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Musculoskeletal development of the Central African caecilian Idiocranium russeli (Amphibia: Gymnophiona: Indotyphlidae) and its bearing on the re-evolution of larvae in caecilian amphibians

  • Tobias Theska
  • Mark Wilkinson
  • David J. Gower
  • Hendrik Müller
Original paper

Abstract

Few detailed accounts of the developmental morphology of caecilian amphibians exist and recent studies have highlighted problems concerning the homology of some skull elements. We investigated the embryonic and post-hatching development of the skeleton and musculature of Idiocranium russeli, a possibly miniaturized caecilian endemic to Cameroon. Idiocranium has been suggested to be direct developing; our results strongly support this hypothesis. The external morphology of different embryonic stages, the ossification sequence, and the configuration of the cranial muscles of I. russeli indicate heterochronic shifts of adult traits into embryonic development, as well as the loss or absence of various larval and metamorphic traits. For example, the tentacle, which plesiomorphically develops during metamorphosis, is already fully developed in late embryos. The maxilla and the palatine, which fuse to form the maxillopalatine (during metamorphosis in most biphasic species), fuse well before hatching. Muscles exclusive to the larva, such as the m. interhyoideus and m. hyomandibularis, are absent during development, whereas adult muscles including the m. genioglossus and m. cephalodorsosubpharyngeus, form during embryonic development. A larval ceratobranchial IV is present and fuses to the ceratobranchial III very early in ontogeny. In its near complete absence of larval traits during development, I. russeli resembles the Indian indotyphlid Gegeneophis ramaswamii; this similarity complicates a straightforward explanation for the re-evolution of free-living larvae in Seychelles indotyphlid caecilians.

Keywords

Morphology Ontogeny Larval re-evolution Life history Ossification sequence 

Notes

Acknowledgements

We thank Katja Felbel for the expert preparation of histological sections and Paul Lukas for advice regarding three-dimensional reconstructions using Amira and Autodesk Maya. The fieldwork for collection of Idiocranium was funded primarily by the US Fish and Wildlife’s Wildlife Without Borders, along with several other programs—viz., Amphibians in Decline, Zoological Society of London’s EDGE Fellowship, Conservation International’s Lost Amphibians, and The Royal Geographical Society—all of which we gratefully acknowledge. This research was funded by a German Research Foundation grant (DFG MU2914/2-1) to HM. DJG and MW are indebted to many Cameroonian people of Mamfe Division who helped us with logistics and generously provided field assistance and hospitality. We thank the people of the villages of Tinta, particularly Tata Eric Tunda, Wilfred, and Rafael (Tinta). We also thank Echalle S. Ndeme and Gespo for looking after us in the field, and Tom Doherty-Bone, Nono Gonwouo, Ngane Benjamin Kome, and Marcel Kouete for their help and support. This manuscript was improved by comments from an anonymous reviewer, which is gratefully acknowledged.

Compliance with ethical standards

Ethical approval

All applicable international, national, and institutional guidelines for the collection and use of animals were followed.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institut für Zoologie und EvolutionsforschungFriedrich-Schiller-Universität JenaJenaGermany
  2. 2.Department of Life SciencesThe Natural History MuseumLondonUK

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