Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-19T21:47:00.870Z Has data issue: false hasContentIssue false
  • English
  • Français

Heterochrony: the interplay between development and ecology exemplified by a Paleozoic amphibian clade

Published online by Cambridge University Press:  08 April 2016

Rainer R. Schoch
Rainer R. Schoch*
Affiliation:
Staatliches Museum für Naturkunde, Rosenstein 1, D-70191 Stuttgart, Germany. E-mail: schoch.smns@naturkundemuseum-bw.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent studies have provided detailed insight into life cycles of early amphibians. These ontogenies were diverse and their evolution involved numerous kinds of change, which can now be addressed by comparison of ontogenetic trajectories. The plesiomorphic trajectory included (1) an early period in which a larval, aquatic predator was established, (2) an intermediate period in which the axial skeleton was strengthened, and (3) a final period during which the jaw joint, braincase, and limbs were ossified, producing an adult capable of terrestrial locomotion if completed. Heterochrony, among other factors, enabled the fine-tuning of the ontogenetic formation of ecologically important features (feeding, respiration, locomotion). Most common was a simple truncation of the trajectory that produced aquatic taxa of various kinds, while changes in the ontogenetic sequence often had a deeper impact on morphology. The most fundamental changes were accompanied by multiple heterochronies, resulting in the condensation or unpacking (stretch-out) of developmental events: metamorphosis evolved by an ever closer packing, whereas a novel larval feeding mechanism was established by a pull-apart of numerous critical events.

Type
Articles
Information
Paleobiology , Volume 36 , Issue 2 , Spring 2010 , pp. 318 - 334
Copyright
Copyright © The Paleontological Society 

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

Alberch, P. 1985. Problems with the interpretation of developmental sequences. Systematic Zoology 34:46–58.CrossRefGoogle Scholar
Alberch, P. 1989. Development and the evolution of amphibian metamorphosis. Fortschritte der Zoologie 35:163–173.Google Scholar
Alberch, P., Gould, S. J., Oster, G. F., and Wake, D. B. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317.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.Google Scholar
Boy, J. A. 1974. Die Larven der rhachitomen Amphibien (Amphibia: Temnospondyli; Karbon-Trias). Paläontologische Zeitschrift 48:236–268.CrossRefGoogle Scholar
Boy, J. A. 1977. Typen und Genese jungpaläozoischer Tetrapoden-Lagerstätten. Palaeontographica, Abteilung A 156:111–167.Google Scholar
Boy, J. A. 1987. Die Tetrapoden-Lokalitäten des saarpfälzischen Rotliegenden (Unter-Perm; SW-Deutschland) und die Biostratigraphie der Rotliegend-Tetrapoden. Mainzer Geowissenschaftliche Mitteilungen 16:31–65.Google Scholar
Boy, J. A. 1990. Über einige Vertreter der Eryopoidea (Amphibia: Temnospondyli) aus dem europäischen Rotliegend (? höchstes Karbon – Perm). 3. Onchiodon . Paläontologische Zeitschrift 64:287–312.Google Scholar
Boy, J. A. 1993. Über einige Vertreter der Eryopoidea (Amphibia: Temnospondyli) aus dem europäischen Rotliegend (? höchstes Karbon – Perm). 4. Cheliderpeton latirostre . Paläontologische Zeitschrift 67:123–143.Google Scholar
Boy, J. A. 1995. Über die Micromelerpetontidae (Amphibia: Temnospondyli). 1. Morphologie und Paläoökologie des Micromelerpeton credneri (Unter-Perm; SW-Deutschland). Paläontologische Zeitschrift 69:429–457.Google Scholar
Boy, J. A. 2003. Paläoökologische Rekonstruktion von Wirbeltieren: Möglichkeiten und Grenzen. Paläontologische Zeitschrift 77:123–152.Google Scholar
