Skip to main content
Log in

Patterns of skull development in anurans: size and shape relationship during postmetamorphic cranial ontogeny in five species of the Leptodactylus fuscus Group (Anura: Leptodactylidae)

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

The effect of allometric ontogenetic changes on morphology has been examined primarily in larval stages of anurans. To our knowledge, such studies after metamorphosis are non-existent, and this information is important because the skull acquires its adult configuration in that period. Using geometric morphometrics, we studied postmetamorphic shape changes in the skull of five species of the Leptodactylus fuscus Group (Leptodactylus bufonius, Leptodactylus elenae, Leptodactylus fuscus, Leptodactylus latinasus, and Leptodactylus mystaceus), a group of small- to medium-sized frogs. Size change is an important factor in explaining shape change during postmetamorphic growth in four of these species; ontogenetic trajectories have in general parallel directions and similar rates of shape change. L. latinasus skulls tend to differ in size and shape from the others, and the allometric model, although significant, explains low percentages of shape change. The diverging slope of its ontogenetic trajectory indicates non-heterochronic, allometric repatterning change regarding the ontogenies of L. bufonius, L. elenae, and L. fuscus. Conversely, ontogenetic scaling appears as the main mechanism modeling shape change as regard to L. mystaceus; hence, we suggest that a process of progenesis determines the small, juvenile-like cranium of L. latinasus. The disparity analysis shows a broader morphological divergence in metamorph morphospace than in adults, suggesting that postmetamorphic stages can contribute with informative characters to phylogenetic analysis. Differences in shapes between metamorphs and adults indicate that many changes occur after metamorphosis, but whether these changes result from internal or ecological requirements at different stages remains unknown.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams DC, Nistri A (2010) Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evol Biol 10:216

    Article  PubMed  Google Scholar 

  • Alberch P, Alberch J (1981) Heterochronic mechanisms of morphological diversification and evolutionary change in the Neotropical salamander, Bolitoglossa occidentalis (Amphibia: Plethodontidae). J Morphol 167:249–264

    Article  Google Scholar 

  • Alberch P, Gould SJ, Oster GF, Wake DB (1979) Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317

    Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Cardini A, Elton S (2007) Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology 126:121–134

    Article  Google Scholar 

  • Ciampaglio CN (2002) Determining the role that ecological and developmental constraints play in controlling disparity: examples from the crinoid and blastozoan fossil record. Evol Dev 4:170–188

    Article  PubMed  Google Scholar 

  • Clarke BT (1996) Small size in amphibians: its ecological and evolutionary implications. Symp Zool Soc London 69:201–224

    Google Scholar 

  • Djorović A, Kalezić ML (2000) Paedogenesis in European newts (Triturus: Salamandridae): cranial morphology during ontogeny. J Morphol 243:127–139

    Article  PubMed  Google Scholar 

  • Drake AG, Klingenberg CP (2008) The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc B 275:71–76

    Article  PubMed  Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of amphibians. The John Hopkins University Press, Baltimore, MD

    Google Scholar 

  • Dzukic G, Kalezic ML, Tvrtkovic N, Djorovic A (1990) An overview of the occurrence of paedomorphosis in Yugoslav newt (Triturus, Salamandridae) populations. Br Herpetol Soc Bull 34:16–22

    Google Scholar 

  • Eble EJ (2003) Developmental morphospaces and evolution. In: Crutchfield JP, Schuster P (eds) Evolutionary dynamics. Oxford University Press, Oxford, pp 35–65

    Google Scholar 

  • Emerson SB, Bramble DM (1993) Scaling, allometry, and skull design. In: Hanken J, Hall BK (eds) The skull, vol 3., Functional and evolutionary mechanisms. University of Chicago Press, Chicago, IL, pp 384–421

    Google Scholar 

  • Fink WL (1982) The conceptual relationship between ontogeny and phylogeny. Paleobiology 8:254–264

    Google Scholar 

  • Fink WL (1988) Phylogenetic analysis and the detection of ontogenetic patterns. In: McKinney ML (ed) Heterochrony in evolution: a multidisciplinary approach. Plenum, New York, NY, pp 71–91

    Google Scholar 

  • Frédérich B, Sheets HD (2010) Evolution of ontogenetic allometry shaping giant species: a case study from the damselfish genus Dascyllus (Pomacentridae). Biol J Linn Soc 99:99–117

    Article  Google Scholar 

  • Frédérich B, Vandewalle P (2011) Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: an example from damselfishes (Pomacentridae). BMC Evol Biol 11:82

