2009. The rise of amphibians: 365 million years of evolution. Johns Hopkins University Press, Baltimore, Md.CrossRefGoogle Scholar
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 68:1–40.Google Scholar
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 100:275–295.Google Scholar
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 85:1–59.Google Scholar
Dilkes, D. W. 1990. A new trematopsid amphibian (Temnospondyli: Dissorophoidea) from the Lower Permian of Texas. Journal of Vertebrate Paleontology 10:222–243.CrossRefGoogle Scholar
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 2902:1–12.Google Scholar
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1–15.Google Scholar
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 28:1015–1030.CrossRefGoogle Scholar
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 32:35–44.Google Scholar
Fröbisch, N. B., and Schoch, R. R.. 2009. Testing the impact of miniaturization on phylogeny: Paleozoic dissorophoid amphibians. Systematic Biology 58:312–327.Google Scholar
Garland, T. Jr., Bennett, A. F., and Rezende, E. L.. 2005. Phylogenetic approaches in comparative physiology. Journal of Experimental Biology 208:3015–3035.CrossRefGoogle ScholarPubMed
Garland, T. Jr., Harvey, P. H., and Ives, A. R.. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:18–32.CrossRefGoogle Scholar
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 177:255–268.CrossRefGoogle ScholarPubMed
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 23:55–75.CrossRefGoogle Scholar
Hanken, J. 1985. Morphological novelty in the limb skeleton accompanies miniaturization in salamanders. Science 229:871–874.Google Scholar
Hanken, J. 1993. Adaptation of bone growth to miniaturization of body size. Pp. 79–104 in B. K. Hall, ed. Bone. CRC Press, Boca Raton, Fl.Google Scholar
Hanken, J., and Wake, D. B.. 1993. Miniaturization of body size: organismal consequences and evolutionary significance. Annual Review of Ecology and Systematics 24:501–519.Google Scholar
Huxley, J. S. 1932. Problems of Relative Growth. John Hopkins University Press, Baltimore, Md.Google Scholar
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 158:285–365.CrossRefGoogle Scholar
Kimmel, C. B., Sidlauskas, B., and Clack, J. A.. 2009. Linked morphological changes during palate evolution in early tetrapods. Journal of Anatomy 215:91–109.Google Scholar
Kowalewski, M., and Novack-Gottshall, P. M.. 2010. Resampling methods in paleontology. Quantitative Methods in Paleobiology. Short Courses in Paleontology 16:19–54.Google Scholar
Laurin, M., and Reisz, R. R.. 1997. A new perspective on tetrapod phylogeny. Pp. 9–59 in S. S. Sumida, and K. L. Martin, eds. Amniote origins. Academic, New York.CrossRefGoogle Scholar
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 345:562–566.Google Scholar
Lombard, R. E., and Wake, D. B.. 1977. Tongue evolution in the lungless salamanders, family Plethodontidae. II. Function and evolutionary diversity. Journal of Morphology 153:39–80.CrossRefGoogle ScholarPubMed
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 5:59–76.Google Scholar
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 12:393–403.Google Scholar
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.Google Scholar
Marjanovic, D., and Laurin, M.. 2013. The origin(s) of extant amphibians: a review with emphasis on the “lepospondyl hypothesis.” Geodiversitas 35:207–272.CrossRefGoogle 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
Milner, A. R. 1982. Small temnospondyl amphibians from the middle Pennsylvanian of Illinois. Palaeontology 25:635–664.Google Scholar
Milner, A. R. 1988. The relationships and origin of living amphibians. Pp. 59–102 in M. J. Benton, ed. The phylogeny and classification of the tetrapods. Clarendon, Oxford, U.K.Google Scholar
Milner, A. R. 1993. The Paleozoic relatives of lissamphibians. Herpetological Monographs 7:8–27.Google Scholar
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 15:65–73.Google Scholar
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 Google Scholar
Paradis, E., Claude, J., and Strimmer, K.. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.Google Scholar
Polley, B., and Reisz, R. R.. 2011. A new Lower Permian trematopid (Temnospondyli: Dissorophoidea) from Richards Spur, Oklahoma. Zoological Journal of the Linnean Society 161:789–815.Google Scholar
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 96:789–796.Google Scholar
Rieppel, O. 1996. Miniaturization in tetrapods: consequences for skull morphology. Pp. 47–61 in P. J. Miller, ed. Miniature vertebrates: the implications of small body size. Clarendon, Oxford, U.K.Google Scholar
Roček, Z., and Rage, J. C.. 2000. Anatomical transformations in the transitions from temnospondyl to proanuran stages. Pp. 1274–1282 in H. Heatwole, and R. L. Carroll, eds. Amphibian biology, Vol. 4. Palaeontology. Surrey Beatty, Chipping Norton, NSW, Australia.Google Scholar