Boy, J. A., and Sues, H. D. 2000. Branchiosaurs: larvae, metamorphosis and heterochrony in temnospondyls and seymouriamorphs. Pp. 1150–1197 in Heatwole, H. and Carroll, R. L., eds. Amphibian biology, Vol. 4. Palaeontology. Surrey Beatty, Chipping Norton, N.S.W., Australia.Google Scholar
Clack, J. A., and Milner, A. R. 2007. The amphibamid Platyrhinops, morphology and metamorphosis. Journal of Vertebrate Paleontology 27:59A.Google Scholar
Collins, J. P., and Cheek, J. E. 1983. Effect of food and density on development of typical and cannibalistic salamander larvae in Ambystoma tigrinum nebulosum . American Zoologist 23:77–84.Google Scholar
Damiani, R. J. 2001. A systematic revision and phylogenetic analysis of Triassic mastodonsauroids (Temnospondyli, Stereospondyli). Zoological Journal of the Linnean Society London 133:379–482.Google Scholar
Denoel, M., Hervant, F., Schabetsberger, R., and Joly, P. 2002. Short- and long-term advantages of an alternative ontogenetic pathway. Biological Journal of the Linnean Society 77:105–112.Google Scholar
Duellman, W. E., and Trueb, L. 1986. Biology of Amphibians. McGraw-Hill, New York.Google Scholar
Fröbisch, N. B., and Schoch, R. R. 2009a. The largest specimen of Apateon and the life history pathway of neoteny in the Paleozoic temnospondyl family Branchiosauridae. Fossil Record 12:83–90.Google Scholar
Fröbisch, N. B., and Schoch, R. R. 2009b. Testing the impact of miniaturization on phylogeny: Paleozoic dissorophoid amphibians. Systematic Biology 58:312–327.Google Scholar
Fröbisch, N. B., Carroll, R. L., and Schoch, R. R. 2007. Limb ossification in the Paleozoic branchiosaurid Apateon (Temnospondyli) and the early evolution of preaxial dominance in tetrapod limb development. Evolution and Development 9:69–75.Google Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Belknap Press of Harvard University Press, Cambridge.Google Scholar
Hall, B. K. 1984. Developmental processes underlying heterochrony as an evolutionary mechanism. Canadian Journal of Zoology 62:1–7.Google Scholar
Klingenberg, C. P. 1998. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews 73:79–123.Google Scholar
McKinney, M. 1999. Heterochrony: beyond words. Paleobiology 25:149–153.CrossRefGoogle Scholar
McKinney, M., and McNamara, K. 1991. Heterochrony: the evolution of ontogeny. Plenum, New York.Google Scholar
Michimae, H., and Wakahara, M. 2001. Factors which affect the occurrence of cannibalism and the broad-headed “cannibal” morph in larvae of the salamander Hynobius retardatus . Behaviour, Ecology and Sociobiology 50:339–345.Google Scholar
Milner, A. R. 1980. The tetrapod assemblage from Nýřany, Czechoslovakia. Pp. 439–496 in Panchen, A. L., ed. The terrestrial environment and the origin of land vertebrates. Academic Press, New York.Google Scholar
Milner, A. R. 1982. Small temnospondyl amphibians from the Middle Pennsylvanian of Illinois. Palaeontology 25:635–664.Google Scholar
Milner, A. R. 1993. The Paleozoic relatives of lissamphibians. Herpetological Monographs 7:8–27.Google Scholar
Milner, A. R. 2007. Mordex laticeps and the base of the Trematopidae. Journal of Vertebrate Paleontology 27:118A.Google Scholar
Poe, S. 2006. Test of von Baer's law of the conservation of early development. Evolution 60:2239–2245.Google Scholar
Poe, S., and Wake, M. H. 2004. Quantitative tests of general models for the evolution of development. American Naturalist 164:415–422.Google Scholar
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.CrossRefGoogle Scholar
Roux, J., and Robinson-Rechavi, M. 2008. Developmental constraints on vertebrate genome evolution. PLOS Genetics 4:1–10.CrossRefGoogle ScholarPubMed
Ruta, M., Jeffrey, E., and Coates, M. I. 2003a. A supertree of early tetrapods. Proceedings of the Royal Society of London B 270:2507–2516.Google Scholar
