University of Massachusetts - Amherst
ScholarWorks@UMass Amherst Dissertations
Dissertations and Theses
9-1-2009
Ciliate Biodiversity and Phylogenetic Reconstruction Assessed by Multiple Molecular Markers Micah Dunthorn University of Massachusetts - Amherst,
[email protected]
Follow this and additional works at: http://scholarworks.umass.edu/open_access_dissertations Recommended Citation Dunthorn, Micah, "Ciliate Biodiversity and Phylogenetic Reconstruction Assessed by Multiple Molecular Markers" (2009). Dissertations. Paper 95.
This Open Access Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks@UMass Amherst. It has been accepted for inclusion in Dissertations by an authorized administrator of ScholarWorks@UMass Amherst. For more information, please contact
[email protected].
CILIATE BIODIVERSITY AND PHYLOGENETIC RECONSTRUCTION ASSESSED BY MULTIPLE MOLECULAR MARKERS
A Dissertation Presented by MICAH DUNTHORN
Submitted to the Graduate School of the University of Massachusetts Amherst in partial fulfillment of the requirements for the degree of Doctor of Philosophy September 2009 Organismic and Evolutionary Biology
© Copyright by Micah Dunthorn 2009 All Rights Reserved
CILIATE BIODIVERSITY AND PHYLOGENETIC RECONSTRUCTION ASSESSED BY MULTIPLE MOLECULAR MARKERS
A Dissertation Presented By MICAH DUNTHORN
Approved as to style and content by:
_______________________________________ Laura A. Katz, chair _______________________________________ Robert L. Dorit, member _______________________________________ George B. McManus, member _______________________________________ Benjamin B. Normark, member
_______________________________________ Joseph S. Elkinton, Graduate Program Director Program in Organismic & Evolutionary Biology
To Frank Buchholz
13 February 1952—15 July 1991
ACKNOWLEDGEMENTS
Much thanks goes to my dissertation committee. Laura A. Katz, my advisor, provided her support throughout this dissertation. I thank Laura for allowing me to work in her lab and for teaching me many molecular methods. Rob Dorit was able to point out the bigger picture and context. George McManus was great to talk about ciliate evolution and the intricacies of ciliate taxonomy. And Ben Normark was always there to push me towards our current theoretical gaps. Much thanks also goes to Professor Dr. Wilhelm Foissner, who isolated and identified most of the ciliates that were used in this dissertation, and is a co-author on many of the chapters. I am not sure how he was able to put up with me while I visited his laboratory. Chapter 2 was a collaboration with Thorsten Stoeck, Marion Eppinger, M. V. Julian Schwarz, Michael Schweikert, and Jens Boenigk. Denis Lynn collaborated on the PhyloCode classification in Chapter 7. Phil Cantino, the editor for the Companion Volume to which the PhyloCode definitions will be published, was extremely helpful and patient in his edits. This dissertation would also not be possible without the many folks in the Katz lab. I will miss Mary Doherty’s jokes and her insights into ciliate biogeography. The following directly or indirectly also made an impact: Becky Zufall, Sofia Annis, Erica Barbero, Jennifer DeBarardinis, Jessica Grant, Meaghan Hall, Hannah Jaris, Allie Kovner, Dan Lahr, Christina Lyman, Bob Merritt, Laura Parfrey, Maiko Tamura, Yonas Tekle, Sam Torquato, and Laura Vann. Help also came from members of the Organismic and Evolutionary Biology program: Penny Jaques, Norman Johnson, David Lahti, and
v
Lynn Margulis. Caffeine and delicious vegan snacks were made possible by Melissa Krueger at the Elbow Room Café. Partial funding for this dissertation and for presenting at conferences came from: International Travel Award for Young Scholars, Society for the Study of Evolution; Holz-Connor Travel Grant, International Society of Protozoologists; Mini-PEET Award, Society of Systematic Biologists; Graduate Research Award, Society of Systematic Biologists; Travel Grant, 56th Annual Meeting, Society of Protozoologists; Graduate Fellowship, Massachusetts Space Grant Consortium. Funding was also provided by Laura A. Katz through her U.S. National Science Foundation grant #636498. I would also like to thank my mother and father—Lani and Tom—for their patience and help throughout my time in graduate school. Finally, I want to thank my son—(captain) Aureliano—for thinking that working in the lab consists of watching movies in my office, since that is what he did the so many times I dragged him to the lab so I can perform just more PCR and cloning on a Saturday afternoon.
vi
ABSTRACT CILIATE BIODIVERSITY AND PHYLOGENETIC RECONSTRUCTION ASSESSED BY MULTIPLE MOLECULAR MARKERS SEPTEMBER 2009 MICAH DUNTHORN, B.A., GEORGE MASON UNIVERSITY M.A., UNIVERSITY OF MISSOURI ST. LOUIS PH.D., UNIVERSITY OF MASSACHUSETTS AMHERST Directed by: Laura A. Katz
Ciliates provide a powerful system within microbial eukaryotes in which molecular genealogies can be compared to detailed morphological taxonomies. Two groups with such detailed taxonomies are the Colpodea and the Halteriidae. There are about 200 described Colpodea species that are found primarily in terrestrial habitats. In Chapters 1 and 2, taxon sampling is increased to include exemplars from all major subclades using nuclear small subunit rDNA (nSSU-rDNA) sequencing. Much of the morphological taxonomy is supported, but extensive non-monophyly is found throughout. The conflict between some nodes of the nSSU-rDNA genealogy and morphology-based taxonomy suggests the need for additional molecular marker. In Chapter 3, character sampling is increased using mitochondrial small subunit rDNA (mtSSU-rDNA) sequencing. The nSSU-rDNA and mtSSU-rDNA topologies for the Colpodea are largely congruent for well-supported nodes, suggesting that nSSU-rDNA work in other ciliate clades will be supported by mtSSU-rDNA as well. Chapter 4 compares the underlying genetic variation within two closely related species in the
vii
Halteriidae with increased taxon and molecular sampling using nSSU-rDNA and internally-transcribed spacer (ITS) region sequencing. The morphospecies Halteria grandinella shows extensive genetic variation that is consistent with either a large effective population size or the existence of multiple cryptic species. This pattern contrasts with the minimal of genetic variation in the morphospecies Meseres corlissi. Chapter 5 discusses the congruence and incongruence among morphological and molecular data in ciliates. Most of the incongruence occurs where there is little statistical support for the molecules, or where molecular data is consistent with alternative morphological hypotheses. Chapter 6 reviews the data for sex, or lack thereof, in the Colpodea, a potentially ancient asexual group where sex was regained in a derived species. In Chapter 7, four ciliate clades are redefined using the PhyloCode.
viii
CONTENTS Page ACKNOWLEDGEMENTS……………………………………………………………… v ABSTRACT…………………………………………………………………………..…vii LIST OF TABLES………………………………………………………………………xiv LIST OF FIGURES……………………………………………………………………...xv CHAPTERS 1. MOLECULAR PHYLOGENETIC ANALYSIS OF CLASS COLPODEA (PHYLUM CILIOPHORA) USING BROAD TAXON SAMPLING………………….……………..1 1.1. Abstract……………………………………………………………………….2 1.2. Introduction……………………….…………………………………………..3 1.3. Materials and methods…………………….……………………….................7 1.3.1. Taxon sampling and collection……………………………..………7 1.3.2. Identification………………………………………………………..7 1.3.3. DNA extraction, amplification, cloning and sequencing…………...7 1.3.4. Genealogical analyses………………………………………………9 1.4. Results……………………………………………………………………….10 1.4.1. Pairwise distances within collections……………………………...10 1.4.2. Deletion within one SSU rDNA copy in Bryometopus pseudochilodon…………………………………………………..11 1.4.3. Intron in Cyrtolophosis mucicola…………………………………12 1.4.4. SSU rDNA genealogy of the Colpodea…………………………...12 1.5. Discussion…………………………………………………………………...16 1.5.1. Comparisons between morphology and molecules………………..16 1.5.1.1. The class…………………………………………………16 1.5.1.2. The orders……………………………………………….16 1.5.1.3. The genus Colpoda……………………………………...20 1.5.2. Open questions with some species designations………………..…21 1.5.3. Evidence for sex…………………………………………………...22 1.5.4. Group I intron in Cyrtolophosis mucicola………………………...23 1.5.5. Reconciling morphology and molecules in the Colpodea………...24 1.6. References………………………………………………………………...…25
ix
2. PHYLOGENETIC PLACEMENT OF THE CYRTOLOPHOSIDIDAE STOKES, 1888 (CILIOPHORA; COLPODEA) AND NEOTYPIFICATION OF ARISTEROSTOMA MARINUM KAHL, 1931…………………………………………...40 2.1. Abstract……...………………………………………………………………41 2.2. Introduction………………………………………………………………….42 2.3. Methods……………………………………………………………………...43 2.3.1. Taxon sampling……………………………………………………43 2.3.2. Light and electron microscopy…………………………………….44 2.3.3. Terminology……………………………………………………….45 2.3.4. Autecology……………………………………………………...…45 2.3.5. Amplification and sequencing ……………………………………47 2.3.6. Genealogical analyses……………………………………………..48 2.3.7. Constrained analysis……………………………………………....49 2.3.8. Rate class analysis…………………………………………………49 2.4. Results……………………………………………………………………….49 2.4.1. Description of the neotype of Aristerostoma marinum Kahl, 1931………………………………………………………..49 2.4.2. Electron microscopy………………………………………………51 2.4.3. Autecology………………………………………………………..52 2.4.4. Pairwise SSU rDNA sequence differences within the Cyrtolophosididae………………………………………………..52 2.4.5. Genealogical analysis……………………………………………...53 2.4.6. Comparisons of hypotheses……………………………………….54 2.4.7. Long-branch attraction…………………………………………….54 2.5. Discussion…..……………………………………………………………….56 2.5.1. Neotypification and emended diagnosis of Aristerostoma marinum Kahl 1931………………………....…………………...55 2.5.2. Emended diagnosis………………………………………………..56 2.5.3. Occurrence and ecology……………………………………….…..57 2.5.4. Comparison with original descriptions and related species……….58 2.5.5. Neotype specimens…………………………………………..……61 2.5.6. Pairwise distance between Aristerostoma morphospecies………...61 2.5.7. Phylogenetic placement of the order Cyrtolophosidida…………...61 2.5.8. Reconciling morphology and molecules…………………………..62 2.5.9. Assignment of GenBank environmental SSU-rDNA sequences to the Cyrtolophosididae…………………………...…64 2.6. Conclusions………………………………………………………………….65 2.7. References…………………………………………………………………...67
x
3. EXPANDING CHARACTER SAMPLING IN CILIATE PHYLOGENETIC RECONSTRUCTION: MITOCHONDRIAL SSU-rDNA AS A MOLECULAR MARKER………………………………………………………………………………..86 3.1. Abstract……...………………………………………………………………87 3.2. Introduction………………………………………………………………….88 3.3. Methods……………………………………………………………………...90 3.3.1. Taxon sampling and terminology…………………………………90 3.3.2. DNA amplification and sequencing……………………………….91 3.3.3. Genealogical analyses……………………………………………..91 3.3.4. Data partitioning and congruence testing…………………………92
3.4. Results……………………………………………………………………….93 3.4.1. Characteristics of gene sequences…………………………………93 3.4.2. MtSSU-rDNA analyses……………………………………………94 3.4.3. Nuclear SSU-rDNA analyses and topology congruence………….96 3.4.4. Concatenated analyses…………………………………………….97 3.5. Discussion……………………………………………………………….…..98 3.5.1. Mitochondrial SSU-rDNA as a ciliate molecular marker…………98 3.5.2. Morphology vs. molecules in ciliates……………………………100 3.5.3. Systematic implications………………………………………….101 3.6. Conclusions………………………………………………………………...101 3.7. References………………………………………………………………….102 4. EXTENSIVE GENETIC DIVERSITY WITHIN HALTERIID CILIATES………...115 4.1. Abstract……...……………………………………………………………..116 4.2. Introduction………………………………………………………………...117 4.3. Methods…………………………………………………………………….118 4.3.1. Taxon sampling and identification……………………………….118 4.3.2. Amplification, cloning, and sequencing…………………………119 4.3.3. Genealogical analyses……………………………………………120 4.4. Results……………………………………………………………………...121 4.4.1. Intra-isolate pairwise distances…………………………………..121 4.4.2. Genealogies………………………………………………………122 xi
4.5. Discussion………………………………………………………………….124 4.4.1. Genetic variation underlying morphospecies…………………….124 4.6. References………………………………………………………………….126 5. RICHNESS OF MORPHOLOGICAL HYPOTHESES IN CILIATE SYSTEMATICS ALLOWS FOR DETAILED ASSESSMENT OF HOMOLOGY AND COMPARISONS WITH GENE TREES………………………………………...138 5.1. Abstract……...……………………………………………………………..139 5.2. Introduction………………………………………………………………...140 5.3. Strengths of morphology…………………………………………………...140 5.3.1. Species delimitations…………………………………………….140 5.3.2. Ciliate tree of life………………………………………………...141 5.4. Challenges to Morphological analyses…………………………………….142 5.4.1. Decline in number of trained taxonomists……………………….142 5.4.2. Number of characters…………………………………………….142 5.4.3. Homology assessment……………………………………………143 5.5. Concordance with molecular hypotheses…………………………………..144 5.6. Open Questions…………………………………………………………….145 5.6.1. Lack of morphological variation when there is genetic diversity..145 5.6.2. Lack of genetic diversity when there is morphological variation..146 5.7. References………………………………………………………………….148 6. ANCIENT ASEXUAL LINEAGE OF CILIATES THAT REGAINED SEX?..........157 6.1. Abstract……...……………………………………………………………..158 6.2. Introduction………………………………………………………………...159 6.3. Empirical evidence…………………………………………………………160 6.4. Are colpodeans ancient asexuals? …………………………………………162 6.5. Did colpodeans reverse the loss of sex? …………………………………..163 6.6. Conclusion…………………………………………………………………165 6.7. References………………………………………………………………….166
xii
7. PHYLOCODE DEFINITIONS FOR FOUR CILIATE CLADES..…………………173 7.1. Abstract……...………………………………………………………….….174 7.2. Introduction………………………………………………………………...175 7.3. The PhyloCode……………………………………………………………..176 7.4. Why the PhyloCode should be applied to ciliate…………………………..177 7.5. Application of the PhyloCode to four ciliate clades……………………….179 7.5.1. Ciliophora………………………………………………………..180 7.5.2. Postciliodesmatophora…………………………………………..182 7.5.3. Intramacronucleata………………………………………………184 7.5.4. Colpodea…………………………………………………………186 7.6. References…………………………………………………………………188 BIBLIOGRAPHY………………………………………………………………………195
xiii
LIST OF TABLES
Figure
Page
1.1
Taxon sampling within the Colpodea……………………………………………31
1.2
Pairwise distance between collections for species sampled more than once…….32
2.1
Taxon sampling and GenBank numbers used in this study……………………...71
2.2
Morphometric data for Aristertostoma marinum population Framvaren Fjord….72
2.3
Comparative morphology of described representatives of four genera in The Cyrtolophosididae…………………………………………………………...73
3.1
Taxon sampling for mtSSU…………………..………………………………...108
4.1
Isolates newly collected for this study………………………………………….130
4.2
Newly sampled loci……………………………………………………………..131
xiv
LIST OF FIGURES Figure
Page
1.1
Evolution among some morphological characters within the class Colpodea…...33
1.2
SSU rDNA genealogy of the class Colpodea and potential sister classes……….35
2.1
Light microscopy of living (a, b) and protargol impregnated (c) Aristerostoma marinum cells....………………………………………………………………….74
2.2
Scanning and transmission electron microscopy of Aristerostoma marinum……76
2.3
Schematic drawing of Aristerostoma marinum (right lateral view) that combines diagnostic features as revealed by live cell imaging, protargol staining and scanning electron microscopy.…………………………………………………...78
2.4
Ecophysiological tolerance limits of Aristerostoma marinum population Framvaren Fjord………………….………………………….…………………...80
2.5
Schematic drawing of the idealized oral structures (paroral membranes and adoral organelles) of the Cyrtolophosididae……………………………………..82
2.6
Most likely Bayesian SSU-rDNA genealogy of the class Colpodea…………….84
3.1
Mitochondrial SSU-rDNA genealogy of the Colpodea………………………...109
3.2
Concatenated nuclear and mitochondrial SSU-rDNA genealogy of the Colpodea………………………………………………………………………..112
4.1
Concatenated SSU-rDNA/ITS genealogy of the halteriids……………….....…132
6.1
Phylogeny and distribution of sex within the Colpodea…….………………….171
Supplementary Figures 1.1
SSU-rDNA genealogy of the class Colpodea and potential outgroups with support from all nodes indicated…………………………………………………37
3.1
Nuclear SSU-rDNA genealogy of the Colpodea…………..…………………...113
4.1
SSU-rDNA genealogy of the halteriids………………………………………...134
4.2
ITS genealogy of the halteriids…………………………………………………136
xv
Appendix 1.A
GenBank accessions used in analyses for both previously sequences Colpodea taxa and outgroups…………………………………………………….39
xvi
CHAPTER 1 MOLECULAR PHYLOGENETIC ANALYSIS OF CLASS COLPODEA (PHYLUM CILIOPHORA) USING BROAD TAXON SAMPLING Micah Dunthorn,a Wilhelm Foissnerb and Laura A. Katza,c
a
Graduate Program in Organismic and Evolutionary Biology, University of
Massachusetts Amherst, USA b
c
FB Organismische Biologie, Universität Salzburg, Austria
Department of Biological Sciences, Smith College, USA
1
1.1. Abstract The ciliate class Colpodea provides a powerful case in which a molecular genealogy can be compared to a detailed morphological taxonomy of a microbial group. Previous analyses of the class using the small-subunit rDNA are based on sparse taxon sampling, and are therefore of limited use in comparisons with morphologically-based classifications. Taxon sampling is increased here to include all orders within the class, and more species within previously sampled orders and in the genus Colpoda. Results indicate that the Colpodea may be paraphyletic, although there is no support for deep nodes. The orders Bursariomorphida, Grossglockneriida, and Sorogenida are monophyletic. The orders Bryometopida, Colpodida and Cyrtolophosidida, and the genus Colpoda, are not monophyletic. Although congruent in many aspects, the conflict between some nodes on this single genealogy and morphology-based taxonomy suggests the need for additional markers as well as a reassessment of the Colpodea taxonomy.