    Article  PubMed  Google Scholar 

  • Frost DR (2011) Amphibian species of the world: an online reference. Version 5.5 (31 January, 2011). Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/. American Museum of Natural History, New York, NY

  • Gerber S, Neige P, Gunther JE (2007) Combining ontogenetic and evolutionary scales of morphological disparity: a study of early Jurassic ammonites. Evol Dev 9:472–482

    Article  PubMed  Google Scholar 

  • Gerber S, Gunther JE, Neige P (2008) Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity. Evolution 62:1450–1457

    Article  PubMed  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anurans embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Goswami A, Prochel J (2007) Ontogenetic morphology and allometry of the cranium in the common european mole (Talpa europaea). J Mamm 88:667–677

    Article  Google Scholar 

  • Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev 41:587–640

    Article  PubMed  CAS  Google Scholar 

  • Gould SJ (1977) Ontogeny and phylogeny. Harvard University Press, Cambridge

    Google Scholar 

  • Hanken J (1984) Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia: Plethodontidae). I. Osteological variation. Biol J Linn Soc 23:55–75

    Article  Google Scholar 

  • Hanken J, Wake DB (1993) Miniaturization of body size: organismal consequences and evolutionary significance. Annu Rev Ecol Syst 24:501–519

    Article  Google Scholar 

  • Heyer WR (1969) Studies on the genus Leptodactylus (Amphibia, Leptodactylidae) III. A redefinition of the genus Leptodactylus and a description of a new genus of Leptodactylid frogs. Contrib Sci Nat Hist Mus Los Angel Cty 155:1–14

    Google Scholar 

  • Heyer WR (1978) Systematics of the fuscus group of the genus Leptodactylus (Amphibia, Leptodactylidae). Contrib Sci Nat Hist Mus Los Angel Cty 29:1–85

    Google Scholar 

  • Heyer RW (2005) Variation and taxonomic clarification of the large species of the Leptodactylus pentadactylus species group (Amphibia: Leptodactylidae) from Middle America, Northern South America, and Amazonia. Arq Zool 37:1–86

    Google Scholar 

  • Heyer RW, Juncá FA (2003) Leptodactylus caatingae, a new species of frog from eastern Brazil (Amphibia: Anura: Leptodactylidae). Proc Biol Soc Wash 116:317–329

    Google Scholar 

  • Heyer WR, García-Lopez JM, Cardoso A (1996) Advertisement call variation in the Leptodactylus mystaceus species complex (Amphibia: Leptodactylidae) with a description of a new sibling species. Amphib–Reptil 17:7–31

    Google Scholar 

  • Holm S (1979) A simple sequential rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Hone DWE, Dyke GJ, Haden M, Benton MJ (2008) Body size evolution in Mesozoic birds. J Evol Biol 21:618–624

    Article  PubMed  CAS  Google Scholar 

  • Ivanović A, Vukov T, Džukic G, Tomašević N, Kalesić ML (2007) Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six Triturus species (Amphibia, Salamandridae). Zoomorphology 126:173–183

    Article  Google Scholar 

  • Klingenberg CP (1998) Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 73:79–123

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg CP (2010) Evolution and development of shape: integrating quantitative approaches. Nature 11:623–634

    CAS  Google Scholar 

  • Klingenberg CP (2011) MORPHOJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  • Klingenberg CP, McIntyre GS (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52:1363–1375

    Article  Google Scholar 

  • Klingenberg CP, Duttke S, Whelan S, Kim M (2011) Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves. J Evol Biol 25:115–129

    Article  PubMed  Google Scholar 

  • Larson PM (2002) Chondrocranial development in larval Rana sylvatica (Anura: Ranidae): a morphometric analysis of cranial allometry and ontogenetic shape change. J Morphol 252:131–144

    Article  PubMed  Google Scholar 

  • Larson PM (2004) Chondrocranial morphology and ontogenetic allometry in larval Bufo americanus (Anura, Bufonidae). Zoomorphology 123:95–106

    Article  Google Scholar 

  • Larson PM (2005) Ontogeny, phylogeny, and morphology in anuran larvae: morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae). J Morphol 264:34–52

    Article  PubMed  Google Scholar 

  • McNamara KJ (1986) A guide to the nomenclature of heterochrony. J Paleontol 60:4–13

    Google Scholar 

  • Mitteroecker P, Gunz P, Bookstein FL (2005) Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes. Evol Dev 7:244–258