Ruta, M., Coates, M. I., and Quicke, D. L. J. 2003b. Early tetrapod relationships revisited. Biological Reviews 78:251–345.Google Scholar
Ruta, M., Pisani, D., Lloyd, G. T., and Benton, M. J. 2007. A supertree of Temnospondyli: cladogenetic patterns in the most species-rich group of early tetrapods. Proceedings of the Royal Society of London B 274:3087–3095.Google Scholar
Sanchez, S., de Ricqlès, A., Steyer, J. S., and Schoch, R. R. 2010. Palaeoecological and palaeoenvironmental influences revealed by long-bone palaeohistology: the example of the Permian branchiosaurid Apateon . Geological Society Special Volume (in press).Google Scholar
Schlichting, C., and Pigliucci, M. 1998. Phenotypic evolution: a reaction norm perspective. Sinauer, Sunderland, Mass. Google Scholar
Schneider, J. 1994. Environment, biotas and taphonomy of the Lower Permian lacustrine Niederhäslich limestone, Döhlen basin, Germany. Transactions of the Royal Society of Edinburgh (Earth Sciences) 84:453–464.Google Scholar
Schoch, R. R. 1992. Comparative ontogeny of early Permian branchiosaurid amphibians from southwestern Germany. Developmental stages. Palaeontographica A 222:43–83.Google Scholar
Schoch, R. R. 1995. Heterochrony in the evolution of the amphibian head. Pp. 107–124 in McNamara, K., ed. Evolutionary change and heterochrony. Wiley, Chichester, U.K. Google Scholar
Schoch, R. R. 2002a. The early formation of the skull in extant and fossil amphibians. Paleobiology 28:278–296.Google Scholar
Schoch, R. R. 2002b. The evolution of metamorphosis in temnospondyls. Lethaia 35:309–327.Google Scholar
Schoch, R. R. 2003. Early larval ontogeny of the Permo-Carboniferous temnospondyl Sclerocephalus . Palaeontology 46:1055–1072.Google Scholar
Schoch, R. R. 2004. Skeleton formation in the Branchiosauridae: a case study in comparing ontogenetic trajectories. Journal of Vertebrate Paleontology 24:309–319.CrossRefGoogle Scholar
Schoch, R. R. 2006. Skull ontogeny: ossification sequences of fishes conserved across major clades of tetrapods. Evolution and Development 8:524–536.Google Scholar
Schoch, R. R. 2008. A new stereospondyl from the German Middle Triassic and the origin of the Metoposauridae. Zoological Journal of the Linnean Society 52:79–113.CrossRefGoogle Scholar
Schoch, R. R. 2009a. The evolution of life cycles in early amphibians. Annual Review of Earth and Planetary Sciences 37:135–162.Google Scholar
Schoch, R. R. 2009b. Developmental evolution as a response to diverse lake habitats in Paleozoic amphibians. Evolution 63:2738–2749.Google Scholar
Schoch, R. R. 2010. Riedl's burden and the body plan: selection, constraint, and deep time. Journal of Experimental Zoology B (Molecular and Developmental Evolution) 314B:1–10.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. 2008. The intrarelationships and evolutionary history of the Permo-Carboniferous temnospondyl family Branchiosauridae. Journal of Systematic Palaeontology 6:409–431.Google Scholar
Schoch, R. R., and Witzmann, F. 2009. Osteology and relationships of the Permo-Carboniferous temnospondyl Sclerocephalus . Zoological Journal of the Linnean Society 157:135–168.Google Scholar
Sequeira, S. E. K. 2004. The skull of Cochleosaurus bohemicus Frič, a temnospondyl from the Czech Republic (Upper Carboniferous) and cochleosaurid interrelationships. Transactions of the Royal Society of Edinburgh (Earth Sciences) 94:21–43.CrossRefGoogle Scholar
Smith, K. K. 2001. Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society 73:169–186.Google Scholar
Smith, K. K. 2003. Time's arrow: heterochrony and the evolution of development. International Journal of Developmental Biology 47:613–621.Google Scholar
