Life cycles, plasticity and palaeoecology in temnospondyl amphibians

57 3 May 517 529 10.1111/pala.12100

SCHOCH, R. R.. 2014, Life cycles, plasticity and palaeoecology in temnospondyl amphibians. Palaeontology, 57, 3, 517–529. doi: 10.1111/pala.12100

<p>Rainer R. Schoch</p>
  • Issue published online: 7 MAY 2014
  • Article first published online: 17 MAR 2014
  • Manuscript Accepted: 30 DEC 2013
  • Manuscript Received: 6 OCT 2013

In the largest early tetrapod clade, the temnospondyls, ontogenies were diverse and quite distinct from the life cycles of extant amphibians. Three well-studied clades exemplify the diversity of these long-extinct ontogenies, here analysed with respect to their bearing on developmental plasticity, reaction norms and evolution. Sclerocephalus readily adjusted by means of developmental evolution to different lake environments. In addition, plasticity (reaction norm) played a significant role, apparent both morphologically and by altered developmental traits. Size increase and extension of the ontogenetic trajectory gave larger predators, a phenomenon also found in the dissorophoid Micromelerpeton. Whereas Sclerocephalus was throughout preying on the same fishes, Micromelerpeton was able to fit into different trophic levels. In the branchiosaurid Apateon, a biphasic life cycle was established, with metamorphosis producing a terrestrial morph in some species; truncation of the ontogenetic trajectory gave a sexually mature larva as an alternative morph (neoteny). Plasticity was high in the larval morphs, permitting neotenes to live as filter feeders or small carnivores. Fine-tuning of development permitted Apateon populations to adjust to specific lake properties and readily change from a filter-feeding to carnivorous mode of life. In the nonmetamorphosing Triassic Gerrothorax, morphology was extremely conserved, but histology reveals much plasticity at the microscopical level, correlating with fluctuating salinity and water energy. In responding to environmental fluctuations by enhanced plasticity, the studied temnospondyls managed to populate lakes inhabitable to other tetrapods and fishes.

