Skip to main content
SpringerLink
Log in

Heterogeneous Rates of Molecular Evolution Among Cryptic Species of the Ciliate Morphospecies Chilodonella uncinata

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

While molecular analyses have provided insight into the phylogeny of ciliates, the few studies assessing intraspecific variation have largely relied on just a single locus [e.g., nuclear small subunit rDNA (nSSU-rDNA) or mitochondrial cytochrome oxidase I]. In this study, we characterize the diversity of several nuclear protein-coding genes plus both nSSU-rDNA and mitochondrial small subunit rDNA (mtSSU-rDNA) of five isolates of the ciliate morphospecies Chilodonella uncinata. Although these isolates have nearly identical nSSU-rDNA sequences, they differ by up to 8.0% in mtSSU-rDNA. Comparative analyses of all loci, including β-tubulin paralogs, indicate a lack of recombination between strains, demonstrating that the morphospecies C. uncinata consists of multiple cryptic species. Further, there is considerable variation in substitution rates among loci as some protein-coding domains are nearly identical between isolates, while others differ by up to 13.2% at the amino acid level. Combining insights on macronuclear variation among isolates, the focus of this study, with published data from the micronucleus of two of these isolates, indicates that C. uncinata lineages are able to maintain both highly divergent and highly conserved genes within a rapidly evolving germline genome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andersson JO, Hirt RP, Foster PG, Roger AJ (2006) Evolution of four gene families with patchy phylogenetic distributions: influx of genes into protist genomes. Bmc Evol Biol 6:18

    Article  Google Scholar 

  • Barth D, Krenek S, Fokin SI, Berendonk TU (2006) Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. J Eukaryot Microbiol 53:20–25

    Article  PubMed  CAS  Google Scholar 

  • Barth D, Tischer K, Berger H, Schlegel M, Berendonk TU (2008) High mitochondrial haplotype diversity of Coleps sp. (Ciliophora: Prostomatida). Environ Microbiol 10:626–634

    Article  PubMed  CAS  Google Scholar 

  • Catania F, Wurmser F, Potekhin AA, Przybos E, Lynch M (2009) Genetic diversity in the Paramecium aurelia species complex. Mol Biol Evol 26:421–431

    Article  PubMed  CAS  Google Scholar 

  • Chantangsi C, Lynn DH, Brandl MT, Cole JC, Hetrick N, Ikonomi P (2007) Barcoding ciliates: a comprehensive study of 75 isolates of the genus Tetrahymena. Int J Syst Evol Microbiol 57:2412–2425

    Article  PubMed  CAS  Google Scholar 

  • Doherty M, Tamura M, Costas BA, Ritchie ME, McManus GB, Katz LA (2010) Ciliate diversity and distribution across an environmental and depth gradient in Long Island Sound, USA. Environ Microbiol 12:886–898

    Article  PubMed  CAS  Google Scholar 

  • Dunthorn M, Foissner W, Katz LA (2011) Expanding character sampling for ciliate phylogenetic inference using mitochondrial SSU-rDNA as a molecular marker. Protist 162:85–99

    Article  PubMed  CAS  Google Scholar 

  • Gentekaki E, Lynn DH (2009) High-level genetic diversity but no population structure inferred from nuclear and mitochondrial markers of the peritrichous ciliate Carchesium polypinum in the Grand River Basin (North America). Appl Environ Microbiol 75:3187–3195

    Article  PubMed  CAS  Google Scholar 

  • Ginger ML, Fritz-Laylin LK, Fulton C, Cande WZ, Dawson SC (2010) Intermediary metabolism in protists: a sequence-based view of facultative anaerobic metabolism in evolutionarily diverse eukaryotes. Protist 161:642–671

    Article  PubMed  CAS  Google Scholar 

  • Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Herrick G (1994) Germline-soma relationships in ciliates protozoa: the inception and evolution of nuclear dimorphism in one-celled animals. Semin Dev Biol 5:3–12

    Article  Google Scholar 

  • Israel RL, Kosakovsky Pond SL, Muse SV, Katz LA (2002) Evolution of duplicated alpha-tubulin genes in ciliates. Evolution 56:1110–1122

    PubMed  CAS  Google Scholar 

  • Juranek SA, Lipps HJ (2007) New insights into the macronuclear development in ciliates. Int Rev Cytol 262:219–251

    Article  PubMed  CAS  Google Scholar 

  • Katz LA, Kovner AM (2010) Alternative processing of scrambled genes generates protein diversity in the ciliate Chilodonella uncinata. J Exp Zool B 314:480–488

    Article  Google Scholar 

  • Katz LA, Bornstein J, Lasek-Nesselquist E, Muse SV (2004) Dramatic diversity of ciliate histone H4 genes revealed by comparisons of patterns of substitutions and paralog divergences among eukaryotes. Mol Biol Evol 21:555–562

    Article  PubMed  CAS  Google Scholar 

  • Katz La, McManus GB, Snoeyenbos-West OLO, Griffin A, Pirog K, Costas B, Foissner W (2005) Reframing the ‘Everything is everywhere’ debate: evidence for high gene flow and diversity in ciliate morphospecies. Aquat Microb Ecol 41:55–65

    Article  Google Scholar 

  • Kloc M, Zagrodzinska B (2001) Chromatin elimination–an oddity or a common mechanism in differentiation and development? Differentiation 68:84–91

    Article  PubMed  CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  Google Scholar 

  • Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098

    Article  PubMed  Google Scholar 

  • Lynch M (2007) Origins of genome architecture. Sinauer Associates, Sunderland

    Google Scholar 

  • Maddison WP, Maddison DR (2005) MacClade v. 4.0.8. Sinauer Assoc, Sunderland

    Google Scholar 

  • McGrath C, Zufall RA, Katz LA (2006) Genome evolution in ciliates. In: Katz LA, Bhattacharya D (eds) Genomics and evolution of eukaryotic microbes. Oxford University Press, New york

    Google Scholar 

  • Muse SV, Gaut BS (1994) A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates with application to the chloroplast genome. Mol Biol Evol 11:715–724

    PubMed  CAS  Google Scholar 

  • Nanney DL (1999) When is a rose?: the kinds of Tetrahymena. In: Wilson RA (ed) Species: new interdisciplinary essays. The MIT Press, Cambridge, pp 93–118

    Google Scholar 

  • Nanney DL, Park C, Preparata R, Simon EM (1998) Comparison of sequence differences in a variable 23S rRNA domain among sets of cryptic species of ciliated protozoa. J Euk Microbiol 45:91–100

    Article  PubMed  CAS  Google Scholar 

  • Peden J (2005) CodonW version 1.4.2. http://codonw.sourceforge.net/culong.html#License

  • Riley JL, Katz LA (2001) Widespread distribution of extensive genome fragmentation in ciliates. Mol Biol Evol 18:1372–1377

    Article  PubMed  CAS  Google Scholar 

  • Robinson T, Katz LA (2008) Non-Mendelian inheritance of two cytoskeletal genes in the ciliate Chilodonella uncinata. Mol Biol Evol 24:2495–2503

    Article  Google Scholar 

  • Simon EM, Nanney DL, Doerder FP (2008) The “Tetrahymena pyformis” complex of cryptic species. Biodiv Conserv 17:365–380

    Article  Google Scholar 

  • Snoke MS, Berendonk TU, Barth D, Lynch M (2006) Large global effective population sizes in Paramecium. Mol Biol Evol 23:2474–2479

    Article  PubMed  CAS  Google Scholar 

  • Sonneborn TM (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proc Natl Acad Sci USA 23:378–383

    Article  PubMed  CAS  Google Scholar 

  • Sonneborn TM (1957) Breeding systems, reproductive methods, and species problems in protozoa. In: Mayr E (ed) The species problem. American Association for the Advancement of Science, Washington DC, pp 155–324

    Google Scholar 

  • Strüder-Kypke MC, Lynn DH (2010) Comparative analysis of the mitochondrial cytochrome c oxidase subunit 1 (CO1) gene in ciliates (Alveolata, Ciliophora) and evaluation of its suitability as a biodiversity marker. Syst Biodivers 8:131–148

    Article  Google Scholar 

  • Weisse T, Lettner S (2002) The ecological significance of intraspecific variation among freshwater ciliates. Verh Intern Verein Limnol 28:1880–1884

    Google Scholar 

  • Weisse T, Strüder-Kypke MC, Berger H, Foissner W (2008) Genetic, morphological, and ecological diversity of spatially separated clones of Meseres corlissi Petz & Foissner, 1992 (Ciliophora, Spirotrichea). J Eukaryot Microbiol 55:257–270

    Article  PubMed  CAS  Google Scholar 

  • Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87:23–29

    Article  PubMed  CAS  Google Scholar 

  • Zmasek CM, Godzik A (2011) Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires. Genome Biol 12:13

    Article  Google Scholar 

  • Zufall RA, Katz LA (2007) Micronuclear and macronuclear forms of beta-tubulin genes in the ciliate Chilodonella uncinata reveal insights into genome processing and protein evolution. J Eukaryot Microbiol 54:275–282

    Article  PubMed  CAS  Google Scholar 

  • Zufall RA, Robinson T, Katz LA (2005) Evolution of developmentally regulated genome rearrangements in eukaryotes. J Exp Zool Part B-Mol Dev Evol 304B:448–455

    Article  CAS  Google Scholar 

  • Zufall RA, McGrath C, Muse SV, Katz LA (2006) Genome architecture drives protein evolution in ciliates. Mol Biol Evol 23:1681–1687

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by two grants to L.A.K.: NSF DEB award (DEB 0816828) and an NIH AREA award 1R15GM081865-01.

Author information

Author notes

  1. Micah Dunthorn

    Present address: Department of Ecology, Technische Universität Kaiserslautern, 67653, Kaiserslautern, Germany

Authors and Affiliations

  1. Department of Biological Sciences, Smith College, Northampton, MA, 01063, USA

    Laura A. Katz, Jennifer DeBerardinis, Meaghan S. Hall & Alexandra M. Kovner

  2. Program in Organismic and Evolutionary Biology, UMass-Amherst, Amherst, MA, 01003, USA

    Laura A. Katz & Micah Dunthorn

  3. Department of Statistics, North Carolina State University, Raleigh, NC, 27695-7566, USA

    Spencer V. Muse

Authors
  1. Laura A. Katz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer DeBerardinis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meaghan S. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandra M. Kovner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Micah Dunthorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Spencer V. Muse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura A. Katz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Katz, L.A., DeBerardinis, J., Hall, M.S. et al. Heterogeneous Rates of Molecular Evolution Among Cryptic Species of the Ciliate Morphospecies Chilodonella uncinata . J Mol Evol 73, 266–272 (2011). https://doi.org/10.1007/s00239-011-9468-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-011-9468-x

Keywords

Search

Navigation