Sprules, W. G. 1974. The adaptive significance of paedogenesis in North American species of Ambystoma (Amphibia: Caudata): an hypothesis. Canadian Journal of Zoology 52:393–400.Google Scholar
Steen, M. C. 1938. On the fossil Amphibia from the Gas Coal of Nýřany and other deposits in Czechoslovakia. Proceedings of the Zoological Society of London B 108:205–283.CrossRefGoogle Scholar
Steyer, J. S., Damiani, R. J., Sidor, C. A., O'Keefe, F. R., Larsson, H. C. E., Maga, A., and Ide, O. 2006. The vertebrate fauna of the Upper Permian of Niger. IV. Nigerpeton ricqlesi (Temnospondyli: Cochleosauridae), and the edopoid colonization of Gondwana. Journal of Vertebrate Paleontology 26:18–28.Google Scholar
Van Valen, L. 1973. Festschrift. Science 180:488.Google Scholar
Wake, D. B. 1991. Homoplasy: the result of natural selection, or evidence of design limitations? American Naturalist 138:543–567.Google Scholar
Wake, D. B., and Larson, A. 1987. Multidimensional analysis of an evolving lineage. Science 238:42–48.Google Scholar
Warren, A. A., and Hutchinson, M. N. 1988. A new capitosaurid amphibian from the early Triassic of Queensland, and the ontogeny of the capitosaur skull. Palaeontology 31:857–876.Google Scholar
Warren, A. A., and Schroeder, N. 1995. Changes in the capitosaur skull with growth: an extension of the growth series of Parotosuchus aliciae (Amphibia, Temnospondyli) with comments on the otic area of capitosaurs. Alcheringa 19:41–46.Google Scholar
Webster, M., and Zelditch, M. L. 2005. Evolutionary modifications of ontogeny: heterochrony and beyond. Paleobiology 31:354–372.Google Scholar
Werneburg, R. 1991. Die Branchiosaurier aus dem Unterrotliegend des Döhlener Beckens bei Dresden. Veröffentlichungen des Naturhistorischen Museums Schleusingen 6:75–99.Google Scholar
Werneburg, R. 2002. Apateon dracyiensis—eine frühe Pionierform aus dem europäischen Rotliegend, Teil 2: Palökologie. Veröffentlichungen des Naturhistorischen Museums Schleusingen 17:17–32.Google Scholar
Werneburg, R. 2008. Der “Manebacher Saurier”—ein neuer großer Eryopide (Onchiodon) aus dem Rotliegend (Unter-Perm) des Thüringer Waldes. Veröffentlichungen des Naturhistorischen Museums Schleusingen 22:3–40.Google Scholar
West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford University Press, Oxford.Google Scholar
Whiteman, H. 1994. Evolution of facultative paedomorphosis in salamanders. Quarterly Review of Biology 69:205–221.Google Scholar
Witzmann, F. 2005. Hyobranchial and postcranial ontogeny of the temnospondyl Onchiodon labyrinthicus (Geinitz, 1861) from Niederhäslich (Döhlen Basin, Autunian, Saxony). Paläontologische Zeitschrift 79:479–492.Google Scholar
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.Google Scholar
Witzmann, F. 2009. Cannibalism in a small growth stage of the Early Permian branchiosaurid Apateon gracilis (Crender, 1881) from Saxony. Fossil Record 12:7–11.Google Scholar
Witzmann, F., and Pfretzschner, H.-U. 2003. Larval ontogeny of Micromelerpeton credneri (Temnosposndyli, Dissorophoidea). Journal of Vertebrate Paleontology 23:750–768.Google Scholar
Witzmann, F., and Schoch, R. R. 2006. Skeletal development of Acanthostomatops vorax from the Döhlen Basin of Saxony. Transactions of the Royal Society of Edinburgh (Earth Sciences) 96:365–385.Google Scholar
Yates, A. M., and Warren, A. A. 2000. The phylogeny of the ‘higher’ temnospondyls (Vertebrata: Choanata) and its implications for the monophyly and origins of the Stereospondyli. Zoological Journal of the Linnean Society 128:77–121.Google Scholar
Zelditch, M., and Fink, W. L. 1996. Heterochrony and heterotopy: stability and innovation in the evolution of form. Paleobiology 22:241–254.Google Scholar