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Direct development in African squeaker frogs (Anura: Arthroleptidae: Arthroleptis) reveals a mosaic of derived and plesiomorphic characters

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Abstract

Direct development has evolved independently several times in anurans and direct-developing species are characterized by large-scale developmental repatterning and a complete, or near complete, absence of most tadpole-specific structures. Earlier studies stressed the similarities among different direct-developing species, but more recent studies have indicated differences in the reduction of tadpole-specific structures among different taxa. Here, we describe egg deposition, clutch characteristics and embryonic development of the direct-developing squeaker frogs of the genus Arthroleptis, providing the first detailed description of direct development in Arthroleptidae. Embryonic development in Arthroleptis is characterized by the presence of an opercular fold that still encloses the developing forelimbs, the absence of external gills and an only moderately extended tail. A comparison with published information on other direct-developing anurans reveals broad dissimilarities in the formation of an opercular fold and very different tail morphology among different taxa. An egg tooth, often considered characteristic of direct-developing anurans, seems to be restricted to New World Terrarana. The embryonic diversity seen in direct-developing anuran taxa argues against simplistic assumptions about the evolution of direct development.

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Acknowledgements

We thank Unilever Tea Tanzania, particularly Andrew Mitei, Amiri Kivambe, Sylvia Rutatina, and Charles Kumbemba, for permission to work on the estate and for providing invaluable help with logistics and accommodation. For help in the field, we are indebted to E. Mulungu. Permits to collect and export A. xenodactyloides were issued by the Tanzania Wildlife Research Institute (TAWIRI), the Tanzanian Commission of Science and Technology (COSTECH Permit No. 2009-306-NA-2009-201) and the Wildlife Division of the Tanzanian Ministry of Tourism and Natural Resources. We particularly thank Drs. V. Kakengi, J. Keyyu and K. Oola (TAWIRI) and M. Munshi (COSTECH) for their help and support. For help with logistics, we thank D. Moyer, K. Howell and D. Nkini (Tanzania Conservation Resource Centre). Permits to collect and export A. wahlbergii were issued by Ezemvelo KZN Wildlife (OP4507/2015). We especially thank Adrian Armstrong, Sharon Louw and James Harvey for facilitating fieldwork in KZN and Jane Chennells for permission to work on her property. We thank Lennart Olsson for commenting on an earlier version of the manuscript. Funding was provided through a Putnam Expedition Grant of the Museum of Comparative Zoology and a German Research Foundation grant (DFG MU2914/2-1) to HM and a Museum of Comparative Zoology Grant-in-Aid for Undergraduate Research and the Harvard College Research Program to JGL. Support by a Volkswagen Postdoctoral Fellowship in Evolutionary Biology to HM is gratefully acknowledged. Two anonymous reviewers provided valuable and insightful comments that helped to improve this manuscript.

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  1. Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich Schiller Universität Jena, Erbertstrasse 1, 07743, Jena, Germany

    Susan Schweiger, Benjamin Naumann, Lars Möckel & Hendrik Müller

  2. Museum of Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA

    Joanna G. Larson & Hendrik Müller

  3. Department of Ecology and Evolutionary Biology and Museum of Zoology, University of Michigan, Ann Arbor, MI, 48109, USA

    Joanna G. Larson

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  1. Susan Schweiger
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Correspondence to Hendrik Müller.

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Schweiger, S., Naumann, B., Larson, J.G. et al. Direct development in African squeaker frogs (Anura: Arthroleptidae: Arthroleptis) reveals a mosaic of derived and plesiomorphic characters. Org Divers Evol 17, 693–707 (2017). https://doi.org/10.1007/s13127-017-0335-5

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