2
1.2. Introduction Assessment of phylogeny based on morphological characters is limited in many microbial eukaryotes. In most amoebae and flagellates morphology provides little guidance and taxonomic resolution is not rich below the class and ordinal levels. In contrast, phylum Ciliophora Doflein, 1901 is relatively morphologically rich and has a well-described taxonomy (Lynn, 2003; Lynn and Small, 2002). Class Colpodea Small and Lynn, 1981 provides a particularly good opportunity to compare the power of morphology and molecular analyses in reconstructing the phylogeny of ciliates. The Colpodea is monographed and contains a number of somatic and oral characteristics that were used to establish an extensive classification (Foisser, 1993a). Because previous molecular investigations of the class are based on sparse taxon sampling (LasekNesselquist and Katz, 2001; Lynn et al., 1999; Stechmann et al., 1998), molecular support for the groups established by Foissner (1993a) remains to be evaluated. The Colpodea is one of eleven ciliate classes (Adl et al., 2005; Lynn, 2003). Although its position in the subphylum Intramacronucleata is established (Lynn, 2003), well-supported evidence for the sister class of the Colpodea remains elusive. With current taxonomic sampling, neither morphology nor molecules give convincing or consistent arguments because of homoplasy, low bootstrap support, and problems from both paralogy and rate heterogeneity in protein-coding genes (Lasek-Nesselquist and Katz, 2001; Lynn et al., 1999; Stechmann et al., 1998). The classes Nassophorea, Oligohymenophorea, Plagiopylea, and Prostomatea are the likely sister-group candidates. Historically, members of the class Colpodea were placed in disparate groups based on oral structure differences (Foissner, 1993a; Lynn et al., 1999). With Lynn’s
3
(1976; 1981) structural conservatism hypothesis, somatic kinety (kinetosomes and associated fibers) differences were found to be more a appropriate guide to the deep divisions within the ciliates. The Colpodea were united because of their left kinetodesmal fiber (LKm fiber) (Foissner, 1993a). This fiber extends posteriorly and to the left of the posterior kinetosome of their somatic dikinetids. In contrast, Bardele (1981; 1989) argues against the monophyly of the class because of differences in the presence or absence of particles (ciliary plaques) in the membrane of the somatic cilia: they are present only in one order in the Colpodea (Colpodida) and are absent in the rest of the class. The Colpodea are a group of primarily terrestrial ciliates (Foissner, 1993a). Besides the unique LKm fiber, the class Colpodea contains distinctive silverline patterns of regular meshes: ‘colpodid’, with large, rectangular meshes; ‘platyophryid’, meshes divided by median silverline between the kineties, or ‘kreyellid’, with minute irregular meshes (Foissner, 1993a). Members of the Colpodea also have somatic stomatogenesis, where parental oral structures are partially or completely reorganized before new oral structures develop during cell division (Foissner, 1993a; Foissner, 1996). In general, a single ‘germline’ micronucleus is close to the single ‘somatic’ macronucleus; in at least some taxa in order Cyrtolophosidida the micronucleus and macronucleus share an outer membrane of the nuclear envelope (Foissner, 1993a). Sex has only been demonstrated in Bursaria truncatella and is unreported in the rest of the class (Foissner, 1993a; Raikov, 1982). Foissner (1993) monographed about 170 species and established an extensive higher-level classification for the Colpodea. Subsequently, new genera and species have been described (Foissner, 1993b; Foissner, 1993c; Foissner, 1994; Foissner, 1995;
4
Foissner, 1999; Foissner, 2003; Foissner et al., 2002; Foissner et al., 2003). Foissner’s (1993a) split the Colpodea into two subclasses: one with the order Bryometopida based on a ‘kreyellid’ silverline pattern; with the rest of the orders in another subclass, based on ‘colpodid’ and ‘platyophryid’ silverline patterns. These silverline patterns were later argued to be misleading, as SSU rDNA places the Bryometopida next to order Bursariomorphida (Lynn et al., 1999). In large part there is agreement over Foissner’s (1993a) orders and families among other classifications (e.g., Puytorac, 1994), except order Grossglockneriida is lumped with order Colpodida in Lynn and Small (1997; 2002). Based on morphological characters, Foissner (1993a) offers several hypotheses for relationships among these Colpodea orders (Figure 1.1, Table 1.1). First, Colpodida and Grossglockneriida are sister taxa since they share merotelokinetal stomatogenesis (complete reorganization of parental oral structures), which is probably the derived condition (Figure 1.1A, character 12). In contrast, the other orders have the possibly plesiomorphic state of pleurotelokinetal stomatogenesis (partial reorganization of parental oral structures) (Figure 1.1A, character 1); this hypothesis is supported in previous molecular analyses (Lynn et al., 1999; Lasek-Nesselquist and Katz, 2001). Second, Bursariomorphida, Colpodida and Grossglockneriidae form a clade because of the possibly apomorphic equally-spaced rows of oral polykinetids (Figure 1.1A, characters 9), as opposed to the possibly plesiomorphic brick-shaped adoral organelles (Figure 1.1A, character 1); this hypothesis is not supported in previous molecular and morphological analyses (Foissner and Kreutz, 1998; Lasek-Nesselquist and Katz, 2001; Lynn et al., 1999). Third, Bryophryida, Bursariomorphida, Colpodida and
5
Grossglockneriida form a clade because of the possibly apomorphic deep vestibulum (depression in the cell with oral structures) (Figure 1.1A, character 7), as opposed to the possibly plesiomorphic flat vestibulum (Figure 1.1A, character 1). Using limited taxon sampling with small-subunit rDNA (SSU rDNA), monophyly of the class Colpodea is strongly supported by least-squares (LS) and neighbor-joining (NJ), and weakly supported by maximum parsimony (MP) analyses in Lynn et al. (1999). In contrast, with just one additional taxon sampled, Lasek-Nesselquist and Katz (2001) find the class to be paraphyletic, with Nassophorea embedded within it—although support is weak from NJ, MP, and maximum likelihood (ML). Here we increase taxon sampling of the Colpodea using SSU rDNA sequences, including morphospecies from all seven orders, multiple morphospecies within most orders, and multiple morphospecies in the genus Colpoda. Our aim is to assess the following hypotheses: (1) the class Colpodea is monophyletic, (2) orders within the class Colpodea are monophyletic, and (3) the genus Colpoda is monophyletic. We will also discuss other features uncovered during characterization of SSU rDNA sequences: two distinct copies of SSU rDNA in one taxon, a group I intron in another, and evidence for sex in the Colpodea taxa sampled here. Furthermore, we discuss alternative hypotheses of morphological evolution based on the SSU rDNA topology. Results from these analyses will further development of a predictive, tree-based framework for the taxonomy of the Colpodea.
6
1.3. Materials and methods 1.3.1. Taxon sampling and collection To reconstruct an SSU rDNA genealogy of the Colpodea 27 collections representing 22 species were sampled for this study (Table 1.1). Most species sequenced were collected from soil, i.e., from non-flooded Petri dish cultures as described in Foissner et al. (2002). Some were from the water and mud occurring in the tanks of bromeliad plants (Foissner et al., 2003). Cells were either collected from the raw culture (with other species in the dish) or were isolated into clonal culture (with one to few starter cells). With the addition of GenBank accessions from previous studies (Appendix 1.A), the current sampling includes exemplars from all orders, 15 families, 18 genera, and seven morphospecies in the genus Colpoda. Outgroup selection is based partially on previous analyses.
1.3.2. Identification Species were identified according to the monograph of Foissner (1993), using live observations and various silver impregnation techniques. The new species collected here—Bursaria sp., Platyophrya-like, Platyophrya sp., Rostrophyra sp., and Sagittaria sp.—will be described in separate papers.
1.3.3. DNA extraction, amplification, cloning and sequencing Between 10 and 10,000 cells were picked with a micropipette, washed, and placed into DNA lysis buffer. Genomic DNA was extracted using phenol/chloroform following standard protocols (Ausubel et al., 1993) or with a DNeasy Tissue kit (Qiagen, CA).
7
Genomic DNA was amplified using universal 5’ and 3’ prime SSU rDNA primers (Medlin et al., 1998) with one of two polymerases. For some species Vent polymerase (New England BioLabs, MA) was used with the following cycling conditions: 4:00 at 950; 32 cycles of 0:30 at 950, 0:30 at 540, and 2:00 at 720; 10:00 extension at 720. For others Phusion polymerase (New England BioLabs, MA) was used with the following cycling conditions: 0:30 at 980; 36 cycles of 0:30 at 980, 0:15 at 680, 1:30 at 720; 10:00 extension at 720. Amplified products were cleaned with a low-melt gel and Ultrafree-Da columns (Millipore, MA), or with microCLEAN (The Gel Company, CA). To assess within-sample variation, amplified products were cloned with the PCRSMART Cloning kit (Lucigen, WI), or Zero Blunt TOPO kit (Invitrogen, CA). Positive clones were identified by PCR screening with AmpliTag Gold polymerase (Applied Biosystems, CA), and minipreped using Qiaprep Spin Miniprep kit (Qiagen, CA). Clones were sequenced with the Big Dye terminator kit (Applied Biosystems, CA), using 5’ and 3’ primers as well as two internal primers (Snoeyenbos-West et al., 2002). All sequences were run on an ABI 3100 automated sequencer. Three samples required further methods. For the Bryometopus pseudochilodon indel found in this study, a 5’ primer (AAA CAG TTA TAG GCA GGC AAT TG) was designed that spanned both sides of the deletion to make sure the sequences containing the deletion were not an amplification artifact. Genomic DNA was amplified with this primer along with the universal 3’ primer, following the above protocol. For Colpoda aspera and Cyrtolophosis mucicola (from Austria), algal contaminant SSU rDNA sequences were removed by enzymatic digestion. Amplified products were cleaned with microCLEAN. Re-suspended DNA was incubated at 370 for three hours with BamH1
8
(New England BioLabs, MA). The reaction was stopped with microCLEAN, and the DNA was cloned with the Zero Blunt TOPO kit and sequenced following the above protocol.
1.3.4. Genealogical analyses Phylotypes were constructed from the consensus of the multiple sequence reads of the cloned products and edited in SeqMan (DNAStar). Pairwise distances for within samples were calculated as uncorrected distances in PAUP* v4.0b8 (Swofford, 2002). Phylotypes were aligned using Hmmer v2.1.4 (Eddy, 2001), with default settings. The training alignment for model building was all available ciliate SSU rDNA sequences downloaded from the European Ribosomal Database (Wuyts et al., 2004) and aligned according to their secondary structure. The alignment was further edited by eye in MacClade v4.05 (Maddison and Maddison, 2005), with ambiguously aligned regions and base-pair positions with more than five taxa having a gap masked. Remaining gaps were treated as missing data. The GTR+I+G evolutionary model was estimated using hLTR in MrModeltest v2 (Nylander, 2004). Maximum parsimony (MP) analyses were carried out in PAUP* v4.0b8 (Swofford, 2002), with all characters equally weighted and unordered. The TBR heuristic search option was used, running ten random additions with MulTree option on. Maximum likelihood (ML) analyses were carried out in RAxML v2.2.0 (Stamatakis, 2006) running 100 replicates. Support for MP and ML analyses came from 1000 bootstrap replicates using heuristic searches. Bayesian analyses was carried out using MrBayes v3.2.1 (Huelsenbeck and Ronquist, 2003) with support coming from posterior
9
probability using four chains and running 10 million generations. Trees were sampled every 100 generations. The first 25% of sampled trees were considered ‘burnin’ trees and were discarded prior to tree reconstruction. A 50% majority rule consensus of the remaining trees was used to calculate posterior probability. Trees were imaged with TreeView v1.6.6 (Page, 1996).
1.4. Results 1.4.1. Pairwise distances within collections SSU rDNA sequences from twenty-seven collections representing 22 morphospecies show, for the most part, less than 0.50% average pairwise difference among clones within samples (Table 1.1). Sequences are deposited in GenBank, numbers EU039884-EU039908. Six clones from Bardeliella pulchra show more variation with an average pairwise difference of 0.94%. Clones from the Bursaria sp. 2 collection contain two different phylotypes that are 0.94% different. The phylotypes of the Ilsiella palustris collection from Brazil are 0.57% different, while in the Hawaiian collection phylotypes are 0.54% different. The levels of within-collection variation are assumed to be a combination of intraspecific variation and experimental error. Contaminant SSU rDNA sequences were found in a few cases; for example: algae in B. pulchra, Bresslauides discoideus, Colpoda aspera, Cyrtolophosis mucicola from Austria, and I. palustris from Hawaii; fungi in Bryometopus pseudochilodon, and Mykophagophrys terricola; and a tetrahymenid ciliate from Hausmanniella discoidea.
10
Five species were collected more than once, allowing for some within species comparison (Table 1.2). There is no variation between the two B. discoideus collected from Dominican Republic. Between the Malaysian and Niger Colpoda cucullus collections the average pairwise difference among collections was 0.47%, with no phylotype shared between the sites. Although there is no difference between the two Brazilian collections of C. mucicola, the Brazilian and the Austrian collections are 1.71% different with no phylotype shared between the countries. The I. palustris collections are 0.64% different and likewise do not share phylotypes between the sites.
1.4.2. Deletion within one SSU rDNA copy in Bryometopus pseudochilodon Two distinct SSU rDNA sequences were characterized from the B. pseudochilodon collection (Table 1.1). One sequence corresponds to the other full-length Colpodea sequences found here and from GenBank accessions. The second sequence is almost identical to the first except there is a 642 bp deletion towards the 5’ prime end of the SSU rDNA sequence and there are two nucleotide differences on the 5’ end. The deletion starts at nucleotide position 129 in E. coli (GB# J01695) (Cannone et al., 2002). There is no evidence of elevated substitutions in the sequence with the deletion. This shorter sequence was uncovered in two separate amplifications using universal SSU rDNA primers, as well as from amplifications using a 5’ primer (see methods) that was designed to span either side of the deletion (data not shown). The deletion spanned multiple regions of the SSU rDNA molecule that are conserved in all extant organisms (Mears et al., 2002). We hypothesize that the deletion sequence is a macronuclear variant,
11
which occurred in the process of macronuclear development and has been perpetuated during asexual divisions.
1.4.3. Intron in Cyrtolophosis mucicola A 427 bp intron was found in all SSU rDNA clones from C. mucicola collected from Austria but not the C. mucicola collected from Brazil. The start residue is T and the ending residue is G, which is consistent with group I introns. Blast results also point to this sequence being a group I intron (E value= 1e-16 with the group I intron in Fulgio septica, GB# AJ555452.1; E value= 5e-13 with the group I intron in Acanthamoeba sp., GB# EF140633.1). There is no evidence for a homing endoculease gene in the intron. The insertion position of this intron in the SSU rDNA molecule corresponds to nucleotide 516 in E. coli (GB# J01695) (Cannone et al., 2002), which is a hotspot for group I intron insertions (Jackson et al., 2002).
1.4.4. SSU rDNA genealogy of the Colpodea After a preliminary analysis using multiple exemplars from all eleven ciliate classes, only Colpodea sequences and close outgroups were chosen for more detailed analyses. The potential sister classes in this analysis as determined in the preliminary global ciliate analysis are the same as in previous studies: Nassophorea, Plagiopylea, Prostomatea, and Oligohymenophorea (data not shown). One phylotype from each sampled species was used in the alignment, except two representatives of C. mucicola (because they may underlie two species, see below) and Bursaria sp. 2 (because the other Bursaria sequences are relatively close).
12
The final SSU rDNA alignment used for comparing the morphological hypotheses of the Colpodea and its subgroups includes 59 sequences and has a length of 1582 unmasked nucleotides, of which 219 are parsimoniously informative. The most parsimonious tree from the MP analysis is 3349 in length, with a Consistency index of 0.3842, and a Homoplasy index of 0.6157. The most likely tree from the ML analysis has a log likelihood of -17450.098, while the most likely tree from the Bayesian analysis has a log likelihood of -17445.169. Here we present only the most likely Bayesian tree with node support from all three methods (Figure 1.2, see Supplementary Figure 1.1 for all node support values). The topologies of the MP- and ML-derived genealogies are mostly congruent with the Bayesian topology, except in three places. First, in the MP and ML analyses Cyrtolophodidia II (see below) is basal to the rest of the Colpodea+Oligohymenophorea+Plagiopylea+Prostomatea with no bootstrap support, and a paraphyletic Nassophorea is basal to this group with no bootstrap. Second, in the MP and ML analyses Bryometopus pseudochilodon is basal to the rest of its order with no bootstrap support, while in the Bayesian tree B. sphagni is basal. Third, in the MP and ML analyses the order Grossglockneriida forms an unsupported clade with Colpoda aspera, C. steinii, Chain-forming colpodid, and Hausmaniella discoidea, while in the Bayesian tree it does not. In our analyses, there is no support for the monophyly of the Colpodea: monophyly of the class is weakly rejected by all three methods based on tree topologies and support values. Furgasonia and Obertrumia (both in the class Nassophorea) fall out sister to part of the order Cyrtolophosidida with no support from all three methods (- MP
13
bootstrap/- ML bootstrap/- Bayesian posterior probability; support >50% or 0.5 is shown as ‘-’). Changing the number of outgroup classes does not significantly alter this nonmonophyletic topology as the deep nodes are not well resolved anyways and there is no support for any class to be sister to the Colpodea. The rest of the Colpodea forms a monophyletic clade with weak support from MP and ML but with high support from Bayesian analysis (53/56/0.99). Support for relationships among the outgroups varied by method. The class Prostomatea is paraphyletic with only moderate support from Bayesian analysis (-//0.90), with the genus Coleps sister to a well-supported monophyletic class Plagiopylea (100/100/1.00). The monophyly of Oligohymenophorea is moderately to highly supported in ML and Bayesian analyses (59/71/1.00). The clade containing Prostomatea, Plagiopylea and Oligohymenophorea is moderately to highly supported by ML and Bayesian analysis (53/-/1.00). Monophyly of the morphologically defined groups could be assessed with our single gene tree for every order within the Colpodea, except Bryophryida as only one morphospecies was sampled for this order. Sorogenida, with two genera, is monophyletic with full support (100/100/1.00). Bursariomorphida, with four taxa, is monophyletic also with high support (93/89/1.00). Grossglockneriida, with two genera, is likewise monophyletic with moderate to high support (90/82/1.00). Order Cyrtolophosidida, with six sampled genera, is not monophyletic. The genus Cyrtolophosis falls sister to the order Colpodida with moderate to high support (86/96/1.00). The remaining Cyrtolophosidida genera (Ottowphrya, Platyophrya-like,
14
Platyophrya, Rostrophrya, and Sagittaria) form a paraphyletic group, with order Sorogenida nested within it, at the base of the class with high support (100/99/1.00). Order Bryometopida, with one genus and three species sampled, is not monophyletic with full support from all three methods (100/100/1.00). Order Bursariomorphida is nested within this order, and it is sister to Bryometopus pseudochilodon with full support (100/100/1.00). To determine whether this topology is spurious due to the GenBank accession for Bryometopus sphagni missing about 500 bp from the 5’ end, the Bryometopida and Bursariomorphida sequences were realigned (with C. magna and C. mucicola as outgroups) minus the 5’ end; the same topology was found with this alignment (data not shown). Order Colpodida is not monophyletic with high support (97/93/1.00), containing orders Grossglockneriida and Bryophryida. B. pulchra is sister to Notoxoma parabryophryides (order Bryophryida) with moderate to high support (87/94/0.98). Monophyly of the genus Colpoda was assessed in this molecular analysis using eight morphospecies within the genus and numerous close outgroups. Colpoda is not monophyletic in the SSU rDNA genealogy with moderate to full support (73/72/1.00). Most Colpoda species form a sister group to the Grossglockneriida with no support from any method (-/-/-). B. vorax, B. discoideus, and Colpoda henneguyi form a clade with moderate to high support (89/84/1.00). This clade is in turn sister to most of the remaining Colpoda species with moderate to high support (72/80/0.97). To determine if the topology of the Colpoda phylotypes is robust, only Colpodida, Grossglockneriida, and Bryophryida phylotypes were realigned and remasked for a separate analysis; overall, the resulting ingroup topology is concordant with the full class analysis (data not shown).