Ruta, M., Coates, M. I., and Quicke, D. L. J.. 2003. Early tetrapod relationships revisited. Biological Reviews 78:251–345.CrossRefGoogle ScholarPubMed
Rohlf, F. J. 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143–2160.Google Scholar
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 12:315–328.Google Scholar
Schoch, R. R. 1992. Comparative ontogeny of early Permian branchiosaurid amphibians. Developmental stages. Palaeontographica Abteilung A 222:43–83.Google Scholar
Schoch, R. R. 1995. Heterochrony in the development of the amphibian head. Pp. 107–124 in K. J. McNamara, ed. Evolutionary change and heterochrony. Wiley, Chichester, U.K.Google Scholar
Schoch, R. R. 2002. The early formation of the skull in extant and Paleozoic amphibians. Paleobiology 28:278–296.Google Scholar
Schoch, R. R. 2009. Evolution of life cycles in early amphibians. Annual Review of Earth and Planetary Sciences 37:135–162.Google Scholar
Schoch, R. R. 2012a. Character distribution and phylogeny of the dissorophid temnospondyls. Fossil Record 15:119–135.Google Scholar
Schoch, R. R. 2012b. How body size and development biased the direction of evolution in early amphibians. Historical Biology 25:155–165.Google Scholar
Schoch, R. R. 2014a. Amphibian skull evolution: the developmental and functional context of simplification, bone loss and heterotopy. Journal of Experimental Zoology B 322:619–630.CrossRefGoogle ScholarPubMed
Schoch, R. R. 2014b. Life cycles, plasticity and palaeoecology in temnospondyl amphibians. Palaeontology 57:517–529.Google Scholar
Schoch, R. R., and Fröbisch, N. B.. 2006. Metamorphosis and neoteny: alternative pathways in an extinct amphibian clade. Evolution 60:1467–1475.Google Scholar
Schoch, R. R., and Milner, A. R.. 2004. Structure and implications of theories on the origins of lissamphibians. Pp. 345–377 in G. Arratia, and M. V. H. Wilson, eds. Recent advances in the origin and early radiation of vertebrates. Dr. Friederich Pfeil, Munich, Germany.Google Scholar
Schoch, R. R., and Milner, A. R.. 2008. The intrarelationships and evolutionary history of the temnospondyl family Branchiosauridae. Journal of Systematic Palaeontology 6:409–431.Google Scholar
Schoch, R. R., and Milner, A. R.. 2014. Handbook of paleoherpetology—Temnospondyli I. Dr. Friedrich Pfeil, Munich, Germany.Google Scholar
Schoch, R. R., and Rubidge, B. S.. 2005. The amphibamid Micropholis from the Lystrosaurus Assemblage Zone of South Africa. Journal of Vertebrate Paleontology 25:502–522.Google Scholar
Schoch, R. R., and Sues, H.-D.. 2013. A new dissorophid temnospondyl from the Lower Permian of north-central Texas. Comptes Rendus Palevol 12:437–445.Google Scholar
Sessions, S. K. 2008. Evolutionary cytogenetics in salamanders. Chromosome Research 16:183–201.Google Scholar
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 30:1360–1377.Google Scholar
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 161:816–838.Google Scholar
Trueb, L., and Alberch, P.. 1985. Miniaturization and the anuran skull: a case study of heterochrony. Pp. 113–121 in H. R. Duncker, and G. Fleischer, eds. Functional morphology of vertebrates. Gustav Fischer, Stuttgart, Germany.Google Scholar
Trueb, L., and Cloutier, R.. 1991. A phylogenetic investigation of the inter– and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). Pp. 223–313 in H.-P. Schultze, and L. Trueb, eds. Origins of the higher groups of tetrapods. Controversy and consensus. Comstock Publishing, Ithaca, N.Y.Google Scholar
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 24:56–72.Google Scholar
Wake, M. H. 1986. The morphology of Idiocranium russeli (Amphibia: Gymnophiona), with comments on miniaturization through heterochrony. Journal of Morphology 189:1–16.Google Scholar
Werneburg, R. 1986. Die Stegocephalen (Amphibia) der Goldlauterer Schichten (Unterrotliegendes, Perm) des Thüringer Waldes. Teil 1. Apateon flagrifer (Whittard). Freiberger Forschungshefte C 410:88–101.Google Scholar
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 427:7–29.Google Scholar
Werneburg, R. 1989. Die Amphibienfauna der Manebacher Schichten (Unterrotliegendes, Unterperm) des Thüringer Waldes. Veröffentlichungen des Naturhistorischen Museums Schleusingen 4:55–68.Google Scholar
Werneburg, R. 2001. Apateon dracyiensis—eine frühe Pionierform der Branchiosaurier aus dem Europaischen Rotliegend. Teil 1: Morphologie. Veröffentlichungen des Naturhistorischen Museums Schleusingen 16:17–36.Google Scholar
Witzmann, F., and Pfretzschner, H.-U.. 2003. Larval ontogeny of Micromelerpeton credneri (Temnospondyli, Dissorophoidea). Journal of Vertebrate Paleontology 23:750–768.Google Scholar
Witzmann, F., Scholz, H., and Ruta, M.. 2009. Morphospace occupation of temnospondyl growth series: a geometric morphometric approach. Alcheringa 33:237–255.Google Scholar
Yeh, J. 2002. The effect of miniaturized body size on skeletal morphology in frogs. Evolution 56:628–641.Google Scholar