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Developmental variations among Panagrolaimid nematodes indicate developmental system drift within a small taxonomic unit

Development Genes and Evolution volume 224, pages 183–188 (2014)Cite this article

Abstract

Comparative studies of nematode embryogenesis among different clades revealed considerable variations. However, to what extent developmental differences exist between closely related species has mostly remained nebulous. Here, we explore the correlation between phylogenetic neighborhood and developmental variation in a restricted and morphologically particularly uniform taxonomic group (Panagrolaimidae) to determine to what extent (1) morphological and developmental characters go along with molecular data and thus can serve as diagnostic tools for the definition of kinship and (2) developmental system drift (DSD; modifications of developmental patterns without corresponding morphological changes) can be found within a small taxonomic unit. Our molecular approaches firmly support subdivision of Panagrolaimid nematodes into two monophyletic groups. These can be discriminated by distinct peculiarities in early embryonic cell lineages and a mirror-image expression pattern of the gene skn-1. This suggests major changes in the logic of cell specification and the action of DSD in the studied representatives of the two neighboring nematode taxa.

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Acknowledgments

P.H.S. was funded by a personal grant of the Volkswagen Foundation in the framework of the Initiative for Evolutionary Biology and by the German Research Foundation (DFG) through the grant SFB680 to T. Wiehe, Institute for Genetics, University of Cologne.

C. L. was funded through a Fletcher Jones endowment and a USD International Opportunity Grant. The authors are grateful to Walter Traunspurger for sharing the Propanagrolaimus strain WTM1. C.L. thanks Terry Bird, Keith MacDonald, and the Biology 342 Microbiology lab students (USD) that first found LC91 in Winogradsky columns made from the San Diego River mud.

Competing interests

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Zoological Institute, Cologne Biocenter, University of Cologne, Cologne, Germany

    Philipp H. Schiffer, Ndifon A. Nsah, Henny Grotehusmann, Michael Kroiher & Einhard Schierenberg

  2. Institute for Genetics, Cologne Biocenter, University of Cologne, Cologne, Germany

    Philipp H. Schiffer

  3. Department of Biology, University of San Diego, San Diego, CA, USA

    Curtis Loer

Authors
  1. Philipp H. Schiffer
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  2. Ndifon A. Nsah
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  3. Henny Grotehusmann
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  4. Michael Kroiher
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  5. Curtis Loer
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  6. Einhard Schierenberg
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Corresponding author

Correspondence to Philipp H. Schiffer.

Additional information

ORCiD: 0000-0001-6776-0934

Communicated by: Volker G. Hartenstein

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 2
figure 4

A, protein alignment of C. elegans skn-1 with the predicted Panagrolaimus and Propanagrolaimus skn-1 sequences. For reference, the Pristionchus pacificus skn-1 retrieved from Wormbase is included. In both Panagrolaimid species the DIDLID and the DNA binding domains are conserved, the latter one stronger than the former. For details, see text. B, results of tblast of the PS1159 SKN-1 prediction against the NCBI protein database. Best scoring hits are obtained for SKN-1 in several Caenorhabditis species, while the C. elegans SNKR-1 co-orthologue receives a significantly lower scoring hit. (JPEG 793 KB)

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Supplementary Fig. 1

A, General habitus of the analysed Panagrolaimid species in comparison to C. elegans. Panagrolaimids possess a generally uniform morphology with obvious differences in tail shape and body length. From top to bottom: Panagrolaimus sp. ES5, male; Panagrolaimus sp. ES5, female; Propanagrolaimus sp. JU765, hermaphrodite; Propanagrolaimus sp. LC91, hermaphrodite; C elegans, male: C. elegans, young hermaphrodite. LC91 is ovoviviparous and juveniles hatch inside the mother. B, vulva lips are more protruding in Panagrolaimus (top, right) than in Propanagrolaimus (bottom, right). (PDF 3,747 kb)

Supplementary Table 1

Names and NCBI database IDs for 7 KOG proteins predicted from RNAseq data using the CEGMA pipeline that were included in the phylogenetic inferences. (DOCX 23 kb)

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Schiffer, P.H., Nsah, N.A., Grotehusmann, H. et al. Developmental variations among Panagrolaimid nematodes indicate developmental system drift within a small taxonomic unit. Dev Genes Evol 224, 183–188 (2014). https://doi.org/10.1007/s00427-014-0471-2

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  • DOI: https://doi.org/10.1007/s00427-014-0471-2

Keywords

  • Nematoda
  • Molecular phylogeny
  • Cell lineage
  • In situ hybridization
  • skn-1
  • Developmental system drift