    Article  PubMed  Google Scholar 

  • Ponssa ML (2008) Cladistic analysis and osteological descriptions of the species of the L. fuscus species group of the genus Leptodactylus (Anura, Leptodactylidae). J Zool Syst Evol Res 46:249–266

    Article  Google Scholar 

  • Ponssa ML, Jowers MJ, De Sá RO (2010) Osteology, natural history notes, and phylogenetic relationships of the poorly known Caribbean frog Leptodactylus nesiotus (Anura, Leptodactylidae). Zootaxa 2646:1–25

    Google Scholar 

  • Reilly SM, Wiley EO, Meinhardt DJ (1997) An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biol J Linn Soc 60:119–143

    Article  Google Scholar 

  • Rohlf J (2010a) TpsDig program version 1.49. Ecology and evolution, SUNY at Stony Brook

  • Rohlf J (2010b) TpsRelw program version 2.16. Ecology and evolution, SUNY at Stony Brook

  • Rohlf FJ, Bookstein FL (1990) Proceedings of the Michigan Morphometrics Workshop. Special publication no. 2. University of Michigan Museum of Zoology, Ann Arbor, MI

  • Shea BT (1983) Allometry and heterochrony in the African apes. Am J Phys Anthropol 62:275–289

    Article  PubMed  CAS  Google Scholar 

  • Shea BT (1985) Ontogenetic allometry and scaling: a discussion based on the growth and form of the skull in African apes. In: Jungers WL (ed) Size and scaling in primate biology. Plenum Press, New York, NY, pp 175–205

    Google Scholar 

  • Sheets H (2004) Morphometrics software: IMP-Integrated morphometrics package. http://www.canisius.edu/~sheets/morphsoft.html

  • Stanley SM (1973) An explanation for Cope’s Rule. Evolution 27:1–26

    Article  Google Scholar 

  • Viscosi V, Cardini A (2011) Leaf morphology, taxonomy and geometric morphometrics: a simplified protocol for beginners. PLoS One 6:1–19

    Article  Google Scholar 

  • Wake MH (1986) The morphology of Idiocranium russeli (Amphibia: Gymnophiona), with comments on miniaturization through heterochrony. J Morphol 189:1–16

    Article  Google Scholar 

  • Wassersug RJ (1976) A procedure for differential staining of cartilage and bone in hole formalin fixed vertebrates. Stain Technol 51:131–134

    PubMed  CAS  Google Scholar 

  • Webster M, Zelditch ML (2005) Evolutionary modifications of ontogeny: heterochrony and beyond. Paleobiology 31:354–372

    Article  Google Scholar 

  • Wilson LA, Sánchez-Villagra MR (2010) Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents. Proc R Soc B 277:1227–1234

    Article  PubMed  Google Scholar 

  • Yeh J (2002) The effect of miniaturized body size on skeletal morphology in frogs. Evolution 56:628–641

    PubMed  Google Scholar 

  • Zelditch ML, Sheets HD, Fink WL (2000) Spatio-temporal reorganization of growth rates in the evolution of ontogeny. Evolution 54:1363–1371

    PubMed  CAS  Google Scholar 

  • Zelditch ML, Sheets HD, Fink WL (2003) The ontogenetic dynamics of shape disparity. Paleobiology 29:139–156

    Article  Google Scholar 

  • Zelditch ML, Swiderski HD Sheets, Fink WL (2004) Geometric morphometrics for biologists: a primer. Elsevier Academic Press, New York, NY

    Google Scholar 

Download references

Acknowledgments

We are deeply indebted to Dr. M. Fabrezi, Dr. L. Trueb, Dr. W. R. Heyer, and anonymous reviewers for their help in improving earlier versions of our work. For loan of specimens employed in this study, we thank S. Kretzschmar and M. Cánepa (Fundación Miguel Lillo), W. R. Heyer (Smithsonian Institution), and H. Zaher (Museu de Zoologia Universidade de São Paulo). This research was supported by the following funds: PIP 112-200801-00225 and PIP 1112008010 402 2422 (CONICET), CIUNT-G430 (UNT), and PICT 2008 578 (FONCYT).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María Laura Ponssa.

Additional information

Communicated by T. Bartolomaeus.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 39 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ponssa, M.L., Candioti, M.F.V. Patterns of skull development in anurans: size and shape relationship during postmetamorphic cranial ontogeny in five species of the Leptodactylus fuscus Group (Anura: Leptodactylidae). Zoomorphology 131, 349–362 (2012). https://doi.org/10.1007/s00435-012-0164-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-012-0164-1

Keywords

Navigation