  • Anderson, J. S. 2008. Focal Review: the origin(s) of modern amphibians. Evolutionary Biology, 35, 231–247.
  • Boy, J. A. 1972. Die Branchiosaurier (Amphibia) des saarpflzischen Rotliegenden (Perm, SW-Deutschland). Abhandlungen des Hessischen Landesamts für Bodenforschung, 65, 1–137.
  • Boy, J. A. 1974. Die Larven der rhachitomen Amphibien (Amphibia: Temnospondyli; Karbon – Trias). Palontologische Zeitschrift, 48, 236–282.
  • Boy, J. A. 1987. Studien über die Branchiosauridae (Amphibia: Temnospondyli; OberKarbon – Unter-Perm) 2. Systematische Übersicht. Neues Jahrbuch für Geologie und Palontologie Abhandlungen, 174, 75–104.
  • Boy, J. A. 1990. Über einige Vertreter der Eryopoidea (Amphibia: Temnospondyli) aus dem europischen Rotliegend (? höchstes Karbon—Perm). 3. Onchiodon. Palontologische Zeitschrift, 64, 287–312.
  • Boy, J. A. 1995. Über die Micromelerpetontidae (Amphibia: Temnospondyli). 1. Morphologie und Paloökologie des Micromelerpeton credneri (Unter-Perm; SW-Deutschland). Palontologische Zeitschrift, 69, 429–457.
  • Boy, J. A. 2002a. Über die Micromelerpetontidae (Amphibia: Temnospondyli). 2. Micromelerpeton ulmetense n.sp. und Micromelerpeton(?) boyi Heyler. Neues Jahrbuch für Geologie und Palontologie Abhandlungen, 223, 241–274.
  • Boy, J. A. 2002b. Über die Micromelerpetontidae (Amphibia: Temnospondyli). 3. Eimerisaurus n.g. Neues Jahrbuch für Geologie und Palontologie Abhandlungen, 225, 425–452.
  • Boy, J. A. 2003. Paloökologische Rekonstruktion von Wirbeltieren: Möglichkeiten und Grenzen. Palontologische Zeitschrift, 77, 123–152.
  • Boy, J. A. and Sues, H. D. 2000. Branchiosaurs: larvae, metamorphosis and heterochrony in temnospondyls and seymouriamorphs. 973–1496. In Heatwole, H. and Carroll, R. L. (eds). Amphibian biology. Volume 4. Palaeontology. Surrey Beattey, Chipping Norton, NSW, 448 pp.
  • Carroll, R. L. 1989. Developmental aspects of lepospondyl vertebrae in Paleozoic tetrapods. Historical Biology, 3, 1–25.
  • Carroll, S. B. 2005. Endless forms most beautiful. The new science of evo-devo. Norton, London, 350 pp.
  • Carroll, S. B. 2008. Evo-Devo and an expanding Evolutionary Synthesis: a genetic theory of morphological evolution. Cell, 134, 25–36.
  • Davidson, E. H. 2006. The regulatory genome. Academic Press, London, 289 pp.
  • Flatt, T. 2005. The evolutionary genetics of canalization. Quarterly Review of Biology, 80, 287–316.
  • Fröbisch, N. B. and Schoch, R. R. 2009. The largest specimen of Apateon, and the life history pathway of neoteny in the Palaeozoic family Branchiosauridae. Fossil Record, 12, 83–90.
  • Hall, B. K. 1999. Evolutionary developmental biology. Kluwer, Dordrecht, 491 pp.
  • Hellrung, H. 2003. Gerrothorax pustuloglomeratus, ein Temnospondyle (Amphibia) mit knöcherner Branchialkammer aus dem Unteren Keuper von Kupferzell (Süddeutschland). Stuttgarter Beitrge zur Naturkunde, B, 330, 1–130.
  • Marjanovi&#x107;, D. and Laurin, M. 2008. A reevaluation of the evidence supporting an unorthodox hypothesis on the origin of extant amphibians. Contributions to Zoology, 77, 149–199.
  • Pigliucci, M. 2007. Do we need an extended evolutionary synthesis? Evolution, 61, 2743–2747.
  • Raff, R. A. 1996. The shape of life. Genes, development, and the evolution of animal form. University of Chicago Press, Chicago, 520 p.
  • Reilly, S. M. 1987. Ontogeny of the hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): the ecological morphology of two neotenic strategies. Journal of Morphology, 191, 205–214.
  • Reilly, S. M., Wiley, E. O. and Meinhardt, D. J. 1997. An integrative approach to heterochrony: distinguishing intraspecific and interspecific phenomena. Biological Journal of the Linnean Society, 60, 119–143.
  • Ruta, M. and Coates, M. I. 2007. Dates, nodes and character conflict: addressing the lissamphibian origin problem. Journal of Systematic Palaeontology, 5, 69–122.
  • Sanchez, M. 2012. Embryos in deep time. University of California Press, 256 pp.
  • Sanchez, S. and Schoch, R. R. 2013. Bone histology reveals a high environmental and metabolic plasticity as a successful evolutionary strategy in a long-lived homeostatic temnospondyl. Evolutionary Biology, 40, 627–647. doi: http://dx.doi.org/10.1007/s11692-013-9238-3
  • Sanchez, S., de Ricqles, A., Schoch, R. R. and Steyer, J. S. 2010a. Developmental plasticity of limb bone microstructural organization in Apateon: histological evidence of paedomorphic conditions in branchiosaurs. Evolution and Development, 12, 315–328.