15
1.5. Discussion 1.5.1. Comparisons between morphology and molecules Here we compare the morphologically-based classification and well-supported SSU rDNA nodes. Furthermore, we evaluate the possible evolution of morphological characters in light of the SSU rDNA genealogy.
1.5.1.1. The class: We find no molecular support for the monophyly of the class Colpodea based on analyses of SSU rDNA sequences (Figure 1.2). Conversely, the nonmonophyly of the class (with part of the class Nassophorea being sister to part of the order Cyrtolophosidida) is not well supported either. Similarly, the Nassophorea is also not monophyletic with respect to the Colpodea, though with no support. The nonmonophyletic relationships of the Colpodea with respect to the Nassophorea should not be given much weight, as there is neither support for this relationship nor for the Nassophorea even being sister to the Colpodea. The SSU rDNA genealogy here provides little support for class-level relationships within the subphylum Intramacronucleata in general, as seen elsewhere (Lynn, 2003). These results do not pose a serious challenge to Lynn’s (1976; 1981) structural conservatism hypothesis given the limited support at deep nodes. On the other hand, these results do challenge Bardele’s (1981; 1989) use of ciliary plaques in his argument that the members in the Colpodea are not closely related.
1.5.1.2. The orders: Molecular support for monophyly could be assessed for all orders within the Colpodea except the Bryophryida. The SSU rDNA genealogy presented here
16
does support much of the morphologically-based classification of the Colpodea, although there is some discordance at the ordinal level between morphology and molecules (Figure 1.2). The order Cyrtolophosidida is polyphyletic. Cyrtolophosidida I, containing the genus Cyrtolophosis, falls away from Cyrtolophosidida II, containing the most recent common ancestor of Sagittaria and Platyophrya and all of its descendants plus the order Sorogenida. This nonmonophyly of the Cyrtolophosidida suggests the need for a reevaluation of the character that was used to establish this group. Cyrtolophosidida was circumscribed based on the shared outer membrane of the nuclear envelope of the micronucleus and macronucleus (Foissner, 1985; Foissner, 1993a). This character, however, has only been confirmed with transmission electron microscopy for six species: Aristerostoma marinum (Detcheva and Puytorac, 1979), Cyrtolophosis mucicola (Detcheva, 1976; Didier et al., 1980), Platyophrya sphagni (Kawakami, 1991), Platyophrya spumacola (Dragesco et al., 1977), Pseudocyrtolophosis alpestris (Foissner, 1993a), and Woodruffides metabolicus (Golder, 1976). Njine (1979) states that nuclei in Kuklikophrya ougandae share an outer membrane (and presents a drawing of a stained cell showing this), but does not present an electron micrograph. Platyophryides latus is drawn with a shared outer membrane by Dragesco and Dragesco-Kernéis (1979), but Puytorac et al. (1992) show that the membranes are separate with their transmission electron micrographs. Foissner (1993a) argues that two taxa, Sagittaria australis and Woodruffia australis, have the shared outer membrane because of their thick silverstained membranes. On the other hand, Díaz et al. (2000) show separate outer nuclear membranes in Cyrtolophosis elongata. Hence, the shared outer membrane of the nuclear
17
envelope of the micronucleus and macronucleus is not only a weak character for the Cyrtolophosidida, but also one whose distribution is neither well known nor confirmed (Figure 1.1B, character 4). Future transmission electron microscopy studies are much needed to confirm the presence or absence of this character in other species. Foissner et al. (2002) suggest those species with a separate outer micronucleus and macronucleus membrane can be transferred to the clade Plesiocaryon or into the order Sorogenida (as was done with Ottowphrya). There are morphological differences between the two Cyrtolophosidida groups. In Cyrtolophosidida I, there are two segments in the paroral (right oral) membranes, the anterior bearing tuft-like cilia (the unique feature of its family) (Figure 1.1B, character 15). Only one paroral segment is present in taxa in Cyrtolophosidida II (Figure 1.1B, character 14). These groups also differ in the presence of non-ciliated kinety on the right margin of the adoral organelles in Cyrtolophosidida I (and its family), which is absent in Cyrtolophosidida II (Figure 1.1B, character 16). Although originally placed with the haptorid ciliates (Bradbury and Olive, 1980), the close relationship between the Sorogenida and the Cyrtolophosidida was soon recognized morphologically (Bardele et al., 1991; Foissner, 1985; Small and Lynn, 1981). This relationship was confirmed in a previous SSU rDNA analysis (LasekNesselquist and Katz, 2001) and the SSU rDNA topology presented here. The Sorogenida was originally separated from the Cyrtolophosidida because it lacked the shared outer membrane of the nuclear envelope of the micronucleus and macronucleus (Foissner, 1985; Foissner, 1993a)—although this character maybe is weak (see above)—and because of its slime mold-like aerial sorocarp in one life history stage (Fig. 1.1, character
18
5). Like the Cyrtolophosidida, the Sorogenida has brick-shaped organelles on the left slope of the vestibulum and pleurotelokinetal stomatogenesis (Figure 1.1B, character 1) (Foissner, 1993a). The SSU rDNA genealogy suggests that the aerial sorocarp of Sorogena may represent a complex apomorphy arising from within Cyrtolophosidida II. The order Bryometopida is paraphyletic in relation to the monophyletic Bursariomorphida in the SSU rDNA genealogy. The close relationship between Bryometopida and Bursariomorphida was also found by Foissner and Kreutz (1998) and Lynn et al. (1999). Although these two orders differ in their silverline pattern (Bryometopida having ‘kryellid’ to ‘platyophryid,’ Bursariomorphida having ‘colpodid’), taxa in these two orders share an apical oral opening, a ventral cleft, conspicuous adoral organelles, and an emergence pore in their cysts (Foissner and Kreutz, 1998; Foissner, pers. obs.). The order Colpodida is paraphyletic in our molecular analyses, though support is limited at many nodes. That the Grossglockneriida was close to the Colpodida has been proposed as they share the unique (in the Colpodea) merotelokinetal stomatogenesis (Figure 1.1B, character 12), colpodid silverline pattern (Figure 1.1B, character 6), and a simple oral polykinetid (Aescht et al., 1991; Foissner, 1993a). These two orders are even lumped together in some classifications (Lynn and Small, 1997; Lynn and Small, 2002). The question remained just how they were related: the SSU rDNA genealogy here suggests that the Grossglockneriida falls within the Colpodida, not sister to it. The position of Bryophryida within the Colpodida has not been hypothesized as the Bryophryida has a platyophryid silverline pattern and brick-shaped organelles on the left
19
vestibulum (Figure 1.1B, character 1). The Bryophryida and Colpodida do, though, share a deep vestibulum (Foissner, 1993a). The use of differences in the type of division seems to be helpful at the ordinal level. As suggested by Foissner (1993a): pleurotelekinetal stomatogenesis is probably plesiomorphic within the Colpodea. Only orders Colpodida and the Grossglockneriida have merotelokinetal division (Foissner, 1993a). Stomatogenesis is undescribed in Bryophryida; assuming that its phylogenetic position found here is confirmed in future studies, then it is predicted that its division type should be merotelokinetal. On the other hand, the power of the silverline pattern for use in the systematics of the Colpodea at the ordinal level is debatable. While Foissner (1993a) uses differences in silverlines to help construct a higher-level classification, Foissner and Kreutz (1998) Lynn et al. (1999) argue that this character is sometimes misleading. The results presented here are in agreement with Lynn et al. (1999) on the limitations of the use of silverline patterns at the ordinal level.
1.5.1.3. The genus Colpoda: In our molecular analyses the large genus Colpoda is paraphyletic not only in relation to genera within its own family, but also to other families in its order (Figure 1.2). Most of the relationships among the Colpoda morphospecies in the SSU rDNA tree are not well supported; there is support for Bresslaua and Bresslauides nesting within the Colpoda. Bresslaua was originally separated from Colpoda based on a difference in vestibulum size (Kahl, 1931). However, Claff et al. (1941), Foissner (1985; 1993a), and Lynn (1979) find that Bresslaua’s voracious feeding behavior and its left-projecting vestibular wall (as opposed to right-
20
projecting in Colpoda) are probably better characters to separate the genus from Colpoda. The SSU rDNA topology suggests that these characters may represent apomorphies arising from within a Colpoda clade. Bresslauides (and its family Hausmanniellidae) also falls within the Colpoda in the SSU rDNA tree. This genus was circumscribed based on the unique semicircular right oral polykinetid that was longer than the left as opposed to being equal in the Colpodidae (Foissner, 1987; Foissner, 1993a). Because Bresslauides is not falling out with the other member of its family (Hausmanniella) sampled here, the character of a semicircularly curved right oral polykinetid may have evolved more than once.
1.5.2. Open questions with some species designations The level of diversity among some SSU rDNA sequences from the morphospecies collected here suggests possible problems with some circumscriptions. Colpoda magna and C. minima differ little in the SSU rDNA phylotypes, indicating a need for further genetic studies. These morphospecies species differ in size and kinety number, as well as the number of micronuclei, with one in C. minima and 2-16 in C. magna (Foissner, 1993a). The low genetic distance between these two species and the lack of much morphological differences could point to these being nascent but “biological” species. Alternatively, C. minima and C. magna may represent morphological variation within a single species where a change in micronuclei and kinety number is correlated with size. The C. mucicola morphospecies may represent two genetic species: there is a putative group I intron in the Austrian collection that is absent from the Brazilian collections, and there is greater than 1% pairwise distance between the Austrian and
21
Brazilian collections. In contrast, the diversity in SSU rDNA phylotypes for the genus Bursaria from this study and GenBank accessions (1.31% average pairwise distance) supports the view that there are more than one species in the genus, although some argue for there being only one species. We do not find the large sequence diversity in our Colpoda morphospecies as does Nanney et al. (1998). In our analysis we find a 2.79% average pairwise distance among the Colpoda morphospecies sampled here and from GenBank accessions, while Nanney et al. (1998) find an average “slack” value of 31.5% among their Colpoda. There are at least two reasons for this difference. First, our analyses were based on SSU rDNA, while theirs is based on 190 bp of the hyper-variable D2 region of the large subunit rRNA (LSU rDNA). Second, our analyses of distance used the uncorrected distance method in PAUP*, while theirs use string analyses in the program PHYLOGEN. Using our distance method, Nanney et al.’s (1998) data show an average pairwise distance of 20.73% for the D2 region of the LSU rDNA (data not shown). Despite the difference in levels of variation between the SSU rDNA and the short variable region of the LSU rDNA, the topology found by Nanney et al. (1998) among their five Colpoda morphospecies is congruent with our analyses (data not shown).
1.5.3. Evidence for sex Conjugation (ciliate sex) is documented in all ciliate classes (Bell, 1988; Dini and Nyberg, 1993; Miyake, 1996; Sonneborn, 1957). In the Colpodea conjugation is only known in B. truncatella even though over the decades researchers have looked for conjugation in other species but have yet to observe it (Foissner, 1993a; Raikov, 1982).
22
There are a few reports of possible conjugation in some species of Colpoda; because nuclear division or exchange was not shown these observations are possibly of “pseudoconjugation,” where exchange of nuclei does not occur (Foissner, 1993a). Assuming that Colpodea species behave genetically in a way similar to other eukaryotes, we could predict that if the Colpodea were asexual, allelic variation would be high within species (Mark Welch and Meselson, 2000; Normark, et al. 2003). The low allelic values within most collections sampled here suggest that the Colpodea species are indeed having sex albeit covertly. There is an important caveat in this statement in that the number of clones sequenced per morphospecies in this study is relatively low (1-7 clones) and we could have missed some variation. The results here are in opposition to Bowers et al. (1998), who present isozyme evidence for asexuality for three Colpoda species. Although cryptic sex is consistent with the low allelic values found here, further evidence of conjugation is much needed to confirm sex within the Colpodea beyond B. truncatella.
1.5.4. Group I intron in Cyrtolophosis mucicola While group I introns are widespread in microbial eukaryotes (Bhattacharya et al., 1996; Haugen et al., 2003; Haugen et al., 2005; Snoeyenbos-West et al., 2004; Wikmark et al., 2007), the putative group I intron found in the Austrian C. mucicola morphospecies is the fourth identification of this type of intron in ciliates. The other known species with group I introns are: Tetrahymena thermophila (Grabowski et al., 1981), Acineta sp. (Snoeyenbos-West et al., 2004), and Tokophrya lemnarum (Snoeyenbos-West et al., 2004). Undoubtedly there remain more of these introns to be uncovered in future
23
sequencing projects of the various ciliate groups. We suggest that the intron in the Austrian Cyrtolophosis mucicola is a product of a recent horizontal transfer into the SSU rDNA locus, as group I introns are known to be mobile over relatively short evolutionary time scales (Haugen et al., 2005; Simon et al., 2005) and because it was not found in other isolates of the species or other Colpodea sequences.
1.5.5. Reconciling morphology and molecules in the Colpodea In large part morphology and the SSU rDNA genealogy agree in the hypothesized relationships within the ciliate class Colpodea, although the paraphyletic relationships among previously hypothesized closely related taxa was unexpected (Figure 1.1). The SSU rDNA genealogy is based on a single gene and may not follow the actual species phylogeny (e.g., Doyle, 1992; Maddison, 1997). Further tests using other loci are needed to confirm the areas where there is discordance between morphology and molecules.
24
1.6. References Adl, S. M., A. G. B. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Browser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, C. E. Lane, L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, R. M. McCourt, L. Mendoza, O. Moestrup, S. E. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52:399-451. Aescht, E., W. Foissner, and M. Mulisch. 1991. Ultrastructure of the mycophagous ciliate Grossglockneria acuta (Ciliophora, Colpodea) and phylogenetic affinities of colpodid ciliates. Eur. J. Protistol 26:350-364. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1993. Current Protocols in Molecular Biology. Wiley-Liss, New York. Bardele, C. F. 1981. Functional and phylogenetic aspects of the ciliary membrane: a comparative freeze-fracture study. Biosystems 14:403-421. Bardele, C. F. 1989. From ciliate ontogeny to ciliate phylogeny: a program. Boll. Zoo. 56:235-243. Bardele, C. F., W. Foissner, and R. L. Blanton. 1991. Morphology, morphogenesis and systematic position of the sorocarp forming ciliate Sorogena stoianovitchae Bardbury & Olive 1980. J. Protozool 38:7-17. Bell, G. 1988. Sex and Death in Protozoa: The History of an Obsession. Cambridge University Press, Cambridge. Bhattacharya, D., T. Friedl, and S. Damberger. 1996. Nuclear-encoded rDNA group I introns: Origin and phylogenetic relationships of insertion site lineages in the green algae. Mol. Biol. Evol. 13:978-989. Bowers, N., T. T. Kroll, and J. R. Pratt. 1998. Diversity and geographic distribution of riboprints from three cosmopolitan species of Colpoda Müller (Ciliophora: Colpodea). Eur. J. Protistol. 34:341-347. Bradbury, P. C., and L. S. Olive. 1980. Fine structure of the feeding stage of a sorogenic ciliate, Sorogena stoianoitchae gen. n. sp. n. J. Protozool. 27:267-277. Cannone, J. J., S. Subramanian, M. N. Schnare, J. R. Collett, L. M. D'Souza, Y. S. Du, B. Feng, N. Lin, L. V. Madabusi, K. M. Muller, N. Pande, Z. D. Shang, N. Yu, and R. R. Gutell. 2002. The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:2.
25
Claff, C. L., V. C. Dewey, and G. W. Kidder. 1941. Feeding mechanisms and nutrition in three species of Bresslaua. Biol. Bull. 81:221-234. Detcheva, R. B. 1976. Particularités ultracrturales du cilié Cyrtolophosis mucicola Stokes, 1885. C. r. Séanc. Soc. Biol. Clermon-Ferrand 170:112-114. Detcheva, R. B., and P. d. Puytorac. 1979. Un nouvel de cilie a micronoyau inclus dans l'enveloppe macronucleaire: le genera Aristerostoma Kahl, 1926. Annls. Stn. Biolog. de Besse 13:247-251. Didier, P., P. Depuytorac, N. Wilbert, and R. Detcheva. 1980. A propos d'observations sur l'ultrastructure de cilié Cyrtolophosis mucicola Stokes, 1885. J. Protozool. 27:72-79. Dini, F., and D. Nyberg. 1993. Sex in ciliates. Adv. Microb. Ecol. 13:85-153. Doyle, J. J. 1992. Gene trees and species trees: molecular systematics as one-character taxonomy. Syst. Bot. 17:144-163. Dragesco, J., and A. Dragesco-Kernéis. 1979. Cilies muscicoles nouveaux ou peu connus. Acta Protozool. 18:401-416. Dragesco, J., G. Fryd-versavel, F. Iftode, and P. Didier. 1977. Le cilie Platyophrya spumacola Kahl, 1926: morphologie, stomatogenèse et ultrastructure. Protistologica 13:419-434. Díaz, S., A. Martin-González, S. Borniquel, and J. C. Gutiérrez. 2000. Cyrtolophosis elongata (Colpodea, Ciliophora): Some aspects of ciliary pattern, division, cortical and nuclear changes during encystment and resting cyst ultrastructure. Eur. J. Protistol. 36:367-378. Eddy, S. R. 2001. HMMER: Profile hidden markov models for biological sequence analysis. http://hmmer.wustl.edu. Foissner, W. 1985. Klassifikation und phylogenie der Colpodea (Protozoa: Ciliophora). Arch. Protistenk. 129:239-290. Foissner, W. 1987. Neue und wenig bekannte hypotriche und colpodide Ciliaten (Protozoa: Ciliophora) aus Böden und Moosen. Zool. Beitr. (N. F.) 31:187-282. Foissner, W. 1993a. Colpodea (Ciliophora). Protozoenfauna 4/1:i-x, 1-798. Foissner, W. 1993b. Corticocolpoda kaneshiroae n. g., n. sp., a new colpodid ciliate (Protozoa, Ciliophora) from the bark of ohia trees in Hawaii. J. Eukaryot. Microbiol. 40:764-775.
