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Development Genes and Evolution

, Volume 224, Issue 3, pp 183–188 | Cite as

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

  • Philipp H. SchifferEmail author
  • Ndifon A. Nsah
  • Henny Grotehusmann
  • Michael Kroiher
  • Curtis Loer
  • Einhard Schierenberg
Short Communication

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.

Keywords

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

Notes

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.

Supplementary material

427_2014_471_MOESM1_ESM.pdf (3.7 mb)
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)
427_2014_471_Fig4_ESM.jpg (793 kb)
Supplementary Fig. 2

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)

427_2014_471_MOESM2_ESM.docx (62 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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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Philipp H. Schiffer
    • 1
    • 2
    Email author
  • Ndifon A. Nsah
    • 1
  • Henny Grotehusmann
    • 1
  • Michael Kroiher
    • 1
  • Curtis Loer
    • 3
  • Einhard Schierenberg
    • 1
  1. 1.Zoological Institute, Cologne BiocenterUniversity of CologneCologneGermany
  2. 2.Institute for Genetics, Cologne BiocenterUniversity of CologneCologneGermany
  3. 3.Department of BiologyUniversity of San DiegoSan DiegoUSA

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