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Open Access Highly Accessed Research article

Timing of organogenesis support basal position of turtles in the amniote tree of life

Ingmar Werneburg* and Marcelo R Sánchez-Villagra

Author Affiliations

Paläontologisches Institut und Museum der Universität Zürich, Karl Schmid-Strasse 4, 8006 Zürich, Switzerland

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BMC Evolutionary Biology 2009, 9:82  doi:10.1186/1471-2148-9-82

Published: 23 April 2009

Abstract

Background

The phylogenetic position of turtles is the most disputed aspect in the reconstruction of the land vertebrate tree of life. This controversy has arisen after many different kinds and revisions of investigations of molecular and morphological data. Three main hypotheses of living sister-groups of turtles have resulted from them: all reptiles, crocodiles + birds or squamates + tuatara. Although embryology has played a major role in morphological studies of vertebrate phylogeny, data on developmental timing have never been examined to explore and test the alternative phylogenetic hypotheses. We conducted a comprehensive study of published and new embryological data comprising 15 turtle and eight tetrapod species belonging to other taxa, integrating for the first time data on the side-necked turtle clade.

Results

The timing of events in organogenesis of diverse character complexes in all body regions is not uniform across amniotes and can be analysed using a parsimony-based method. Changes in the relative timing of particular events diagnose many clades of amniotes and include a phylogenetic signal. A basal position of turtles to the living saurian clades is clearly supported by timing of organogenesis data.

Conclusion

The clear signal of a basal position of turtles provided by heterochronic data implies significant convergence in either molecular, adult morphological or developmental timing characters, as only one of the alternative solutions to the phylogenetic conundrum can be right. The development of a standard reference series of embryological events in amniotes as presented here should enable future improvements and expansion of sampling and thus the examination of other hypotheses about phylogeny and patterns of the evolution of land vertebrate development.