26
Foissner, W. 1993c. Idiocolpoda pelobia gen. n., sp. n., a new colpodid ciliate (Protozoa, Ciliophora) from an ephemeral stream in Hawaii. Acta Protozool. 32:175-182. Foissner, W. 1994. Pentahymena Corticicola nov. gen., nov. spec., a new colpodid ciliate (Protozoa, Ciliophora) from bark of acacia trees in Costa Rica. Arch. Protistenk. 144:289-295. Foissner, W. 1995. Tropical protozoan diversity: 80 ciliate species (Protozoa, Ciliophora) in a soil sample from a tropical dry forest of Costa Rica, with description of four new genera and seven new species. Arch. Protistenk. 145:3779. Foissner, W. 1996. Ontogenesis of ciliated protozoa with emphasis on stomatogenesis. Pp. 95-178 in K. Hausmann and P. C. Bradbury, eds. Ciliates: Cells as Organisms. Gustav Fischer, Stuttgart. Foissner, W. 1999. Description of two new, mycophagous soil ciliates (Ciliophora, Colpodea): Fungiphrya strobli n. g., n. sp. and Grossglockneria ovata n. sp. J. Eukaryot. Microbiol. 46:34-42. Foissner, W. 2003. Pseudomaryna australiensis nov gen., nov spec. and Colpoda brasiliensis nov spec., two new colpodids (Ciliophora, Colpodea) with a mineral envelope. Eur. J. Protistol. 39:199-212. Foissner, W., S. Agatha, and B. H. 2002. Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest Africa), with emphasis on two contrasting environments, the Etosha Region and the Namib Desert: Part I. Densia 5:1-1063. Foissner, W., and M. Kreutz. 1998. Systematic position and phylogenetic relationships of the genera Bursaridium, Paracondylostoma, Thylakidium, Bryometopus, and Bursaria (Ciliophora: Colpodea). Acta Protozool. 37:227-240. Foissner, W., M. Struder-Kypke, G. W. M. van der Staay, S. Y. Moon-van der Staay, and J. H. P. Hackstein. 2003. Endemic ciliates (Protozoa, Ciliophora) from tank bromeliads (Bromeliaceae): a combined morphological, molecular, and ecological study. Eur. J. Protistol. 39:365-372. Golder, T. K. 1976. The macro-micronuclear complex of Woodruffia metabolica. J. Ultrastruct. Res. 54:169-175. Grabowski, P. J., A. J. Zaug, and T. R. Cech. 1981. The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of Tetrahymena. Cell 23:467-476.
27
Haugen, P., D. H. Coucheron, S. B. Ronning, K. Haugli, and S. Johansen. 2003. The molecular evolution and structural organization of self-splicing group I introns at position 516 in nuclear SSU rDNA of myxomycetes. J. Eukaryot. Microbiol. 50:283-292. Haugen, P., D. M. Simon, and D. Bhattacharya. 2005. The natural history of group I introns. Trends Genet. 21:111-119. Huelsenbeck, J. P., and F. R. Ronquist. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. Jackson, S. A., J. J. Cannone, J. C. Lee, R. R. Gutell, and S. A. Woodson. 2002. Distribution of rRNA introns in the three-dimensional structure of the ribosome. J. Mol. Biol. 323:35-52. Kahl, A. 1931. Urtiere oder Protozoa I: Wimpertiere oder Ciliate (Infusoria) 2. Holotricha außer den im 1. Teil behandelten Prostomata. Tierwelt Dtl. 21:181398. Kawakami, H. 1991. An endosymbiotic Chlorella-bearing ciliate: Platyophrya chlorelligera Kawakami 1989. Eur. J. Protistol. 26:245-255. Lasek-Nesselquist, E., and L. A. Katz. 2001. Phylogenetic position of Sorogena stoianovitchae and relationships within the class Colpodea (Ciliophora) based on SSU rDNA sequences. J. Eukaryot. Microbiol. 48:604-607. Lynn, D. H. 1976. Comparative ultrastructure and systematics of colpodida. Structural conservatism hypothesis and a description of Colpoda steinii Maupas. J. Protozool. 23:302-314. Lynn, D. H. 1979. Fine structural specializations and evolution of carnivory in Bresslaua (Ciliophora, Colpodida). Trans. Am. Microsc. Soc. 98:353-368. Lynn, D. H. 1981. The organization and evolution of microtubular organelles in ciliated protozoa. Biol. Rev. 56:243-292. Lynn, D. H. 2003. Morphology or molecules: How do we identify the major lineages of ciliates (Phylum Ciliophora)? Eur. J. Protistol. 39:356-364. Lynn, D. H., and E. B. Small. 1997. A revised classification of the phylum Ciliophora Doflein, 1901. Rev. Soc. Mex. Hist. Nat. 47:65-78. Lynn, D. H., and E. B. Small. 2002. Phylum Ciliophora Doflein, 1901. Pp. 371-656 in J. J. Lee, G. F. Leedale and P. C. Bradbury, eds. An Illustrated Guide to the Protozoa, 2nd ed. Society of Protozoologists, Lawrence, Kansas.
28
Lynn, D. H., A.-D. G. Wright, M. Schlegel, and W. Foissner. 1999. Phylogenetic relationships of orders within the class Colpodea (Phylum Ciliophora) inferred from small subunit rRNA gene sequences. J. Mol. Evol. 48:605-614. Maddison, W. P. 1997. Gene trees in species trees. Syst. Biol. 46:523-536. Maddison, W. P., and D. R. Maddison. 2005. MacClade v. 4.0.8. Sinauer Assoc. Mark Welch, D., and M. Meselson. 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288:1211-1215. Mears, J. A., J. J. Cannone, S. M. Stagg, R. R. Gutell, R. K. Agrawal, and S. C. Harvey. 2002. Modeling a minimal ribosome based on comparative sequence analysis. J. Mol. Biol. 321:215-234. Miyake, A. 1996. Fertilization and sexuality in ciliates. Pp. 243-290 in K. Hausmann and P. C. Bradbury, eds. Ciliates: Cells as Organisms. Gustav Fischer, Stuttgart. Nanney, D. L., C. Park, R. Preparata, and E. M. Simon. 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. Njine, T. 1979. Etude ultrastructurale de cilié Kuklikophyra dragescoi gen. n., sp. n. J. Protozool. 26:589-598. Normark, B. B., O. P. Judson, and N. A. Moran. 2003. Genomic signatures of ancient asexual lineages. Biol. J. Linn. Soc. 79:69-84. Nylander, J. A. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Center, Uppsala University Page, R. D. 1996. TREEVIEW: An application to display phylogenetic tress on personal computers. Comput. Appl. Biosci. 12:357-358. Puytorac, P. d. 1994. Phylum Ciliophora Doflein, 1901. Pp. 1-15 in P. P. de, ed. Traité de Zoologie, Tome II, Infusoires Ciliés, Fasc. 2, Systématique. Masson, Paris. Puytorac, P. d., M. R. Kattar, C. A. Grolière, and I. d. Silva Neto. 1992. Polymorphism and ultrastructure of the colpodean ciliate of the genus Platyophryides Foissner, 1987. J. Protozool. 39:154-159. Raikov, I. B. 1982. The Protozoan Nucleus: Morphology and Evolution. SpringerVerlag, Wien.
29
Simon, D., J. Moline, G. Helms, T. Friedl, and D. Bhattacharya. 2005. Divergent histories of rDNA group I introns in the lichen family Physciaceae. J. Mol. Evol. 60:434-446. Small, E. B., and D. H. Lynn. 1981. A new macrosystem for the phylum Ciliophora Doflein, 1901. Biosystems 14:387-401. Snoeyenbos-West, O. L. O., J. Cole, A. Campbell, D. W. Coats, and L. A. Katz. 2004. Molecular phylogeny of phyllopharyngean ciliates and their group I introns. J. Eukaryot. Microbiol. 51:441-450. Snoeyenbos-West, O. L. O., T. Salcedo, G. B. McManus, and L. A. Katz. 2002. Insights into the diversity of choreotrich and oligotrich ciliates (Class: Spirotrichea) based on genealogical analyses of multiple loci. Int. J. Syst. Evol. Microbiol. 52:19011913. Sonneborn, T. M. 1957. Breeding systems, reproductive methods, and species problems in protozoa. Pp. 155-324 in E. Mayr, ed. The Species Problem. American Association for the Advancement of Science, Washington D. C. Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. Stechmann, A., M. Schlegel, and D. H. Lynn. 1998. Phylogenetic relationships between Prostome and Colpodean ciliates tested by small subunit rRNA sequences. Mol. Phyl. Evol. 9:48-54. Swofford, D. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Assoc, Sunderland MA. Wikmark, O.-G., P. Haugen, E. W. Lundblad, K. Haugli, and S. D. Johansen. 2007. The molecular evolution and structural organization of group I introns at position 1389 in nuclear small subunit rDNA of myxomycetes. J. Eukaryot. Microbiol. 54:4956.
30
Table 1.1. Taxon sampling within the Colpodea. Species were identified using silver impregnation by W. Foissner. Type and voucher material of the new species and the newly investigated populations are deposited at the Oberoesterreichische Landesmuseum in Linz (LI), Austria. nc - non-clonal culture, c- clonal culture, npc - non-pure culture, pc - pure culture.
31
Table 1.2. Pairwise distance between collections for species sampled more than once. Pairwise Taxon Collection site distance (%) Bresslauides discoideus Dominican Republic 1 and 2 0 Colpoda cucullus Malaysia and Niger 0.47 Cyrtolophosis mucicola Brazil 1 and 2 0 Cyrtolophosis mucicola Brazil 1 and Austria 1.71 Ilsiella palustris Brazil and Hawaii 0.64
32
Figure 1.1. Evolution among some morphological characters within the class Colpodea. (A) Hypotheses of relationships among orders and morphological character evolution modified from Foissner (1993a), where some characters are removed. (B) Possible alternative evolution of characters mapped out on the SSU rDNA gene tree found here; the deeper nodes in the Colpodea are not well supported and are thus shown as a polytomy. The character are: 1) Lkm fiber, pleurotelokinetal stomatogenesis, brickshaped adoral organelles, flat vesitibulum, and ‘kreyellid,’ ‘platyophryid,’ or ‘colpodid’ silverline pattern; 2) ‘kreyellid’ silverline pattern; 3) ‘platyophrid’ or ‘colpodid’ silverline pattern; 4) shared micronuclear and macronuclear outer membrane of the nuclear envelope; 5) aerial sorocarps; 6) ‘colpodid’ silverline pattern; 7) deep vestibulum, 8) paroral formation with radial ciliary fields; 9) equidistantly spaced adoral organelles; 10) conjugation; 11) emergence pore in resting cysts; 12) merotelokinetal stomatogenesis; 13) feeding tube; 14) one paroral membrane segment; 15) two paroral membrane segments; 16) postoral pseudomembrane. See text for explanations of characters.
33
34
Figure 1.2. SSU rDNA genealogy of the class Colpodea and potential sister classes. The most likely Bayesian tree is shown. Bayesian posterior probability support is shown by differences in thickness of branches. Numerical values from bootstrap support is shown next to the branches as: MP bootstrap/ML bootstrap. Values ∇ exhibiting intramacronuclear microtubules (Tetrahymena thermophila Nanney and McCoy 1976).
Etymology: Derived from the Latin intra (within), Greek makros (large), and Latin nucleus (kernel), in reference to the presence of intramacronuclear microtubules during cell division (see Diagnostic Apomorphies).
Reference Phylogeny: The primary reference phylogeny is Hammerschmidt et al. Hammerschmidt et al. (1996: Fig. 2). See also Hirt et al. (1995: Fig. 2) and Yoon et al. (2008: Fig. 2).
Composition: The majority of clades within the Ciliophora, as defined in this volume, are within the Intramacronucleata. Lynn (2008) lists the following taxa as included in the Intramacronucleata: Armophorea, Colpodea, Litostomatea, Nassophorea, Oligohymenophorea, Phyllopharyngea, Plagiopylea, Prostomatea, and Spirotrichea.
184
Diagnostic Apomorphies: The most distinctive diagnostic apomorphy is the presence of microtubules within the macronuclear envelope during nuclear division. In other Ciliophora (i.e. Postciliodesmotophora), microtubules are either extra-macronuclear, or macronuclei do not divide.
Synonyms: None
Comments: Lynn (1996) established this taxon, which contains most known ciliates, based on small subunit ribosomal RNA gene phylogenies as well as the presence of intranuclear microtubules in dividing macronuclei. Monophyly of this clade is strongly supported, but internal relationships are unresolved (Lynn 2008).
185
7.5.4. Colpodea E. B. Small & D. H. Lynn 1981 [M. Dunthorn & D. H. Lynn 2009], converted clade name
Definition: The most inclusive clade exhibiting a LKm fiber (as described below under Diagnostic Apomorphies) synapomorphic with that in Colpoda cucullus O. F. Müller (1773) K. C. Gmelin 1790. This is an apomorphy-modified node-based definition in which the specifier is extant; it is intended to apply to a crown clade. Abbreviated definition: >∇ exhibiting a LKm fiber (Colpoda cucullus O. F. Müller (1773) K. C. Gmelin 1790).
Etymology: Derived from the Greek kolpus (womb).
Reference Phylogeny: The primary reference phylogeny is Dunthorn et al. (2008: Fig. 2). See also Dunthorn et al. (2009), and Lynn et al. (1999).
Composition: All taxa listed in Foissner (1993) and Lynn (2008).
Diagnostic Apomorphies: The most distinctive diagnostic apomorphy of the Colpodea is the LKm fiber (=transversodesmal fiber) composed of overlapping transverse ribbons of microtubules extending from the posterior kinetosome (= eukaryotic basal body) of the somatic dikinetids (Foissner 1993; Lynn 2008). The Colpodea also have: somatic stomatogenesis, where parental oral structures are partially to completely reorganized during cell division; and a reticulate silverline system.
186
Synonyms: None.
Comments: Using the structural conservatism hypothesis (Lynn 1976, 1981), Small and Lynn (1981) brought once disparate taxa together into the Colpodea. The Colpodea was expanded by Foissner (1985), who later monographed the group (Foissner 1993). Bardele (1989) rejects the monophyly of the taxon based on the presence or absence of ciliary plaques, but there is no support for this claim (Lynn et al. 1999; Dunthorn et al. 2008). Monophyly of the Colpodea is currently neither supported nor rejected by small subunit ribosomal DNA sequences (Dunthorn et al. 2008).
187
7.6. References Adl, S. M., B. S. Leander, A. G. B. Simpson, S. B. Archibald, O. R. Anderson, D. Bass, S. S. Bowser, G. Brugerolle, M. A. Farmer, S. Karpov, M. Kolisko, C. E. Lane, D. J. Lodge, D. G. Mann, R. Meisterfeld, L. Mendoza, Ø. Moestrup, S. E. Mozley-Standridge, A. V. Smirnov, and F. Spiegel. 2007. Diversity, nomenclature, and taxonomy of protists. Syst. Biol. 56:684-689. APG II. 2003. An update of the Angiosperm Phylogeny Group classification for the oders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141:399-436. Baldauf, S. L., A. J. Roger, I. Wenk-Siefert, and W. F. Doolittle. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972-977. Bardele, C. F. 1989. From ciliate ontogeny to ciliate phylogeny: a program. Boll. Zool. 56:235-243. Barkley, T. M., P. DePriest, V. Funk, R. W. Kiger, W. J. Kress, and G. Moore. 2004. Linnaean nomenclature in the 21st Century: A report from a workshop on integrating traditional nomenclature and phylogenetic classification. Taxon 53:153-158. Benton, M. J. 2000. Stems, nodes, crown clades, and rank-free lists: Is Linnaeus dead? Biol. Rev. 75:633-648. Berger, H. 1999. Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biol. 78:i-xii, 1-1080. Berger, H. 2006. Monograph of the Urostyloidea (Ciliophora, Hypotrichia). Monographiae Biol. 85:i-xv, 1-1303. Bertrand, Y., and M. Härlin. 2006. Stability and universality in the application of taxon names in phylogenetic nomenclature. Syst. Biol. 55:848-858. Brothers, D. J. 1983. Nomenclature at the ordinal and higher levels. Syst. Zool. 32:34-42. Brummitt, R. K. 2003. Further dogged defense of paraphyletic taxa. Taxon 52:803-804. Bryant, H. N. 1994. Comments on the phylogenetic definitions of taxon names and conventions regarding the naming of crown clades. Syst. Biol. 43:124-130. Bryant, H. N., and P. D. Cantino. 2002. A review of criticisms of phylogenetic nomenclature: Is taxonomic freedom the fundamental issue? Biol. Rev. 77:39-55. Bütschli, O. 1887-1889. Protozoa. Abt. III. Infusoria und System der Radiolaria in H. G. Bronn, ed. Klassen und Ordnungen de Thier-Reichs, Vol. I. C. F. Winter, Leipzig.
188
Cantino, P. D., and K. de Queiroz. 2007. International Code of Phylogenetic Nomenclature. Version 4b [http://www.ohiou.edu/phylocode/]. Cantino, P. D., J. A. Doyle, S. W. Graham, W. S. Judd, R. G. Olmstead, D. E. Soltis, P. S. Soltis, and M. J. Donoghue. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56:E1-E44. Cantino, P. D., R. G. Olmstead, and S. J. Wagstaff. 1997. A comparison of phylogenetic nomenclature with the current system: A botanical case study. Syst. Biol. 46:313331. Carpenter, J. M. 2003. Critique of pure folly. Bot. Rev. 69:79-92. Cavalier-Smith, T. 1999. Zooflagellate phylogeny and the systematics of Protozoa. Biol. Bull. 196:393-396. Cavalier-Smith, T. 2004. Only six kingdoms of life. Proc. R. Soc. Lond. B 271:12511262. Cavalier-Smith, T. 2007. Evolution and relationships of algae: major branches of the tree of life. Pp. 21-55 in J. Brodie, and J. Lewis, eds. Unravelling the algae: the past, present, and future of algal systematics. CRC Press, Boca Raton. Corliss, J. O. 1972. Common sense and courtesy in nomenclatural taxonomy. Syst. Zool. 21:117-122. Corliss, J. O. 1979. The ciliated protozoa: characterization, classification and guide to the literature. Pergamon Press, Oxford. Corliss, J. O. 1983. Consequences of creating new kingdoms of organisms. Bioscience 33:314-318. de Queiroz, K. 1997. The Linnaean hierarchy and the evolutionatization of taxonomy, with emphasis on the problem of nomenclature. Aliso 15:125-144. de Queiroz, K. 2006. The Phylocode and the distinction between taxonomy and nomenclature. Syst. Biol. 55:160-162. de Queiroz, K. 2007. Toward an intergrated system of clade names. Syst. Biol. 956-974. de Queiroz, K., and J. Gauthier. 1990. Phylogeny as a central principle in taxonomy: phylogenetic definitions of taxon names. Syst. Biol. 39:307-322. de Queiroz, K., and J. Gauthier. 1992. Phylogenetic taxonomy. Annual Review Of Ecology And Systematics 23:449-480. de Queiroz, K., and J. Gauthier. 1994. Toward a phylogenetic system of biological nomenclature. Trends Ecol. Evol. 9:27-31.
