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

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Andrássy I (2005) Free-living nematodes of Hungary (Nematoda errantia), 1st edn. Pedozoologica Hungarica, Hungarian Natural History Museum, Budapest

    Google Scholar 

  2. Bowerman B, Eaton BA, Priess JR (1992) skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68:1061–1075

    Article  CAS  PubMed  Google Scholar 

  3. Bowerman B, Draper BW, Mello CC, Priess JR (1993) The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos. Cell 74:443–452

    Article  CAS  PubMed  Google Scholar 

  4. Broitman-Maduro G, Maduro MF (2011) In situ hybridization of embryos with antisense RNA probes. Meth Cell Biol 106:253–270

    Article  CAS  Google Scholar 

  5. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165

    Article  CAS  PubMed  Google Scholar 

  6. Holterman M, van der Wurff A, van den Elsen S, van Megen H, Bongers T, Holovachov O, Bakker J, Helder J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol 23:1792–1800

    Article  CAS  PubMed  Google Scholar 

  7. Laugsch M, Schierenberg E (2004) Differences in maternal supply and early development of closely related nematode species. Int J Dev Biol 48:655–662

  8. Lewis S, Dyal L, Hilburn C, Weitz S, Liau W, LaMunyon C, Denver D (2009) Molecular evolution in Panagrolaimus nematodes: origins of parthenogenesis, hermaphroditism and the Antarctic species P. davidi. BMC Evol Biol 9:15

    Article  PubMed Central  PubMed  Google Scholar 

  9. Lin KT-H, Broitman-Maduro G, Hung WWK, Cervantes S, Maduro MF (2009) Knockdown of SKN-1 and the Wnt effector TCF/POP-1 reveals differences in endomesoderm specification in C. briggsae as compared with C. elegans. Dev Biol 325:296–306

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Maduro MF (2006) Endomesoderm specification in Caenorhabditis elegans and other nematodes. BioEssays 28:1010–1022

    Article  CAS  PubMed  Google Scholar 

  11. Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061–1067

    Article  CAS  PubMed  Google Scholar 

  12. Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  13. Schiffer PH, Kroiher M, Kraus C, Koutsovoulos GD, Kumar S, Camps JIR, Nsah NA, Stappert D, Morris K, Heger P, Altmüller J, Frommolt P, Nürnberg P, Thomas WK, Blaxter ML, Schierenberg E (2013) The genome of Romanomermis culicivorax: revealing fundamental changes in the core developmental genetic toolkit in Nematoda. BMC Genomics 14:923

    Article  PubMed Central  PubMed  Google Scholar 

  14. Schulze J, Schierenberg E (2011) Evolution of embryonic development in nematodes. EvoDevo 2:18

    Article  PubMed Central  PubMed  Google Scholar 

  15. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Ding JSO, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:1–6

    Google Scholar 

  16. Sommer RJ, Bumbarger DJ (2012) Nematode model systems in evolution and development. Wiley Interdiscip Rev Dev Biol 1:389–400

    Article  CAS  PubMed  Google Scholar 

  17. Stamatakis AV (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  18. True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3:109–119

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

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
figure4

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)

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)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

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