Hydrobiologia

, Volume 687, Issue 1, pp 101–106 | Cite as

First evaluation of mitochondrial DNA as a marker for phylogeographic studies of Calcarea: a case study from Leucetta chagosensis

SPONGE RESEARCH DEVELOPMENTS Short Research Note

Abstract

In most animals mitochondrial DNA (mtDNA) evolves much faster than nuclear DNA. Therefore, and because of its shorter coalescent time, mitochondrial (mt) markers provide better resolution to trace more recent evolutionary events compared to nuclear DNA. But in contrast to most other Metazoa, previous studies suggested that in sponges mitochondrial sequence evolution is much slower, making mtDNA less suitable for studies at the intraspecific level. However, these observations were made in the class Demospongiae and so far no data exist for calcareous sponges (Class Calcarea). We here provide the first study that evaluates intraspecific mt sequence variation in Calcarea. We focus on arguably the best-studied species Leucetta chagosensis, for which three nuclear DNA marker datasets existed previously. We here sequenced the partial mitochondrial cytochrome oxidase subunit III gene (cox3). Our analyses reveal an unexpected variability of up to 8.5% in this mitochondrial marker. In contrast to other sponges where this marker evolves considerable slower than the nuclear internal transcribed spacer region (ITS), we found that cox3 in L. chagosensis evolves about five times as fast as ITS. The variability is similar to that of nuclear intron data of the species. The phylogeny inferred with cox3 is congruent with other markers, but separates earlier reported genetic groups much more distinctively than nuclear DNA. This provides further evidence for cryptic speciation in L. chagosensis. All these features make calcarean mtDNA exceptional among sponges and show its suitability for phylogeographic studies and potential as a species-specific (DNA barcoding) marker to distinguish morphologically identical cryptic species.

Keywords

Leucetta chagosensis Calcarea Mitochondrial DNA Cytochrome oxidase subunit III Phylogeography DNA barcoding 

Supplementary material

10750_2011_800_MOESM1_ESM.pdf (114 kb)
Supplementary material (PDF 115 kb)

References

  1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller & D. J. Lipman, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389–3402.PubMedCrossRefGoogle Scholar
  2. Avise, J. C., J. Arnold, R. M. Ball, E. Bermingham, T. Lamb, J. E. Neigel, C. A. Reeb & N. C. Saunders, 1987. Intraspecific phylogeography—the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18: 489–522.Google Scholar
  3. Bentlage, B. & G. Wörheide, 2007. Low genetic structuring among Pericharax heteroraphis (Porifera: Calcarea) populations from the Great Barrier Reef (Australia), revealed by analysis of nrDNA and nuclear intron sequences. Coral Reefs 26: 807–816.CrossRefGoogle Scholar
  4. Birky, C. Jr., T. Maruyama & P. Fuerst, 1983. An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103: 513–527.PubMedGoogle Scholar
  5. Dohrmann, M., O. Voigt, D. Erpenbeck & G. Wörheide, 2006. Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA. Molecular Phylogenetics and Evolution 40: 830–843.PubMedCrossRefGoogle Scholar
  6. Duran, S., M. Pascual & X. Turon, 2004. Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida). Marine Biology 144: 31–35.CrossRefGoogle Scholar
  7. Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.PubMedGoogle Scholar
  8. Gouy, M., S. Guindon & O. Gascuel, 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27: 221–224.PubMedCrossRefGoogle Scholar
  9. Guindon, S. & O. Gascuel, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.PubMedCrossRefGoogle Scholar
  10. Huang, D., R. Meier, P. A. Todd & L. M. Chou, 2008. Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution 66: 167–174.PubMedCrossRefGoogle Scholar
  11. Lavrov, D. V., L. Forget, M. Kelly & B. F. Lang, 2005. Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution. Molecular Biology and Evolution 22: 1231–1239.PubMedCrossRefGoogle Scholar
  12. Meyer, C. P. & G. Paulay, 2005. DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3: 2229–2238.Google Scholar
  13. Nylander, J. A., J. C. Wilgenbusch, D. L. Warren & D. L. Swofford, 2008. AWTY (Are We There Yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24: 581–583.PubMedCrossRefGoogle Scholar
  14. Park, M. H., C. J. Sim, J. Baek & G. S. Min, 2007. Identification of genes suitable for DNA barcoding of morphologically indistinguishable Korean Halichondriidae sponges. Molecules and Cells 23: 220–227.PubMedGoogle Scholar
  15. Philippe, H., R. Derelle, P. Lopez, K. Pick, C. Borchiellini, N. Boury-Esnault, J. Vacelet, E. Renard, E. Houliston, E. Quéinnec, C. Da Silva, P. Wincker, H. Le Guyade, S. Leys, D. J. Jackson, F. Schreiber, D. Erpenbeck, B. Morgenstern, G. Wörheide & M. Manuel, 2009. Phylogenomics revives traditional views on deep animal relationships. Current Biology 19: 706–712.PubMedCrossRefGoogle Scholar
  16. Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.PubMedCrossRefGoogle Scholar
  17. R Development Core Team, 2001. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria [available on internet at http://www.R-project.org].
  18. Ronquist, F. & J. P. Huelsenbeck, 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.PubMedCrossRefGoogle Scholar
  19. Rua, C., C. Zilberberg & A. Solé-Cava., 2011. New polymorphic mitochondrial markers for sponge phylogeography. Journal of the Marine Biological Association of the UK. doi:10.1017/S0025315410002122.
  20. Shearer, T. L., M. J. H. Van Oppen, S. L. Romano & G. Wörheide, 2002. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11: 2475–2487.PubMedCrossRefGoogle Scholar
  21. Swofford, D. L., 2003. PAUP*. Phylogenetic Analysis Using Parsimony (and Other Methods). Version 4. Sinauer Associates, Sunderland.Google Scholar
  22. Wang, X. & D. V. Lavrov, 2008. Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS ONE 3: e2723.PubMedCrossRefGoogle Scholar
  23. Wörheide, G., 2006. Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific. Marine Biology 148: 907–912.CrossRefGoogle Scholar
  24. Wörheide, G., J. N. A. Hooper & B. M. Degnan, 2002. Phylogeography of western Pacific Leucetta ‘chagosensis’ (Porifera : Calcarea) from ribosomal DNA sequences: implications for population history and conservation of the Great Barrier Reef World Heritage Area (Australia). Molecular Ecology 11: 1753–1768.PubMedCrossRefGoogle Scholar
  25. Wörheide, G., D. Erpenbeck & C. Menke, 2007. The Sponge Barcoding Project: aiding in the identification and description of poriferan taxa. In Custódio, M. R. & E. Hajdu (eds), Porifera Research: Biodiversity, Innovation & Sustainability. Museu Nacional Serie Livros, Rio de Janerio: 123–128.Google Scholar
  26. Wörheide, G., L. S. Epp & L. Macis, 2008. Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both? BMC Evolutionary Biology 8: 24.PubMedCrossRefGoogle Scholar
  27. Zink, R. M. & G. F. Barrowclough, 2008. Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology 17: 2107–2121.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Oliver Voigt
    • 1
  • Vincent Eichmann
    • 1
  • Gert Wörheide
    • 1
    • 2
  1. 1.Department of Earth and Environmental Sciences & GeoBio-CenterLMULudwig-Maximilians-University MunichMunichGermany
  2. 2.Bayerische Staatssammlung für Paläontologie und GeologieMunichGermany

Personalised recommendations