189
Dominguez, E., and Q. D. Wheeler. 1997. Taxonomic stability is ignorance. Cladistics 13:367-372. Donoghue, M. J., T. Eriksson, P. A. Reeves, and R. G. Olmstead. 2001. Phylogeny and phylogenetic taxonomy of Dipsacales with special reference to Sinadoxa and Tetradoxa (Adoxaceae). Harv. Pap. Bot. 6:459-479. Dubois, A. 2005. Proposed Rules for the incorporation of nomina of higher-ranked zoological taxa in the International Code of Zoological Nomenclature. 1. Some general questions, concepts and terms of biological nomenclature. Zoosystema 27:365-426. Dubois, A. 2006. Proposed Rules for the incorporation of nomina of higher-ranked zoological taxa in the International Code of Zoological Nomenclature. 2. The proposed Rules and their rationale. Zoosystema 28:165-258. Dundee, H. A. 1989. Higher category name usage for amphibians and reptiles. Syst. Zool. 38:398-406. Dunthorn, M., M. Eppinger, M. V. J. Schwarz, M. Schweikert, J. Boenigk, L. A. Katz, and T. Stoeck. 2009. Phylogenetic placement of the Cyrtolophosididae Stokes, 1888 (Ciliophora; Colpodea) and neotypification of Aristerostoma marinum Kahl, 1931. Int. J. Syst. Evol. Microbiol. 59:167-180. Dunthorn, M., W. Foissner, and L. A. Katz. 2008. Molecular phylogenetic analysis of class Colpodea (phylum Ciliophora) using broad taxon sampling. Mol. Phylogenet. Evol. 48:316-327. Dyke, G. J. 2002. Should paleontologists use "phylogenetic" nomenclature? J. Paleontol. 76:793-796. Faivovich, J., C. F. B. Haddad, P. C. A. Garcia, D. R. Frost, J. A. Campbell, and W. C. Wheeler. 2005. Systematic review of the frog family Hylidae, with special reference to Hylinae: a phylogenetic analysis and taxonomic revisison. Bull. Amer. Mus. Nat. Hist. 294. Farris, J. S. 1974. Formal definitions of paraphyly and polyphyly. Syst. Zool. 23:548-554. Foissner, W. 1985. Klassifikation und phylogenie der Colpodea (Protozoa: Ciliophora). Arch. Protistenk. 129:239-290. Foissner, W. 1993. Colpodea (Ciliophora). Protozoenfauna 4/1:i-x, 1-798. Gerassimova, Z. P., and L. N. Seravin. 1976. Ectoplasmic fibrillar system of Infusoria and its role for the understanding of their phylogeny. Zool. Zh. 55:645-656. Ghiselin, M. T. 1977. On changing the names of higher taxa. Syst. Zool. 26:346-349.
190
Hammerschmidt, B., M. Schlegel, D. Lynn, D. D. Leipe, M. L. Sogin, and I. B. Raikov. 1996. Insights into the evolution of nuclear dualism in the ciliates revealed by phylogenetic analysis of rRNA sequences. J. Eukaryot. Microbiol. 43:225-230. Hemming, F., ed. 1953. Copenhagen decisions on zoological nomenclature, addirions to, and modeifications of, the Règles internationales de la nomenclature zoologique; approved and adapted by the 14th International Congress of Zoology, Copenhagen, August, 1953. International Trust for Zoological Nomenclature, London. Hennig, W. 1966. Phylogenetic systematics. University of Illinois Press, Urbana. Heywood, V. H., R. K. Brummitt, A. Culham, and O. Seberg. 2007. Flowering Plant Families of the World. Firefly Books, Ontario, Canada. Hibbett, D. S., and M. J. Donoghue. 1998. Intergrating phylogenetic analysis and classification in fungi. Mycologia 90:347-356. Hirt, R. P., P. L. Dyal, M. Wilkinson, B. J. Finlay, D. M. Roberts, and T. M. Embley. 1995. Phylogenetic relationships among Karyorelictids and Heterotrichs inferred from small subunit rRNA sequences: resolution at the base of the ciliate tree. Mol. Phylogenet. Evol. 4:77-87. Hörandl, E. 2007. Neglecting evolution is bad taxonomy. Taxon 56:1-5. International Commission on Zoological Nomenclature. 1999. International Code of Zoological Nomenclature, 4th ed. The International Trust for Zoological Nomenclature, London. Jankowski, A. W. 2007. Phylum Ciliophora Doflein, 1901. Pp. 415-993 in A. F. Alimov, ed. Protista. Part 2, Handbook of Zoology. Russian Academy of Sciences, Zoological Institure, St. Petersburg. Joyce, W. G., J. F. Parham, and J. A. Gauthier. 2004. Developing a protocol for the conversion of rank-based taxon names to phylogenetically defined clade names, as exemplified by turtles. J. Paleontol. 78:989-1013. Kahl, A. 1926. Neue und wenig bekannte Formen der holotrichen und heterotrichen Ciliaten. Arch. Protistenk. 55:197-438. Kahl, A. 1930-1935. Urtiere oder Protozoa. I: Wimpertiere oder Ciliata (Infusoria), eine Bearbeitung der freilebenden und ectocommensalen Infusorien der Erde, unter Ausschluss der marinen Tintinnidae. Pp. 1-886 in F. Dahl, ed. Die Teirwelt Deutschlands. G. Fischer, Jena. Kahl, A. 1931. Urtiere oder Protozoa I: Wimpertiere oder Ciliate (Infusoria) 2. Holotricha außer den im 1. Teil behandelten Prostomata. Tierwelt Dtl. 21:181-398.
191
Keller, R. A., R. N. Boyd, and Q. D. Wheeler. 2003. The illogical basis of phylogenetic nomenclature. Bot. Rev. 69:93-110. Kojima, J. 2003. Apomorphy-based definition also pinpoints a node, and PhyloCode names prevent effective communication. Bot. Rev. 69:44-58. Laurin, M., K. de Queiroz, and P. D. Cantino. 2006. Sense and stability of taxon names. Zoologica Scripta 35:113-114. Lee, M. S. Y. 1996. Stability in meaning and content of taxon names: an evaluation of crown clade definitions. Proc. R. Soc. Lond. B 263:1103-1109. Lee, M. S. Y. 2001. On recent arguments for phylogenetic nomenclature. Taxon 50:175180. Lynn, D. H. 1976. Comparative ultrastructure and systematics of colpodida. Structural conservatism hypothesis and a description of Colpoda steinii Maupas. J. Protozool. 23:302-314. Lynn, D. H. 1981. The organization and evolution of microtubular organelles in ciliated protozoa. Biol. Rev. 56:243-292. Lynn, D. H. 1996. My journey in ciliate systematics. J. Eukaryot. Microbiol. 43:253-260. Lynn, D. H. 2008. The ciliated protozoa: characterization, classification, and guide to the literature, 3rd edition. Springer, Dordrecht. Lynn, D. H., and E. B. Small. 2002. Phylum Ciliophora Doflein, 1901. Pp. 371-656 in J. J. Lee, G. F. Leedale, and P. C. Bradbury, eds. An illustrated guide to the protozoa, 2nd ed. Society of Protozoologists, Lawrence, Kansas. Lynn, D. H., A. D. G. Wright, M. Schlegel, and W. Foissner. 1999. Phylogenetic relationships of orders within the class Colpodea (phylum Ciliophora) inferred from small subunit rRNA gene sequences. J. Mol. Evol. 48:605-614. Matthes, D. 1988. Suctoria und Urceolariidae. Protozoenfauna 7/1:i-ix, 1-309. Mayr, E. 1998. Two empires or three? Proc. Natl. Acad. Sci., USA 95:9720-9723. Mayr, E., and W. J. Bock. 2002. Classifications and other ordering systems. J. Zoo. Syst. Evol. Research 40:169-194. Modesto, S. P., and J. S. Anderson. 2004. The phylogenetic definition of Reptilia. Syst. Biol. 53:815-821. Moore, G. 1998. A comparison of traditional and phylogenetic nomenclature. Taxon 47:561-579. Moore, G. 2003. Should taxon names be explicitly defined? Bot. Rev. 69:2-21. 192
Nixon, K. C., and J. M. Carpenter. 2000. On the other "phylogenetic systematics". Cladistics 16:298-318. Nixon, K. C., J. M. Carpenter, and D. W. Stevenson. 2003. The PhyloCode is fatally flawed, and the "Linnaean" system can easily be fixed. Bot. Rev. 69:111-120. Nordal, H., and B. Stedje. 2005. Paraphyletic taxa should be accepted. Taxon 54:5-6. Pleijel, F., and G. W. Rouse. 2003. Ceci n'est pas une pipe: names, clades and phylogenetic nomenclature. J. Zool. Syst. Evol. Research 41:162-174. Polaszek, A., and E. O. Wilson. 2005. Sense and stability in animal names. Trends Ecol. Evol. 20:421-422. Puytorac, P. d. 1994. Phylum Ciliophora Doflein, 1901. Pp. 1-15 in P. P. de, ed. Traité de Zoologie, Tome II, Infusoires Ciliés, Fasc. 2, Systématique. Masson, Paris. Puytorac, P. d., A. Batisse, J. Bohatier, J. O. Corliss, G. Deroux, P. Didier, J. Dragesco, G. Fryd-Versavel, J. Grain, C.-A. Groliére, F. Iftode, M. Laval, M. Roque, A. Savoie, and M. Tuffrau. 1974. Proposition d'une classification du phylum Ciliophora Doflein, 1901. C.R. Acad. Sci. Paris 278:2799-2802. Raikov, I. B. 1996. Nuclei of ciliates. Pp. 221-242 in K. Hausmann, and P. C. Bradbury, eds. Ciliates: cells as organisms. Gustav Fischer, Stuttgart. Sangster, G. 2005. A name for the clade formed by owlet-nightjars, swifts and hummingbirds (Aves). Zootaxa:1-6. Schander, C., and M. Thollesson. 1995. Phylogenetic Taxonomy―Some Comments. Zool. Scr. 24:263-268. Schuh, R. 2003. The Linnaean system and its 250-year persistence. Bot. Rev. 69:59-78. Sereno, P. C. 1999. Definitions in phylogenetic taxonomy: Critique and rationale. Syst. Biol. 48:329-351. Sereno, P. C. 2005. The logical basis of phylogenetic taxonomy. Systematic Biology 54:595-619. Small, E. B., and D. H. Lynn. 1981. A new macrosystem for the phylum Ciliophora Doflein, 1901. Biosystems 14:387-401. Sosef, M. S. M. 1997. Hierarchical models, reticulate evolution and the inevitability of paraphyletic supraspecific taxa. Taxon 46:75-85. Stefanovic, S., D. F. Austin, and R. G. Olmstead. 2003. Classification of Convolvulaceae: A phylogenetic approach. Syst. Bot. 28:791-806.
193
Taylor, M. P., and D. Naish. 2005. The phylogenetic taxonomy of Diplodocoidea (Dinosauria: Sauropoda). PaleoBios 25:1-7. Thorne, R. F. 2000. The classification and geography of the flowering plants: Dicotyledons of the class angiospermae (Subclasses magnoliidae, ranunculidae, caryophyllidae, dilleniidae, rosidae, asteridae, and lamiidae). Botanical Review 66:441-647. Wenzel, J. W., K. C. Nixon, and G. Cuccudoro. 2004. Dites non au PhyloCode! Bull. Soc. Fr. Syst. 31:19-23. Wu, Z. Y., A. M. Lu, Y. C. Tang, Z. D. Chen, and D. Z. Li. 2002. Synopsis of a new "polyphyletic-polychronic-polytopic" system of the angiosperms. Acta Phytotax. Sin. 40:2289-2322. Yoon, H. S., J. Grant, Y. I. Tekle, M. Wu, B. C. Chaon, J. C. Cole, J. M. Logsdon, D. J. Patterson, D. Bhattacharya, and L. A. Katz. 2008. Broadly sampled multigene trees of eukaryotes. BMC Evol. Biol. 8:14.
194
BIBLIOGRAPHY
Adl, S. M., B. S. Leander, A. G. B. Simpson, S. B. Archibald, O. R. Anderson, D. Bass, S. S. Bowser, G. Brugerolle, M. A. Farmer, S. Karpov, M. Kolisko, C. E. Lane, D. J. Lodge, D. G. Mann, R. Meisterfeld, L. Mendoza, Ø. Moestrup, S. E. Mozley-Standridge, A. V. Smirnov, and F. Spiegel. 2007. Diversity, nomenclature, and taxonomy of protists. Syst. Biol. 56:684-689. Adl, S. M., A. G. B. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Browser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, C. E. Lane, L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, R. M. McCourt, L. Mendoza, Ø. Moestrup, S. E. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52:399-451. Aescht, E., W. Foissner, and M. Mulisch. 1991. Ultrastructure of the mycophagous ciliate Grossglockneria acuta (Ciliophora, Colpodea) and phylogenetic affinities of colpodid ciliates. Eur. J. Protistol 26:350-364. Affa'a, F. M., D. A. Hickey, M. Strüder-Kypke, and D. H. Lynn. 2004. Phylogenetic position of species in the genera Anoplophrya, Plagiotoma, and Nyctotheroides (Phylum Ciliophora), endosymbiotic ciliates of annelids and anurans. J. Eukaryot. Microbiol. 51:301-306. Agatha, S. 2004a. A cladistic approach for the classification of oligotrichid ciliates (Ciliophora: Spirotricha). Acta Protozool. 43:201-217. Agatha, S. 2004b. Evolution of ciliary patterns in the oligotrichida (Ciliophora, Spirotricha) and its taxonomic implications. Zoology 107:153-168. Agatha, S., and W. Foissner. 2009. Conugation in the spirotrich ciliate Halteria grandinella (Müller, 1773) Dujardin, 1841 (Protozoa, Ciliophora) and its phylogenetic implications. Eur. J. Protistol. 45:51-63. Agatha, S., and M. Strüder-Kypke. 2007. Phylogeny of the order Choreotrichida (Ciliophora, Spriotricha, Oligotrichea) as inferred from morphology, ultrastructure, ontogenesis, and SSrRNA sequences. Europ. J. Protistol. 43:37-63. Anderson, F. E., and D. L. Swofford. 2004. Should we be worried about long-branch attraction in real data sets? Investigations using metazoan 18S rDNA. Mol. Phylogenet. Evol. 33:440-451. APG II. 2003. An update of the Angiosperm Phylogeny Group classification for the oders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141:399-436.
195
Ardell, D. H., C. A. Lozupone, and L. F. Landweber. 2003. Polymorphism, recombination and alternative unscrambling in the DNA polymerase alpha gene of the ciliate Stylonychia lemnae (Alveolata, class Spirotrichea). Genetics 165:1761-1777. Arkhipova, I., and M. Meselson. 2000. Transposable elements in sexual and ancient asexual taxa. Proc. Natl. Acad. Sci. USA 97:14473-14477. Arkhipova, I., and M. Meselson. 2004. Deleterious transposable elements and the extinction of asexuals. Bioessays 27:76-85. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1993. Current Protocols in Molecular Biology. Wiley-Liss, New York. Baldauf, S. L., A. J. Roger, I. Wenk-Siefert, and W. F. Doolittle. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972-977. Bardele, C. F. 1981. Functional and phylogenetic aspects of the ciliary membrane: a comparative freeze-fracture study. Biosystems 14:403-421. Bardele, C. F. 1989. From ciliate ontogeny to ciliate phylogeny: a program. Boll. Zool. 56:235-243. Bardele, C. F., W. Foissner, and R. L. Blanton. 1991. Morphology, morphogenesis and systematic position of the sorocarp forming ciliate Sorogena stoianovitchae Bardbury & Olive 1980. J. Protozool 38:7-17. Barkley, T. M., P. DePriest, V. Funk, R. W. Kiger, W. J. Kress, and G. Moore. 2004. Linnaean nomenclature in the 21st Century: A report from a workshop on integrating traditional nomenclature and phylogenetic classification. Taxon 53:153-158. Barth, D., S. Krenek, S. I. Fokin, and T. U. Berendonk. 2006. Intraspecific genetic variation in Paramecium revealed by cytochrome c oxidase I sequences. J. Eukaryot. Microbiol. 53:20-25. Barth, D., K. Tischer, H. Berger, M. Schlegel, and T. U. Berendonk. 2008. High mitochondrial haplotype diversity of Coleps sp. (Ciliophora: Prostomatida). Environ. Microbiol. 10:626-634. Bell, G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, Berkeley. Bell, G. 1988. Sex and death in protozoa: the history of an obsession. Cambridge University Press, Cambridge. Benton, M. J. 2000. Stems, nodes, crown clades, and rank-free lists: Is Linnaeus dead? Biol. Rev. 75:633-648.
196
Berger, H. 1999. Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biol. 78:i-xii, 1-1080. Berger, H. 2006. Monograph of the Urostyloidea (Ciliophora, Hypotrichia). Monographiae Biol. 85:i-xv, 1-1303. Berger, H., K. A. S. Al-Rasheid, and W. Foissner. 2006. Morphology and cell division of Saudithrix terricola n. gen., n. sp., a large, stichotrich ciliate from Saudi Arabia. J. Eukaryot. Microbiol. 53:260-268. Berger, H., and W. Foissner. 1997. Cladistic relationships and generic characterization of oxytrichid hypotrichs (Protozoa, Ciliophora). Arch. Protistenk. 148:125-155. Bergsten, J. 2005. A review of long-branch attraction. Cladistics 21:163-193. Bertrand, Y., and M. Härlin. 2006. Stability and universality in the application of taxon names in phylogenetic nomenclature. Syst. Biol. 55:848-858. Bhattacharya, D., T. Friedl, and S. Damberger. 1996. Nuclear-encoded rDNA group I introns: Origin and phylogenetic relationships of insertion site lineages in the green algae. Mol. Biol. Evol. 13:978-989. Bicknell, R. A., N. K. Borst, and A. M. Koltunow. 2000. Monogenic inheritance of apomixis in two Hieracium species with distinct developmental mechanisms. Heredity 84:228-237. Birky, C. W. 1996. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144:427-437. Birky, C. W. 2005. Sex: is Giardia doing in the dark? Curr. Biol. 15:R56-R58. Bowers, N., T. T. Kroll, and J. R. Pratt. 1998. Diversity and geographic distribution of riboprints from three cosmopolitan species of Colpoda Müller (Ciliophora: Colpodea). Europ. J. Protistol. 34:341-347. Bradbury, P. C., and L. S. Olive. 1980. Fine structure of the feeding stage of a sorogenic ciliate, Sorogena stoianovitchae gen. n., sp. n. J. Protozool. 27:267-277. Brothers, D. J. 1983. Nomenclature at the ordinal and higher levels. Syst. Zool. 32:34-42. Brummitt, R. K. 2003. Further dogged defense of paraphyletic taxa. Taxon 52:803-804. Bryant, H. N. 1994. Comments on the phylogenetic definitions of taxon names and conventions regarding the naming of crown clades. Syst. Biol. 43:124-130. Bryant, H. N., and P. D. Cantino. 2002. A review of criticisms of phylogenetic nomenclature: Is taxonomic freedom the fundamental issue? Biol. Rev. 77:39-55. Bull, J. J., and E. L. Charnov. 1985. On irreversible evolution. 39:1149-1155. 197
Burt, A. 2000. Sex, recombination, and the efficacy of natural selection — was Weisman right? Evolution 54:337-351. Bütschli, O. 1887-1889. Protozoa. Abt. III. Infusoria und System der Radiolaria in H. G. Bronn, ed. Klassen und Ordnungen de Thier-Reichs, Vol. I. C. F. Winter, Leipzig. Cannone, J. J., S. Subramanian, M. N. Schnare, J. R. Collett, L. M. D'Souza, Y. S. Du, B. Feng, N. Lin, L. V. Madabusi, K. M. Muller, N. Pande, Z. D. Shang, N. Yu, and R. R. Gutell. 2002. The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:2. Cantino, P. D., and K. de Queiroz. 2007. International Code of Phylogenetic Nomenclature. Version 4b [http://www.ohiou.edu/phylocode/]. Cantino, P. D., J. A. Doyle, S. W. Graham, W. S. Judd, R. G. Olmstead, D. E. Soltis, P. S. Soltis, and M. J. Donoghue. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56:E1-E44. Cantino, P. D., R. G. Olmstead, and S. J. Wagstaff. 1997. A comparison of phylogenetic nomenclature with the current system: A botanical case study. Syst. Biol. 46:313331. Carpenter, J. M. 2003. Critique of pure folly. Bot. Rev. 69:79-92. Catania, F., F. Wurmser, A. A. Potekhin, E. Przyboś, and M. Lynch. 2008. Genetic diversity in the Paramecium aurelia species complex. Mol. Bio. Evol. 26:421431. Cavalier-Smith, T. 1999. Zooflagellate phylogeny and the systematics of Protozoa. Biol. Bull. 196:393-396. Cavalier-Smith, T. 2004. Only six kingdoms of life. Proc. R. Soc. Lond. B 271:12511262. Cavalier-Smith, T. 2007. Evolution and relationships of algae: major branches of the tree of life. Pp. 21-55 in J. Brodie, and J. Lewis, eds. Unravelling the algae: the past, present, and future of algal systematics. CRC Press, Boca Raton. Ceplitis, A. 2003. Coalescence times and the Meselson effect in asexual eukaryotes. Genet. Res. 82:183-190. Chantangsi, C., D. H. Lynn, M. T. Brandl, J. C. Cole, N. Hetrick, and P. Ikonomi. 2007. Barcoding ciliates: a comprehensive study of 75 isolates of the genus Tetrahymena. Int. J. Syst. Evol. Microbiol. 57:2412-2425.
