Evolution of terrestrial development in anurans

• Applicant: Privatdozent Dr. Hendrik Müller
• Subject Area: Systematics and Morphology (Zoology) ; Evolution, Anthropology
• Term: from 2013 to 2017
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 240585867

• Final Report Year: 2019

Final Report Abstract

Direct development is a highly derived form of reproduction in which the aquatic larva (tadpole) is complete absent and a fully formed hatchling emerges directly from the egg. At the same time, development is highly modified in that a tadpolelike stage is not simply internalized in the egg but instead embryonic development is greatly remodelled and most adult features form early during embryonic development. Direct development evolved several times independently in frogs, salamanders and caecilians, but comparatively little is known about its evolution and developmental consequences in general. Data for the terraranan directdeveloping Eleutherodactylus coqui indicate a very comprehensive loss of larvaspecific characters during development and also point to some special adaptations (e.g. egg tooth, greatly enlarged tailfins presumed to act in gas exchange). These were seen as characteristic for direct-developing anurans and especially the largescale loss of larval characters led to the hypothesis that the tadpole larva represents a developmental module that gets simple deleted in the ontogeny of direct-developing anurans. However, more limited data on other, non-terraranan direct-developing anurans indicated that not all taxa show similar reductions of larval characters as E. coqui. We investigated development in the direct-developing Arthroleptis wahlbergii, which also shows a large-scale loss of larval characters. However, the pattern of larval character loss is not identical to E. coqui and a review of the available literature shows that many of the characters previously thought to characterize direct development in anurans are either not present in all direct-developing taxa or special adaptations of some taxa. We also investigated development in the terrestrial developing Arthroleptella villiers, which has non-feeding, terrestrial tadpoles. Although far more tadpole-like in external appearance, A. villiersi also shows high degree of loss of larval characters and is more similar to directdeveloping taxa in its musculoskeletal development than to taxa with free-living tadpoles. Take together, these data strongly indicate that the anuran tadpole does not represent a developmental module that can simply be deleted from development and thus lead to direct development. Instead, the evolution of direct development led to a taxon-specific pattern of the reduction of larval characters. The development of A. villiersi is also surprisingly similar to direct-developing taxa and terrestrial development with a non-feeding tadpole appears to be (at least conceptionally) a plausible intermediate condition in the evolution of direct development. We also investigated closely related larval developers and could show that some of the characters missing in A. wahlbergii are also absent in its closest larval-developing relatives, which clearly indicates that their loss in A. wahlbergii is a result of phylogeny and not direct development. This highlights the need for a comprehensive analysis of novel developmental reproductive strategies within a meaningful comparative framework.

Publications

• (2019) Description of the Tadpole of the Critically Endangered Ethiopian Toad Altiphrynoides osgoodi (Amphibia: Anura: Bufonidae). Journal of Herpetology 53 (3) 218
  Müller, Hendrik
  
• (2015) Die Evolution der terrestrischen Entwicklung bei Anuren. TERRARIA/elaphe 4/2015: 95–97
  Schweiger, S. & Müller, H.
  
• (2017) Direct development in African squeaker frogs (Anura: Arthroleptidae: Arthroleptis) reveals a mosaic of derived and plesiomorphic characters. Organisms, Diversity and Evolution 17:693–707
  Schweiger, S., Naumann, B., Larson, J. G., Möckel, L. & Müller, H.
  
• (2017) Meristic and morphometric characters of Leptopelis natalensis tadpoles (Amphibia: Anura: Arthroleptidae) from Entumeni Forest reveal variation and inconsistencies with previous descriptions. Acta Herpetologica 12:125–132
  Schweiger, S., Harvey, J., Otremba, T., Weber, J. & Müller, H.
  
• (2017) Terrestrial Reproduction as an Adaptation to Steep Terrain in African Toads. Proceedings of the Royal Society, Series B 284: 20162598
  Liedtke, H. C., Müller, H., Hafner, J., Penner, J., Gower, D. J., Mazuch, T., Rödel, M.-O. & Loader, S. P.
  
• (2019) Development, Morphology and the Evolution of Terrestrial Reproductive Strategies in Amphibians. Friedrich-Schiller-Universität Jena
  Müller, H.
  
• (2019) Musculoskeletal development of the Central African caecilian Idiocranium russeli (Lissamphibia: Gymnophiona: Indotyphlidae) and its bearing on the reevolution of larvae in caecilian amphibians. Zoomorphology 138:137–158
  Theska, T., Wilkinson, M., Gower, D. J. & Müller, H.