  • Sanchez, S., Steyer, J. S., Schoch, R. R. and de Ricqles, A. 2010b. Palaeoecological and palaeoenvironmental influences revealed by long-bone palaeohistology: the example of the Permian branchiosaurid Apateon. 139–149. In Vecoli, M., Clement, G. and Meyer Berthaud, B. (eds). The terrestrialization process: modelling complex interactions at the biosphere-geosphere Interface. The Geological Society, London, 179 pp.
  • Schindler, T. 2011. Der Niederkirchen-See des Saar-Nahe-Beckens: ein Lebensraum für Haie (Perm, Rotliegend; SW-Deutschland). Semana, 26, 7–12.
  • Schlichting, C. and Pigliucci, M. 1998. Phenotypic evolution. A Reaction Norm Perspective, Sinauer, Sunderland, 387 pp.
  • Schmalhausen, I. I. 1949. Factors of evolution. University of Chicago Press, Chicago, 327 pp.
  • Schoch, R. R. 1995. Heterochrony in the development of the amphibian head. 107–124. In McNamara, K. J. (ed.). Evolutionary change and heterochrony, John Wiley and Sons, Chichester, 286 pp.
  • Schoch, R. R. 2004. Skeleton formation in the Branchiosauridae as a case study in comparing ontogenetic trajectories. Journal of Vertebrate Paleontology, 24, 309–319.
  • Schoch, R. R. 2009a. The evolution of life cycles in early amphibians. Annual Review of Earth and Planetary Sciences, 37, 135–162.
  • Schoch, R. R. 2009b. Developmental evolution as response to diverse lake habitats in Paleozoic amphibians. Evolution, 63, 2738–2749.
  • Schoch, R. R. 2010. Heterochrony: the interplay between development and ecology in an extinct amphibian clade. Paleobiology, 36, 318–334.
  • Schoch, R. R. 2013. The evolution of major temnospondyl clades: an inclusive phylogenetic analysis. Journal of Systematic Palaeontology, 11, 673–705.
  • Schoch, R. R. 2014. Amphibian evolution. The life of early land vertebrates. Wiley, New York, 296 pp.
  • Schoch, R. R. and Fröbisch, N. B. 2006. Metamorphosis and neoteny: alternative developmental pathways in an extinct amphibian clade. Evolution, 60, 1467–1475.
  • 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.
  • Schoch, R. R. and Witzmann, F. 2011. Bystrow's Paradox: gills, fossils, and the fish-to-tetrapod transition. Acta Zoologica, 92, 251–265.
  • Schoch, R. R. and Witzmann, F. 2012. Cranial morphology of the plagiosaurid Gerrothorax pulcherrimus as an extreme example of evolutionary stasis. Lethaia, 45, 371–385.
  • Stearns, S. C. 1992. The evolution of life histories. Oxford University Press, Oxford, 249 pp.
  • Valentine, B. D. and Dennis, D. M. 1964. A comparison of the gill-arch system and fins of three genera of larval salamanders, Rhyacotriton, Gyrinophilius, and Ambystoma. Copeia, 1964, 196–201.
  • Wagner, G. P. and Larsson, H. C. E. 2003. What is the promise of developmental evolution? III. The crucible of developmental evolution. Journal of Experimental Zoology, 300B, 1–4.
  • Werneburg, R. 1991. Die Branchiosaurier aus dem Unterrotliegend des Döhlener Beckens bei Dresden. Veröffentlichungen Naturhistorisches Museum Schleusingen, 6, 75–99.
  • Werneburg, R. 2001. Apateon dracyiensis – eine frühe Pionierform der Branchiosaurier aus dem europischen Rotliegend. Teil 1: Morphologie. Veröffentlichungen Naturhistorisches Museum Schleusingen, 16, 17–36.
  • Werneburg, R. 2002. Apateon dracyiensis – eine frühe Pionierform der Branchiosaurier aus dem europischen Rotliegend. Teil 2: Paloökologie. Veröffentlichungen Naturhistorisches Museum Schleusingen, 17, 17–32.
  • West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford University Press, Oxford, 797 pp.
  • Witzmann, F. 2006. Developmental patterns and ossification sequence in the Permo-Carboniferous temnospondyl Archegosaurus decheni (Saar-Nahe Basin, Germany). Journal of Vertebrate Paleontology, 26, 7–17.
  • Witzmann, F. 2009. Cannibalism in a small growth stage of the branchiosaurid Apateon gracilis (Credner, 1881) from the Early Permian Döhlen Basin, Saxony. Fossil Record, 12, 7–11.
  • Witzmann, F. and Pfretzschner, H. U. 2003. Larval ontogeny of Micromelerpeton credneri (Temnosposndyli, Dissorophoidea). Journal of Vertebrate Paleontology, 23, 750–768.
  • Witzmann, F. and Schoch, R. R. 2013. Reconstruction of cranial and hyobranchial muscles in the Triassic temnospondyl Gerrothorax provides evidence for akinetic suction feeding. Journal of Morphology, 274, 525–542.
  • Witzmann, F. and Soler-Gijón, R. 2010. The bone histology of osteoderms in temnospondyl amphibians and in the chroniosuchian Bystrowiella. Acta Zoologica, 91, 96–114.
  • Woltereck, R. 1909. Weitere experimentelle Untersuchungen über Artvernderung, speziell über das Wesen quantitativer Artunterschiede der Daphniden. Verhandlungsbericht der Deutschen Zoologischen Gesellschaft, 1909, 110–172.
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