198
Chao, A., P. C. Li, S. Agatha, and W. Foissner. 2006. A statistical approach to estimate soil ciliate diversity and distribution based on data from five continents. Oikos 114:479-493. Chapman, H., G. J. Houliston, B. Robson, and I. Iline. 2003. A case of reversal: the evolution and maintenance of sexuals from parthenogenetic clones in Hieracium pilosella. Int. J. Plant Sci. 164:719-728. Claff, C. L., V. C. Dewey, and G. W. Kidder. 1941. Feeding mechanisms and nutrition in three species of Bresslaua. Biol. Bull. 81:221-234. Collin, R., and M. P. Miglietta. 2008. Reversing opinions on Dollo's Law. Trends Ecol. Evol. 23:602-609. Corliss, J. O. 1961. The ciliated protozoa: Characteriszation, classification, and guide to the literature. Pergamon Press, London. Corliss, J. O. 1972. Common sense and courtesy in nomenclatural taxonomy. Syst. Zool. 21:117-122. Corliss, J. O. 1979. The ciliated protozoa: characterization, classification and guide to the literature. Pergamon Press, Oxford. Corliss, J. O. 1983. Consequences of creating new kingdoms of organisms. Bioscience 33:314-318. Cummings, M. P., and A. Meyer. 2005. Magic bullets and golden rules: data sampling in molecular phylogenetics. Zoology 108:329-336. Dacks, J., and A. J. Roger. 1999. The first sexual lineage and the relevance of facultative sex. J. Mol. Evol. 48:779-783. de Pinna, M. G. G. 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367-394. de Queiroz, K. 1997. The Linnaean hierarchy and the evolutionatization of taxonomy, with emphasis on the problem of nomenclature. Aliso 15:125-144. de Queiroz, K. 2006. The Phylocode and the distinction between taxonomy and nomenclature. Syst. Biol. 55:160-162. de Queiroz, K. 2007. Toward an intergrated system of clade names. Syst. Biol. 956-974. de Queiroz, K., and J. Gauthier. 1990. Phylogeny as a central principle in taxonomy: phylogenetic definitions of taxon names. Syst. Biol. 39:307-322. de Queiroz, K., and J. Gauthier. 1992. Phylogenetic taxonomy. Annual Review Of Ecology And Systematics 23:449-480.
199
de Queiroz, K., and J. Gauthier. 1994. Toward a phylogenetic system of biological nomenclature. Trends Ecol. Evol. 9:27-31. Detcheva, R. B. 1976. Particularités ultracrturales du cilié Cyrtolophosis mucicola Stokes, 1885. C. r. Séanc. Soc. Biol. Clermon-Ferrand 170:112-114. Detcheva, R. B. 1982. Recherches, en Bulgarie, sur les cilies de certaines plages de la Mer Niore et des rivieres y aboutissant. Annls. Stn. limnol. Besse 15:231-253. Detcheva, R. B., and P. d. Puytorac. 1979. Un nouvel de cilie a micronoyau inclus dans l'enveloppe macronucleaire: le genera Aristerostoma Kahl, 1926. Annls. Stn. limnol. Besse 13:247-251. Díaz, S., A. Martin-González, S. Borniquel, and J. C. Gutiérrez. 2000. Cyrtolophosis elongata (Colpodea, Ciliophora): Some aspects of ciliary pattern, division, cortical and nuclear changes during encystment and resting cyst ultrastructure. Eur. J. Protistol. 36:367-378. Didier, P., P. Depuytorac, N. Wilbert, and R. Detcheva. 1980. A propos d'observations sur l'ultrastructure de cilié Cyrtolophosis mucicola Stokes, 1885. J. Protozool. 27:72-79. Dini, F., and D. Nyberg. 1993. Sex in ciliates. Adv. Microb. Ecol. 13:85-153. Dobell, C. 1932. Antony van Leeuwenhoek and his "little animals". Dover Publications, Inc., New York. Doherty, M., B. Costas, G. B. McManus, and L. A. Katz. 2007. Culture-independent assessment of planktonic ciliate diversity in coastal northwest Atlantic water. Aquat. Microb. Ecol. 48:141-154. Domes, K., R. A. Norton, M. Maraun, and S. Scheu. 2007. Reevolution of sexuality breaks Dollo's law. Proc. Natl. Acad. Sci. USA 104:7139-7144. Dominguez, E., and Q. D. Wheeler. 1997. Taxonomic stability is ignorance. Cladistics 13:367-372. Donoghue, M. J., T. Eriksson, P. A. Reeves, and R. G. Olmstead. 2001. Phylogeny and phylogenetic taxonomy of Dipsacales with special reference to Sinadoxa and Tetradoxa (Adoxaceae). Harv. Pap. Bot. 6:459-479. Doyle, J. A., and P. K. Endress. 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Int. J. Plant Sci. 161:S121-S153. Doyle, J. J. 1992. Gene trees and species trees: molecular systematics as one-character taxonomy. Syst. Bot. 17:144-163.
200
Doyle, J. J. 1997. Trees within trees: genes and species, molecules and morphology. Syst. Biol. 46:537-553. Dragesco, J., and A. Dragesco-Kernéis. 1979. Cilies muscicoles nouveaux ou peu connus. Acta Protozool. 18:401-416. Dragesco, J., G. Fryd-versavel, F. Iftode, and P. Didier. 1977. Le cilie Platyophrya spumacola Kahl, 1926: morphologie, stomatogenèse et ultrastructure. Protistologica 13:419-434. Dubois, A. 2005. Proposed Rules for the incorporation of nomina of higher-ranked zoological taxa in the International Code of Zoological Nomenclature. 1. Some general questions, concepts and terms of biological nomenclature. Zoosystema 27:365-426. Dubois, A. 2006. Proposed Rules for the incorporation of nomina of higher-ranked zoological taxa in the International Code of Zoological Nomenclature. 2. The proposed Rules and their rationale. Zoosystema 28:165-258. Dundee, H. A. 1989. Higher category name usage for amphibians and reptiles. Syst. Zool. 38:398-406. Dunthorn, M., M. Eppinger, M. V. J. Schwarz, M. Schweikert, J. Boenigk, L. A. Katz, and T. Stoeck. 2009. Phylogenetic placement of the Cyrtolophosididae Stokes, 1888 (Ciliophora; Colpodea) and neotypification of Aristerostoma marinum Kahl, 1931. Int. J. Syst. Evol. Microbiol. 59:167-180. Dunthorn, M., W. Foissner, and L. A. Katz. 2008. Molecular phylogenetic analysis of class Colpodea (phylum Ciliophora) using broad taxon sampling. Mol. Phylogenet. Evol. 48:316-327. Dunthorn, M., and L. A. Katz. 2008. Richness of morphological hypotheses in ciliate systematics allows for detailed assessment of homology and comparisons with gene trees. Denisia 23:389-394. Dyke, G. J. 2002. Should paleontologists use "phylogenetic" nomenclature? J. Paleontol. 76:793-796. Eddy, S. R. 2001. HMMER: Profile hidden markov models for biological sequence analysis. http://hmmer.wustl.edu. Faivovich, J., C. F. B. Haddad, P. C. A. Garcia, D. R. Frost, J. A. Campbell, and W. C. Wheeler. 2005. Systematic review of the frog family Hylidae, with special reference to Hylinae: a phylogenetic analysis and taxonomic revisison. Bull. Amer. Mus. Nat. Hist. 294. Farris, J. S. 1974. Formal definitions of paraphyly and polyphyly. Syst. Zool. 23:548-554.
201
Felsenstein, J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27:401-410. Finlay, B. J. 2002. Global dispersal of free-living microbial eukaryote species. Science 296:1061-1063. Finlay, B. J., G. F. Esteban, and T. Fenchel. 1996. Global diversity and body size. Nature 383:132-133. Fischer, R. A. 1930. The genetical theory of natural selection. Oxford University Press, Oxford. Foissner, W. 1978. Das Silberliniensystem und die Infraciliatur der Gattungen Platyophrya Kahl, 1926, Cyrtolophosis Stokes, 1885 und Colpoda O.F.M., 1786: Ein Beitrag zur Systematik der Colpidida (Ciliata, Vestibulifera). Acta Protozool. 17:215-231. Foissner, W. 1985. Klassifikation und phylogenie der Colpodea (Protozoa: Ciliophora). Arch. Protistenk. 129:239-290. Foissner, W. 1987. Neue und wenig bekannte hypotriche und colpodide Ciliaten (Protozoa: Ciliophora) aus Böden und Moosen. Zool. Beitr. (N. F.) 31:187-282. Foissner, W. 1991. Basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. Europ. J. Protistol. 27:313-330. Foissner, W. 1993a. Colpodea (Ciliophora). Protozoenfauna 4/1:i-x, 1-798. Foissner, W. 1993b. Corticocolpoda kaneshiroae n. g., n. sp., a new colpodid ciliate (Protozoa, Ciliophora) from the bark of ohia trees in Hawaii. J. Eukaryot. Microbiol. 40:764-775. Foissner, W. 1993c. Idiocolpoda pelobia gen. n., sp. n., a new colpodid ciliate (Protozoa, Ciliophora) from an ephemeral stream in Hawaii. Acta Protozool. 32:175-182. Foissner, W. 1994. Pentahymena corticicola nov. gen., nov. spec., a new colpodid ciliate (Protozoa, Ciliophora) from bark of acacia trees in Costa Rica. Arch. Protistenk. 144:289-295. Foissner, W. 1995. Tropical protozoan diversity: 80 ciliate species (Protozoa, Ciliophora) in a soil sample from a tropical dry forest of Costa Rica, with description of four new genera and seven new species. Arch. Protistenk. 145:37-79. Foissner, W. 1996. Ontogenesis of ciliated protozoa with emphasis on stomatogenesis. Pp. 95-178 in K. Hausmann, and P. C. Bradbury, eds. Ciliates: Cells as Organisms. Gustav Fischer, Stuttgart.
202
Foissner, W. 1997a. Faunistic and taxonomic studies on ciliates (Protozoa, Ciliophora) from clean rivers in Bavaria (Germany), with descriptions of new species and ecological notes. Limnologica 27:179-238. Foissner, W. 1997b. Global soil ciliate (Protozoa, Ciliophora) diversity: a probabilitybased approach using large sample collections from Africa, Australia and Antarctica. Biodivers. Conserv. 6:1627-1638. Foissner, W. 1998. An updated compilation of world soil ciliates (Protozoa, Ciliophora), with ecological notes, new recordsm and descriptions of new species. Europ. J. Protistol. 34:195-235. Foissner, W. 1999a. Description of two new, mycophagous soil ciliates (Ciliophora, Colpodea): Fungiphrya strobli n. g., n. sp. and Grossglockneria ovata n. sp. J. Eukaryot. Microbiol. 46:34-42. Foissner, W. 1999b. Protist diversity: estimates of the near-imponderable. Protist 150:363-368. Foissner, W. 2002. Neotypification of protists, especially ciliates (Protozoa, Ciliophora). Bull. Zool. Nom. 59:165-169. Foissner, W. 2003. Pseudomaryna australiensis nov gen., nov spec. and Colpoda brasiliensis nov spec., two new colpodids (Ciliophora, Colpodea) with a mineral envelope. Europ. J. Protistol. 39:199-212. Foissner, W. 2005a. The unusual, lepidosome-coated resting cyst of Meseres corlissi (Ciliophora : Oligotrichea): Transmission electron microscopy and phylogeny. Acta Protozool. 44:217-230. Foissner, W. 2005b. Two new "flagship" ciliates (Protozoa, Ciliophora) from Venezuela: Sleighophrys pustulata and Luporinophrys micelae. Europ. J. Protistol. 41:99117. Foissner, W., S. Agatha, and B. H. 2002. Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest Africa), with emphasis on two contrasting environments, the Etosha Region and the Namib Desert: Part I. Densia 5:1-1063. Foissner, W., and H. Berger. 1999. Identification and ontogenesis of the nomen nudum hypotrichs (Protozoa: Ciliophora) Oxytricha nova (= Sterkiella nova sp. n.) and O. trifallax (= S. histriomuscorum). Acta Protozool. 38:215-248. Foissner, W., H. Berger, and J. Schaumburg. 1999. Indentification and ecology of limnetic plankton ciliates. Inf. Bayer. Landesamt Wasserwirtschaft 3/99:1-793. Foissner, W., H. Berger, K. Xu, and S. Zechmeister-Boltenstern. 2005a. A huge, undescribed soil ciliate (Protozoa : Ciliophora) diversity in natural forest stands of Central Europe. Biodivers. Conserv. 14:617-701.
203
Foissner, W., H. Blatterer, H. Berger, and F. Kohmann. 1991. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems—Band I: Cyrtophorida, Oligotrichida, Hypotrichia, Colpodea. Informationsberichte Bayer. Landesmat für Wasserwirtschaft, München. Foissner, W., A. Chao, and L. A. Katz. 2008. Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodivers. Conserv. 17:345-363. Foissner, W., and M. Kreutz. 1998. Systematic position and phylogenetic relationships of the genera Bursaridium, Paracondylostoma, Thylakidium, Bryometopus, and Bursaria (Ciliophora: Colpodea). Acta Protozool. 37:227-240. Foissner, W., S. Y. Moon-van der Staay, G. W. M. van der Staay, J. H. P. Hackstein, W.D. Krautgartner, and H. Berger. 2004. Reconciling classical and molecular phylogenies in the stichotrichines (Ciliophora, Spirotrichea), including new sequences from some rare species. Europ. J. Protistol. 40:265-281. Foissner, W., H. Müller, and S. Agatha. 2007. A comparative fine structural and phylogenetic analysis of resting cysts in oligotrich and hypotrich Spirotrichea (Ciliophora). Europ. J. Protistol. 43:295-314. Foissner, W., H. Müller, and T. Weisse. 2005b. The unusual, lepidosome-coated resting cyst of Meseres corlissi (Ciliophora : Oligotrichea): Light and scanning electron microscopy, cytochemistry. Acta Protozool. 44:201-215. Foissner, W., and M. Pichler. 2006. The unusual, lepidosome-coated resting cyst of Meseres corlissi (Ciliophora : Oligotrichea): Genesis of four complex types of wall precursors and assemblage of the cyst wall. Acta Protozool. 45:339-366. Foissner, W., M. Pichler, K. A. S. Al-Rasheid, and T. Weisse. 2006. The unusual, lepidosome-coated resting cyst of Meseres corlissi (Ciliophora : Oligotrichea): Encystment and genesis and release of the lepidosome. Acta Protozool. 45:323338. Foissner, W., and T. Stoeck. 2006. Rigidothrix goiseri nov. gen., nov. spec. (Rigidotrichidae nov. fam.), a new "flagship" ciliate from the Niger floodplain breaks the flexibility-dogma in the classification of stichotrichine spirotrichs (Ciliophora, Spirotrichea). Europ. J. Protistol. 42:249-267. Foissner, W., M. Struder-Kypke, G. W. M. van der Staay, S. Y. Moon-van der Staay, and J. H. P. Hackstein. 2003. Endemic ciliates (Protozoa, Ciliophora) from tank bromeliads (Bromeliaceae): a combined morphological, molecular, and ecological study. Europ. J. Protistol. 39:365-372. Foissner, W., and K. Xu. 2007. Monograph of the Spathidiida (Ciliophora: Haptoria), Vol I: Protospathidiidae, Arcuospathidiidae, Apterospathulidae. Monographiae Biol. 81.
204
Foissner, W., K. Xu, and M. Kreutz. 2005c. The Apertospathulidae, a new family of Haptorid ciliates (Protozoa, Ciliophora). J. Eukaryot. Microbiol. 52:360-373. Gatesy, J., R. DeSalle, and N. Wahlberg. 2007. How many genes should a systematist sample? Conflicting insights from a phylogenomic matrix characterized by replicated incongruence. Syst. Biol. 56:355-363. Gerassimova, Z. P., and L. N. Seravin. 1976. Ectoplasmic fibrillar system of Infusoria and its role for the understanding of their phylogeny. Zool. Zh. 55:645-656. Ghiselin, M. T. 1977. On changing the names of higher taxa. Syst. Zool. 26:346-349. Giribet, G., and W. Wheeler. 2002. On bivalve phylogeny: a high-level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data. Invert. Biol. 121:271-324. Givnish, T. J., and K. J. Sytsma. 1997. Consistency, characters, and the likelihood of correct phylogenetic inference. Mol. Phylogenet. Evol. 7:320-330. Goldberg, E. E., and B. Igic. 2008. On phylogenetic tests of irreversible evolution. Evolution 62:2727-2741. Golder, T. K. 1976. The macro-micronuclear complex of Woodruffia metabolica. J. Ultrastruct. Res. 54:169-175. Gong, Y., Y. Yu, P. E. V., F. Zhu, and W. Miao. 2006. Reevaluation of he phylogenetic relationship between mobilid and sessilid peritrichs (Ciliophora, Oligohymenophorea) based on small subunit rRNA gene sequences. J. Eukaryot. Microbiol. 53:397-403. Gould, S. J. 1970. Dollo on Dollo's Law: irreversibility and the status of evolutionary laws. J. Hist. Biol. 3:189-212. Grabowski, P. J., A. J. Zaug, and T. R. Cech. 1981. The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of Tetrahymena. Cell 23:467-476. Graybeal, A. 1998. Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47:9-17. Greenwood, S. J., M. L. Sogin, and D. H. Lynn. 1991. Phylogenetic relationships within the class oligohymenophorea, phylum Ciliophora, inferred from the complete small subunit rRNA gene sequences of Colpidium campylum, Glaucoma chattoni and Opisthonecta henneguyi. J. Mol. Evol. 33:163-174. Greslin, A. F., D. M. Prescott, Y. Oka, S. H. Loukin, and J. C. Chappell. 1989. Reordering of 9 exons is necessary to form a functional actin gene in Oxytricha nova. Proc. Natl. Acad. Sci. USA 86:6264-6268.
205
Hamilton, W. D. 2001. Narrow roads of gene land, Vol. 2: the evolution of sex. Oxford University Press, Oxford. Hammerschmidt, B., M. Schlegel, D. Lynn, D. D. Leipe, M. L. Sogin, and I. B. Raikov. 1996. Insights into the evolution of nuclear dualism in the ciliates revealed by phylogenetic analysis of rRNA sequences. J. Eukaryot. Microbiol. 43:225-230. Haugen, P., D. H. Coucheron, S. B. Ronning, K. Haugli, and S. Johansen. 2003. The molecular evolution and structural organization of self-splicing group I introns at position 516 in nuclear SSU rDNA of myxomycetes. J. Eukaryot. Microbiol. 50:283-292. Haugen, P., D. M. Simon, and D. Bhattacharya. 2005. The natural history of group I introns. Trends Genet. 21:111-119. Hedtke, S. M., T. M. Townsend, and D. M. Hillis. 2006. Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Syst. Biol. 55:522-529. Hemming, F., ed. 1953. Copenhagen decisions on zoological nomenclature, addirions to, and modeifications of, the Règles internationales de la nomenclature zoologique; approved and adapted by the 14th International Congress of Zoology, Copenhagen, August, 1953. International Trust for Zoological Nomenclature, London. Hendy, M. D., and D. Penny. 1989. A framework for the quantitative study of evolution. Syst. Zool. 38:297-309. Hennig, W. 1966. Phylogenetic systematics. University of Illinois Press, Urbana. Hewitt, E. A., K. M. Müller, J. Cannone, D. J. Hoga, R. Gutell, and D. M. Prescott. 2003. Phylogenetic relationships among 28 spirotrichous ciliates documented by rDNA. Mol. Phylogenet. Evol. 29:258-267. Heywood, V. H., R. K. Brummitt, A. Culham, and O. Seberg. 2007. Flowering Plant Families of the World. Firefly Books, Ontario, Canada. Hibbett, D. S., and M. J. Donoghue. 1998. Intergrating phylogenetic analysis and classification in fungi. Mycologia 90:347-356. Hillis, D. M. 1998. Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst. Biol. 47:3-8. Hillis, D. M., D. D. Pollock, J. A. McGuire, and D. J. Zwickl. 2003. Is sparse taxon sampling a problem for phylogenetic inference? Syst. Biol. 52:124-126. Hillis, D. M., and J. J. Wiens. 2000. Molecules versus morphology in systematics: conflicts, artifacts, and misconceptions in J. J. Wiens, ed. Phylogenetic analysis of morphological data. Smithsonian Institution Press, Washington.
206
Hirt, R. P., P. L. Dyal, M. Wilkinson, B. J. Finlay, D. M. Roberts, and T. M. Embley. 1995. Phylogenetic relationships among Karyorelictids and Heterotrichs inferred from small subunit rRNA sequences: resolution at the base of the ciliate tree. Mol. Phylogenet. Evol. 4:77-87. Holder, M. T., J. Sukumaran, and P. O. Lewis. 2008. A justification for reporting the majority-rule consensus tree in Bayesian phylogenetics. Syst. Biol. 57:814-821. Hörandl, E. 2007. Neglecting evolution is bad taxonomy. Taxon 56:1-5. Hori, M., I. Tomikawa, E. Przyboś, and M. Fugishima. 2006. Comparison of the evolutionary distances among syngens and sibling species of Paramecium. Molec. Phylogen. Evol. 38:697-704. Huelsenbeck, J. P., and D. M. Hillis. 1993. Success of phylogenetic methods in the fourtaxon case. Syst. Biol. 42:247-264. Huelsenbeck, J. P., and F. R. Ronquist. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. Hurst, L. D., W. D. Hamilton, and R. J. Ladle. 1992. Covert sex. Trends Ecol. Evol. 7:144-145. ICZN. 1999. International Code of Zoological Nomenclature, 4th ed. The International Trust for Zoological Nomenclature, London, U.K. International Commission on Zoological Nomenclature. 1999. International Code of Zoological Nomenclature, 4th ed. The International Trust for Zoological Nomenclature, London. Israel, R. L., S. L. Kosakovsky Pond, S. V. Muse, and L. A. Katz. 2002. Evolution of duplicated alpha-tubulin genes in ciliates. Evolution 56:1110-1122. Jackson, S. A., J. J. Cannone, J. C. Lee, R. R. Gutell, and S. A. Woodson. 2002. Distribution of rRNA introns in the three-dimensional structure of the ribosome. J. Mol. Biol. 323:35-52. Jankowski, A. W. 2007. Phylum Ciliophora Doflein, 1901. Pp. 415-993 in A. F. Alimov, ed. Protista. Part 2, Handbook of Zoology. Russian Academy of Sciences, Zoological Institure, St. Petersburg. Joyce, W. G., J. F. Parham, and J. A. Gauthier. 2004. Developing a protocol for the conversion of rank-based taxon names to phylogenetically defined clade names, as exemplified by turtles. J. Paleontol. 78:989-1013. Judo, M. S. B., A. B. Wedel, and C. Wilson. 1998. Stimulation and suppression of PCRmediated recombination. Nucleic Acids Res. 26:1819-1825.
207
Judson, O. P., and B. B. Normark. 1996. Ancient asexual scandals. Trends Ecol. Evol. 11:A41-A46. Kahl, A. 1926. Neue und wenig bekannte Formen der holotrichen und heterotrichen Ciliaten. Arch. Protistenk. 55:197-438. Kahl, A. 1930-1935. Urtiere oder Protozoa. I: Wimpertiere oder Ciliata (Infusoria), eine Bearbeitung der freilebenden und ectocommensalen Infusorien der Erde, unter Ausschluss der marinen Tintinnidae. Pp. 1-886 in F. Dahl, ed. Die Teirwelt Deutschlands. G. Fischer, Jena. Kahl, A. 1931. Urtiere oder Protozoa I: Wimpertiere oder Ciliate (Infusoria) 2. Holotricha außer den im 1. Teil behandelten Prostomata. Tierwelt Dtl. 21:181-398. Katz, L. A., J. G. Bornstein, E. Lasek-Nesselquist, and S. V. Muse. 2004a. Dramatic diversity of ciliate histone H4 genes revealed by comparisons of patterns of substitutions and paralog divergences among eukaryotes. Mol. Biol. Evol. 21:555562. Katz, L. A., E. Lasek-Nesselquist, J. Bornstein, and S. V. Muse. 2004b. Dramatic diversity of ciliate histone H4 genes revealed by comparisons of patterns of substitutions and paralog divergences among eukaryotes. Mol. Biol. Evol. 21:555562. Katz, L. A., G. B. McManus, O. L. O. Snoeyenbos-West, A. Griffin, K. Pirog, B. Costas, and W. Foissner. 2005. Reframing the 'Everything is everywhere' debate: Evidence for high gene flow and diversity in ciliate morphospecies. Aquat. Microb. Ecol. 41:55-65. Katz, L. A., O. Snoeyenbos-West, and F. P. Doerder. 2006. Patterns of protein evolution in Tetrahymena thermophila: implications for estimates of effective population size. Mol. Biol. Evol. 23:608-614. Kawakami, H. 1991. An endosymbiotic Chlorella-bearing ciliate: Platyophrya chlorelligera Kawakami 1989. Eur. J. Protistol. 26:245-255. Keller, R. A., R. N. Boyd, and Q. D. Wheeler. 2003. The illogical basis of phylogenetic nomenclature. Bot. Rev. 69:93-110. Kim, J. S., H. J. Jeong, D. H. Lynn, J. Y. Park, Y. W. Lim, and W. Shin. 2007. Balanion masanensis n. sp. (Ciliophora: Prostomatea) from the coastal waters of Korea: Morphology and small subunit ribosomal RNA gene sequence. J. Eukaryot. Microbiol. 54:482-494. Kishino, H., and M. Hasegawa. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data and the branching order in Hominoidea. J. Mol. Evol. 29:170-179.
208
Kojima, J. 2003. Apomorphy-based definition also pinpoints a node, and PhyloCode names prevent effective communication. Bot. Rev. 69:44-58. Kolaczkowski, B., and J. W. Thornton. 2004. Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431:980-984. Kondrashov, A. S. 1982. Selection against harmful mutations in large sexual and asexual population. Genet. Res. 40:325-332. Kondrashov, A. S. 1993. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84:372-387. Kosakovsky Pond, S. L., S. D. W. Frost, and S. V. Muse. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679. Lasek-Nesselquist, E., and L. A. Katz. 2001. Phylogenetic position of Sorogena stoianovitchae and relationships within the class Colpodea (Ciliophora) based on SSU rDNA sequences. J. Eukaryot. Microbiol. 48:604-607. Laurin, M., K. de Queiroz, and P. D. Cantino. 2006. Sense and stability of taxon names. Zoologica Scripta 35:113-114. Lee, M. S. Y. 1996. Stability in meaning and content of taxon names: an evaluation of crown clade definitions. Proc. R. Soc. Lond. B 263:1103-1109. Lee, M. S. Y. 2000. A worrying systematic decline. Trends Ecol. Evol. 15:346. Lee, M. S. Y. 2001. On recent arguments for phylogenetic nomenclature. Taxon 50:175180. Lefèvre, E., C. Bardot, C. Noël, J. F. Carrias, E. Viscogliosi, C. Amblard, and T. SimeNgando. 2007. Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ. Microbiol. 9:61-71. Lin, X., W. Song, and J. Li. 2007. Description of two new marine pleurostomatid ciliates, Loxophyllum choii nov. spec. and L. shini nov spec. (Ciliophora, Pleurostomatida) from China. Europ. J. Protistol. 43:131-139. Lynch, M., R. Bürger, D. Butcher, and W. Gabriel. 1993. Mutational meltdowns in asexual populations. J. Hered. 84:339-344. Lynch, M., and J. S. Conery. 2003. The origins of genome complexity. Science 302:1401-1404. Lynn, D. H. 1976. Comparative ultrastructure and systematics of colpodida. Structural conservatism hypothesis and a description of Colpoda steinii Maupas. J. Protozool. 23:302-314.
209
Lynn, D. H. 1979. Fine structural specializations and evolution of carnivory in Bresslaua (Ciliophora, Colpodida). Trans. Am. Microsc. Soc. 98:353-368. Lynn, D. H. 1981. The organization and evolution of microtubular organelles in ciliated protozoa. Biol. Rev. 56:243-292. Lynn, D. H. 1996. My journey in ciliate systematics. J. Eukaryot. Microbiol. 43:253-260. Lynn, D. H. 2003. Morphology or molecules: how do we identify the major lineages of ciliates (Phylum Ciliophora)? Europ. J. Protistol. 39:356-364. Lynn, D. H. 2008. The ciliated protozoa: characterization, classification, and guide to the literature, 3rd edition. Springer, Dordrecht. Lynn, D. H., and E. B. Small. 1997. A revised classification of the phylum Ciliophora Doflein, 1901. Rev. Soc. Mex. Hist. Nat. 47:65-78. Lynn, D. H., and E. B. Small. 2002. Phylum Ciliophora Doflein, 1901. Pp. 371-656 in J. J. Lee, G. F. Leedale, and P. C. Bradbury, eds. An illustrated guide to the protozoa, 2nd ed. Society of Protozoologists, Lawrence, Kansas. Lynn, D. H., and M. L. Sogin. 1988. Assessment of phylogenetic relationships among ciliated protists using partial ribosomal RNA sequences derived from reverse transcripts. Biosystems 21:249-254. Lynn, D. H., and M. Strüder-Kypke. 2002. Phylogenetic position of Licnophora, Lechriopyla, and Schizocaryum, three unusual ciliates (Phylum Ciliophora) endosymbiotic in echinoderms (Phylum echinodermata). J. Eukaryot. Microbiol. 49:460-468. Lynn, D. H., and M. Strüder-Kypke. 2006. Species of Tetrahymena indentical by small subunut rRNA gene sequences are discriminated by mitochondrial cytochrome c oxidase I gene sequences. J. Eukaryot. Microbiol. 53:385-387. Lynn, D. H., A.-D. G. Wright, M. Schlegel, and W. Foissner. 1999a. Phylogenetic relationships of orders within the class Colpodea (Phylum Ciliophora) inferred from small subunit rRNA gene sequences. J. Mol. Evol. 48:605-614. Lynn, D. H., A. D. G. Wright, M. Schlegel, and W. Foissner. 1999b. Phylogenetic relationships of orders within the class Colpodea (phylum Ciliophora) inferred from small subunit rRNA gene sequences. J. Mol. Evol. 48:605-614. Ma, H. W., R. M. Overstreet, J. H. Sniezek, M. Solangi, and D. W. Coats. 2006. Two new species of symbiotic ciliates from the respiratory tract of cetaceans with establishment of the new genus Planilamina n. gen. (Dysteriida, Kyaroikeidae). J. Eukaryot. Microbiol. 53:407-419. Maddison, W. P. 1997. Gene trees in species trees. Syst. Biol. 46:523-536.
210
Maddison, W. P., and D. R. Maddison. 2005. MacClade v. 4.0.8. Sinauer Assoc. Maeda, M. 1986. An illustrated guide to the species of the families Halteriidae and Strobilidiidae (Oligotrichida, Ciliophora), free swimming protozoa common in the aquatic environment. Mark Welch, D., M. P. Cummings, D. M. Hillis, and M. Meselson. 2004a. Divergent gene copies in the asexual class Bdelloidea (Rotifera) separated before the bdelloid radiation or within bdelloid families. Proc. Natl. Acad. Sci. USA 101:1622-1625. Mark Welch, D., J. L. Mark Welch, and M. Meselson. 2008. Evidence for degenerate tetraploidy in bdelloid rotifers. Proc. Natl. Acad. Sci. USA 105:5145-5149. Mark Welch, D., and M. Meselson. 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288:1211-1215. Mark Welch, J. L., D. Mark Welch, and M. Meselson. 2004b. Cytogenetic evidence for asexual evolution of bdelloid rotifers. Proc. Natl. Acad. Sci. USA 101:1618-1621. Marshall, C. R., E. C. Raff, and R. A. Raff. 1994. Dollo's law and the death and resurrection of gene. Proc. Natl. Acad. Sci. USA 91:12283-12287. Martin, D., and E. Rybicki. 2000. RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562-563. Martín-González, A., J. Wierzchos, J. C. Gutiérrez, J. Alonso, and C. Ascaso. 2008. Morphological stasis of protists in lower Cretaceous amber. Protist 159:251-257. Matthes, D. 1988. Suctoria und Urceolariidae. Protozoenfauna 7/1:i-ix, 1-309. Maynard Smith, J. 1978. The evolution of sex. Cambridge University Press, Cambridge. Maynard Smith, J. 1992. Analyzing the mosaic structure of genes. J. Mol. Evol. 34:126129. Mayr, E. 1963. Animal species and evolution. The Belknap Press of Harvard University Press, Cambridge. Mayr, E. 1976. Evolution and the diversity of life. The Belknap Press of Havard University Press, Cambridge. Mayr, E. 1998. Two empires or three? Proc. Natl. Acad. Sci., USA 95:9720-9723. Mayr, E., and W. J. Bock. 2002. Classifications and other ordering systems. J. Zoo. Syst. Evol. Research 40:169-194.
211
McGrath, C. L., R. A. Zufall, and L. A. Katz. 2006. Genome evolution in ciliates. Pp. 6477 in L. A. Katz, and D. Bhattacharya, eds. Genomics and evolution of eukaryotic microbes. Oxford Uniuversity Press, New York. Mears, J. A., J. J. Cannone, S. M. Stagg, R. R. Gutell, R. K. Agrawal, and S. C. Harvey. 2002. Modeling a minimal ribosome based on comparative sequence analysis. J. Mol. Biol. 321:215-234. Medlin, L., H. J. Elwood, S. Stickel, and M. L. Sogin. 1988. The characterization of enzymatically amplified eukaryotes 16S-like ribosomal RNA coding regions. Gene 71:491-500. Miyake, A. 1996. Fertilization and sexuality in ciliates. Pp. 243-290 in K. Hausmann, and P. C. Bradbury, eds. Ciliates: cells as organisms. Gustav Fischer, Stuttgart. Modesto, S. P., and J. S. Anderson. 2004. The phylogenetic definition of Reptilia. Syst. Biol. 53:815-821. Moore, G. 1998. A comparison of traditional and phylogenetic nomenclature. Taxon 47:561-579. Moore, G. 2003. Should taxon names be explicitly defined? Bot. Rev. 69:2-21. Morin, G. B., and T. R. Cech. 1988. Phylogenetic relationships and altered genome structures among Tetrahymena mitochondrial DNAs. Nucleic Acids Res 16:327346. Muller, H. J. 1964. The relation of recombination to mutational advance. Mutation Res. 1:2-9. Nanney, D. L. 1977. Molecules and morphospecies: the perpetuation of pattern in ciliates protozoa. J. Protozool. 24:27-35. Nanney, D. L. 1980. Experimental ciliatology: an introduction to genetic and developmental analysis in ciliates. John Wiley & Sons, New York. Nanney, D. L. 1982. Genes and phenes in Tetrahymena. Bioscience 32:783-788. Nanney, D. L. 1999. When is a rose?: the kinds of Tetrahymena. Pp. 93-118 in R. A. Wilson, ed. Species: new interdisciplinary essays. The MIT Press, Cambridge. Nanney, D. L., and J. W. McCoy. 1976. Characterization of the species of the Tetrahymena pyriformis complex. Trans. Am. Microsc. Soc. 95:664-682. Nanney, D. L., C. Park, R. Preparata, and E. M. Simon. 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.
212
Nixon, K. C., and J. M. Carpenter. 2000. On the other "phylogenetic systematics". Cladistics 16:298-318. Nixon, K. C., J. M. Carpenter, and D. W. Stevenson. 2003. The PhyloCode is fatally flawed, and the "Linnaean" system can easily be fixed. Bot. Rev. 69:111-120. Njine, T. 1979. Etude ultrastructurale de cilié Kuklikophyra dragescoi gen. n., sp. n. J. Protozool. 26:589-598. Nordal, H., and B. Stedje. 2005. Paraphyletic taxa should be accepted. Taxon 54:5-6. Normark, B. B., O. P. Judson, and N. A. Moran. 2003. Genomic signatures of ancient asexual lineages. Biol. J. Linn. Soc. 79:69-84. Nylander, J. A. 2004. MrModeltest v2. Distrubuted by the author. Evolutionary Biology Center, Uppsala University, Upsalla. Nylander, J. A., J. C. Wilgenbusch, D. L. Warren, and D. L. Swofford. 2008. AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phyologenetics. Bioinformatics 24:581-583. Omilian, A. R., M. E. A. Cristescu, J. L. Dudycha, and M. Lynch. 2006. Ameiotic recombination in asexual lineages of Daphnia. Proc. Natl. Acad. Sci. USA 103:18638-18643. Page, R. D. 1996. TREEVIEW: An application to display phylogenetic tress on personal computers. Comput. Appl. Biosci. 12:357-358. Patterson, C. 1982. Morphological characters and homology. Pp. 21-74 in K. A. Joysey, and A. E. Friday, eds. Problems of phylogenetic reconstruction. Academic Press, London. Pernin, P., A. Ataya, and M. L. Cariou. 1992. Genetic structure of natural populations of the free-living ameba, Naegleria lovaniensis. evidence for sexual reproduction. Heredity 68:173-181. Petz, W., and W. Foissner. 1992. Morphology and morphogenesis of Strobilidium caudatum (Fromentel), Meseres corlissi n. sp., Halteria grandinella (Muller), and Strombidium rehwaldi n. sp., and a proposed phylogenetic system for oligotrich ciliates (Protozoa, Ciliophora). J. Protozool. 39:159-176. Petz, W., W. Song, and N. Wilbert. 1995. Taxonomy and ecology of the ciliate fauna (Protozoa: Ciliophora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Staphia 4:1-223. Pfenninger, M., and K. Schwenk. 2007. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol. Biol. 7:121.
213
Pleijel, F., and G. W. Rouse. 2003. Ceci n'est pas une pipe: names, clades and phylogenetic nomenclature. J. Zool. Syst. Evol. Research 41:162-174. Poe, S., and D. L. Swofford. 1999. Taxon sampling revisited. Nature 398:299-300. Polaszek, A., and E. O. Wilson. 2005. Sense and stability in animal names. Trends Ecol. Evol. 20:421-422. Poljansky, G. 1934. Geschlechtsprozesse bei Bursaria truncatella O.F. Müll. Arch. Protistenk. 81:420-546. Porter, M. L., and K. A. Crandall. 2003. Lost along the way: significance of evolution in reverse. Trends. Ecol. Evol. 18:541-547. Posada, D., and K. A. Crandall. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulation. Proc. Natl. Acad. Sci. USA 98:13757-13762. Prescott, D. M. 1992. The unusual organization and processing of genomic DNA in hypotrichous ciliates. Trends Genet. 8:439-445. Przyboś, E., A. Maciejewska, and B. Skotarczak. 2006. Relationship of species of the Paramecium aurelia complex (Protozoa, ph. Ciliophora, cl. Oligohymenophorea) based on sequences of the histone H4 gene fragment. Folia Biol. (Praha). 54:3742. Puytorac, P. d. 1994. Phylum Ciliophora Doflein, 1901. Pp. 1-15 in P. P. de, ed. Traité de Zoologie, Tome II, Infusoires Ciliés, Fasc. 2, Systématique. Masson, Paris. Puytorac, P. d., A. Batisse, J. Bohatier, J. O. Corliss, G. Deroux, P. Didier, J. Dragesco, G. Fryd-Versavel, J. Grain, C.-A. Groliére, F. Iftode, M. Laval, M. Roque, A. Savoie, and M. Tuffrau. 1974. Proposition d'une classification du phylum Ciliophora Doflein, 1901. C.R. Acad. Sci. Paris 278:2799-2802. Puytorac, P. d., J. Grain, and P. Legendre. 1994. An attempt at reconstructing a phylogenetic tree of the ciliophora using parsimony methods. Europ. J. Protistol. 30:1-17. Puytorac, P. d., M. R. Kattar, C. A. Grolière, and I. d. Silva Neto. 1992. Polymorphism and ultrastructure of the colpodean ciliate of the genus Platyophryides Foissner, 1987 J. Protozool. 39:154-159. Puytorac, P. d., F. Perez-Paniagua, and J. Perez-Silva. 1979. A propos d'observations sur la stomatogenèse et l'ultrastructure de cilié Woodruffia metabolica (Johnson et Larson, 1938). Protistologica 15:231-243. Raikov, I. B. 1982. The protozoan nucleus: morphology and evolution. Springer-Verlag, Wien.
214
Raikov, I. B. 1996. Nuclei of ciliates. Pp. 221-242 in K. Hausmann, and P. C. Bradbury, eds. Ciliates: cells as organisms. Gustav Fischer, Stuttgart. Ramesh, M. A., S.-B. Malik, and J. M. Longsdon. 2005. A phylogenomic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr. Biol. 15:185-191. Rannala, B., J. P. Huelsenbeck, Z. Yang, and R. Neilsen. 1998. Taxon sampling and the accuracy of large phylogenies. Syst. Biol. 47:702-710. Reize, I. B., and M. Melkonian. 1989. A new way to investigate living flagellate/ciliated cells in the light microscopr: Immobilization of cells in agarose. Bot. Acta 102:145-151. Rokas, A., and S. B. Carroll. 2005. More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. Mol. Biol. Evol. 22:1337-1344. Rokas, A., B. L. Williams, N. King, and S. B. Carroll. 2003. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798-804. Sadler, L. A., and C. F. Brunk. 1992. Phylogenetic relationships and unusual diversity in histone H4 proteins within the Tetrahymena pyriformis complex. Mol. Biol. Evol. 9:70-84. Sangster, G. 2005. A name for the clade formed by owlet-nightjars, swifts and hummingbirds (Aves). Zootaxa:1-6. Schander, C., and M. Thollesson. 1995. Phylogenetic Taxonomy―Some Comments. Zool. Scr. 24:263-268. Schmidt, A. R., H. von Eynatten, and M. Wagreich. 2001. The Mesozoic amber of Schliersee (southern Germany) is Cretaceous in age. Cretaceous Res. 22:423-428. Schmidt, S. L., D. Bernard, M. Schlegel, and W. Foissner. 2007a. Phylogeny of the Stichotrichea (Ciliophora: Spirotrichea) reconstructed with nulcear small subunit rRNA gene sequences: discrepancies and accordances with morphological data. J. Eukaryot. Microbiol. 54:201-209. Schmidt, S. L., W. Foissner, M. Schlegel, and D. Bernhard. 2007b. Molecular phylogeny of the heterotrichea (Ciliophora, postciliodesmatophora) based on small subunit rRNA gene sequences. J. Eukaryot. Microbiol. 54:358-363. Schönborn, W., H. Dörfelt, W. Foissner, L. Krientiz, and U. Schäfer. 1999. A fossilized microcenosis in Triassic amber. J. Eukaryot. Microbiol. 46:571-584. Schuh, R. 2003. The Linnaean system and its 250-year persistence. Bot. Rev. 69:59-78.
215
Schwander, T., and B. J. Crespi. 2009. Twigs on the tree of life? Neutral and selective models for intergrating macroevolutionary patterns and microevolutionary processes in the analysis of asexuality. Molec. Ecol. 18:28-42. Scotland, R. W., R. G. Olmstead, and J. R. Bennett. 2003. Phylogeny reconstruction: the role of morphology. Syst. Biol. 52:539-548. Sereno, P. C. 1999. Definitions in phylogenetic taxonomy: Critique and rationale. Syst. Biol. 48:329-351. Sereno, P. C. 2005. The logical basis of phylogenetic taxonomy. Systematic Biology 54:595-619. Shimodaira, H., and M. Hasegawa. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246-1247. Shin, M. K., U. W. Hwang, W. Kim, A.-D. G. Wright, C. Krawczyk, and D. H. Lynn. 2000. Phylogenetic position of the ciliates Phacodinium (Order Phacodiniida) and Protocruzia (Subclass Protocruziidia) and systematics of the spirotrich ciliates examined by small subunit ribosomal RNA gene sequences. Europ. J. Protistol. 36:293-302. Siddall, M. E., and M. F. Whiting. 1999. Long-branch abstractions. Cladistics 15:9-24. Simon, D., J. Moline, G. Helms, T. Friedl, and D. Bhattacharya. 2005. Divergent histories of rDNA group I introns in the lichen family Physciaceae. J. Mol. Evol. 60:434-446. Simon, E. M., D. L. Nanney, and F. P. Doerder. 2008. The "Tetrahymena pyformis" complex of cryptic species. Biodivers. Conserv. 17:365-380. Simpson, G. G. 1953. The major features of evolution. Columbia University Press, New York. Small, E. B., and D. H. Lynn. 1981. A new macrosystem for the phylum Ciliophora Doflein, 1901. Biosystems 14:387-401. Small, E. B., and D. H. Lynn. 1985. Phylum Ciliophora, Doflein 1901 in J. J. Lee, S. H. Hutner, and E. C. Bovee eds. An illustrated guide to the protozoa. Society of Protozoologists, Lawrence, KS. Smith, R. J., T. Kamiya, and D. J. Horne. 2006. Living males of the 'ancient asexual' Darinulidae (Ostracoda: Crustacea). Proc. R. Soc. Lond. B 273:1569-1578. Snoeyenbos-West, O. L. O., J. Cole, A. Campbell, D. W. Coats, and L. A. Katz. 2004. Molecular phylogeny of phyllopharyngean ciliates and their group I introns. J. Eukaryot. Microbiol. 51:441-450.
216
Snoeyenbos-West, O. L. O., T. Salcedo, G. B. McManus, and L. A. Katz. 2002. Insights into the diversity of choreotrich and oligotrich ciliates (Class : Spirotrichea) based on genealogical analyses of multiple loci. Int. J. Syst. Evol. Microbiol. 52:19011913. Snoke, M. S., T. U. Berendonk, D. Barth, and M. Lynch. 2006. Large global effective population sizes in Paramecium. Mol. Biol. Evol. 23:2474-2479. Sogin, M. L., and H. J. Elwood. 1986. Primary structure of the Paramecium tetraurelia small-subunit rRNA coding region: phylogenetic relationships within the Ciliophora. J. Mol. Evol. 23:53-60. Sonneborn, T. M. 1937. Sex, sex inheritance and sex determination in Paramecium aurelia. Proc. Natl. Acad. Sci. 23:378-383. Sonneborn, T. M. 1957. Breeding systems, reproductive methods, and species problems in protozoa. Pp. 155-324 in E. Mayr, ed. The species problem. American Association for the Advancement of Science, Washington D. C. . Sonneborn, T. M. 1975. The Paramecium aurelia complex of fourteen sibiling species. Trans. Am. Microsc. Soc. 94:155-178. Sosef, M. S. M. 1997. Hierarchical models, reticulate evolution and the inevitability of paraphyletic supraspecific taxa. Taxon 46:75-85. Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A fast boostrap algorithm for the RAxML web-servers. Syst. Biol. 57:758-771. Stechmann, A., M. Schlegel, and D. H. Lynn. 1998. Phylogenetic relationships between Prostome and Colpodean ciliates tested by small subunit rRNA sequences. Mol. Phyl. Evol. 9:48-54. Stefanovic, S., D. F. Austin, and R. G. Olmstead. 2003. Classification of Convolvulaceae: A phylogenetic approach. Syst. Bot. 28:791-806. Stetter, K. O., H. Köning, and E. Stachebrandt. 1983. Pyrodictium gen. nov., a new genus of submarine disc-shaped sulphur reducing archaebacteria growing optimally at 1050C. Appl. Microbiol. 4:535-551. Stevens, P. F. 1984. Homology and phylogeny: morphology and systematics. Syst. Bot. 9:395-409.
217
Stoeck, T., W. Foissner, and D. H. Lynn. 2007. Small-subunit rDNA phylogenies sugest that Epalxella antiquorum (Penard, 1922) Corliss, 1960 (Ciliophora, Odontostomatida) is a member of the Plagyopylea. J. Eukaryot. Microbiol. 54:436-442. Stoeck, T., B. Hayward, G. T. Taylor, R. Varela, and S. S. Epstein. 2006. A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157:31-43. Stoeck, T., M. V. J. Schwarz, J. Boenigk, M. Schweikert, S. von der Heyden, and A. Behnke. 2005. Cellular identity of an 18S rRNA gene sequence clade within the class Kinetoplastea: the novel genus Actuariola gen. nov. (Neobodonida) with description of the type species Actuariola framvarensis sp. nov. Int. J. Syst. Evol. Microbiol. 55:2623-2635. Strüder-Kypke, M., O. A. Kornilova, and D. H. Lynn. 2007. Phylogeny of trichostome ciliates (Ciliophora, Litostomatea) endosymbiotic in the Yakut horse (Equus caballus). Europ. J. Protistol. 43:319-328. Strüder-Kypke, M., A.-D. G. Wright, W. Foissner, and D. H. Lynn. 2006. Molecular phylogeny of Litostome ciliates (Ciliophora, Litostomatea) with emphasis on freeliving haptorian genera. Protist 157:261-278. Strüder-Kypke, M. C., and D. H. Lynn. 2003. Sequence analyses of the small subunit rRNA gene confirm the paraphyly of oligotrich ciliates sensu lato and support the monophyly of the subclasses Oligotrichia and Choreotrichia (Ciliophora, Spirotrichea). J. Zool. 260:87-97. Swofford, D. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Assoc, Sunderland MA. Szabó, M. 1935. Neuere Beiträge zur Kenntnis der Gattung Halteria (Protozoa, Ciliata). Arch. Protistenk. 86:307-317. Taylor, M. P., and D. Naish. 2005. The phylogenetic taxonomy of Diplodocoidea (Dinosauria: Sauropoda). PaleoBios 25:1-7. Teotónio, H., and M. R. Rose. 2001. Perspective: reverse evolution. Evolution 55:653660. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:4673-4680.
218
Thorne, R. F. 2000. The classification and geography of the flowering plants: Dicotyledons of the class angiospermae (Subclasses magnoliidae, ranunculidae, caryophyllidae, dilleniidae, rosidae, asteridae, and lamiidae). Botanical Review 66:441-647. Tourancheau, A. B., E. Villalobo, N. Tsao, A. Torres, and R. E. Pearlman. 1998. Protein coding gene trees in ciliates: comparisons with rRNA-based phylogenies. Mol. Phyl. Evol. 10:299-309. Van Bell, C. T. 1985. The 5s and 5.8s ribosomal RNA sequences of Tetrahymena thermophila and T. pyriformis. J. Protozool. 32:640-644. van Hannen, E. J., W. M. Mooij, M. P. van Agterveld, H. J. Gons, and H. J. Laanbroek. 1999. Detritus-dependent development of the microbial community in an experimental system: Qualitative analysis by denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 65:2478-2484. van Hoek, A. H. A. M., A. S. Akhmanova, M. A. Huynen, and J. H. P. Hackstein. 2000a. A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol. Biol. Evol. 17:202-206. van Hoek, A. H. A. M., T. A. van Alen, V. S. I. Sprakel, J. A. M. Leunissen, T. Brigge, G. D. Vogels, and J. H. P. Hackstein. 2000b. Multiple acquisitions of methanogenic Archaeal symbionts by anaerobic ciliates. Mol. Bio. Evol. 17:251258. Weisse, T. 2002. The significance of inter- and intraspecific variation in bacterivorous and herbivorous protists. Antonie Van Leeuwenhoek 81:327-341. Weisse, T., and S. Lettner. 2002. The ecological significance of intraspecific variation among freshwater ciliates. Verh. Internat. Verein. Limnol. 28:1880-1884. Weisse, T., and S. Rammer. 2006. Pronounced ecophysiological clonal differences of two common freshwater ciliates, Coleps spetai (Prostomatida) and Rimostrombidium lacustris (Oligotrichida), challenge the morphospecies concept. J. Plankton Res. 28:55-63. Weisse, T., M. C. Strüder-Kypke, H. Berger, and W. Foissner. 2008. Genetic, morphological, and ecological diversity of spatially separated clones of Meseres corlissi Petz & Foissner, 1992 (Ciliophora, Spirotrichea). J. Eukaryot. Microbiol. 55:257-270. Wenzel, J. W., K. C. Nixon, and G. Cuccudoro. 2004. Dites non au PhyloCode! Bull. Soc. Fr. Syst. 31:19-23. West, S. A., C. M. Lively, and A. F. Read. 1999. A pluralist approach to sex and recombination. J. Evol. Biol. 12:1003-1012.
219
Wheeler, Q. D. 2008. Undisciplined thinking: morphology and Hennig's unfinished revolution. Syst. Entomol. 33:2-7. Wikmark, O.-G., P. Haugen, E. W. Lundblad, K. Haugli, and S. D. Johansen. 2007. The molecular evolution and structural organization of group I introns at position 1389 in nuclear small subunit rDNA of myxomycetes. J. Eukaryot. Microbiol. 54:4956. Williams, D., and J. C. Clamp. 2007. A molecular phylogenetic investigation of Opisthonecta and related genera (Ciliophora, Peritrichia, Sessilida). J. Eukaryot. Microbiol. 54:317-323. Williams, G. C. 1975. Sex and evolution. Princeton University Press, Princeton. Wright, A.-D. G., and D. H. Lynn. 1997. Maximum ages of ciliate lineages estimated using a small subunit rRNA molecular clock: crown eukaryotes date back to the paleoprotoerozoic. Arch. Protistenk. 148:329-341. Wu, Z. Y., A. M. Lu, Y. C. Tang, Z. D. Chen, and D. Z. Li. 2002. Synopsis of a new "polyphyletic-polychronic-polytopic" system of the angiosperms. Acta Phytotax. Sin. 40:2289-2322. Ye, A., J., and D. P. Romero. 2002. Phylogenetic relationships amongst tetrahymenine ciliates inferred by a comparison of telomerase RNAs. Int. J. Syst. Evol. Microbiol. 52:2297-3202. Yi, Z., W. Song, A. Warren, D. M. Roberts, K. A. S. Al-Rasheid, Z. Chen, S. A. AlFarraj, and X. Hu. 2008. A molecular phylogenetic investigation of Pseudoamphisiellla and Parabirojima (Protozoa, Ciliophora, Spirotrichea), two genera with ambiguous systematic positions. Eur. J. Protistol. 44:45-53. Yoon, H. S., J. Grant, Y. I. Tekle, M. Wu, B. C. Chaon, J. C. Cole, J. M. Logsdon, D. J. Patterson, D. Bhattacharya, and L. A. Katz. 2008. Broadly sampled multigene trees of eukaryotes. BMC Evol. Biol. 8:14. Zufall, R. A., C. L. McGrath, S. V. Muse, and L. A. Katz. 2006. Genome architecture drives protein evolution in ciliates. Mol. Biol. Evol. 23:1681-1687.
220
