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Copyright by Andrew James Alverson 2006 Copyright by Andrew James Alverson 2006 The Dissertation Committee for Andrew James Alverson certifies that this is the approved version of the following dissertation: Phylogeny and evolutionary ecology of thalassiosiroid diatoms Committee: ________________________________ Edward C. Theriot, Supervisor ________________________________ David M. Hillis ________________________________ Robert K. Jansen ________________________________ John W. La Claire II ________________________________ C. Randal Linder Phylogeny and evolutionary ecology of thalassiosiroid diatoms by Andrew James Alverson, B.S.; M.S. Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin August 2006 Phylogeny and evolutionary ecology of thalassiosiroid diatoms Publication No. _________ Andrew James Alverson, Ph.D. The University of Texas at Austin, 2006 Supervisor: Edward C. Theriot Salinity is a significant barrier to the distribution of diatoms, and though it is generally understood that diatoms are ancestrally marine, the number of times diatoms independently colonized fresh waters and the adaptations that facilitated these colonizations remain outstanding questions in diatom evolution. Resolving the exact number of freshwater colonizations will require large-scale phylogenetic reconstruction with dense sampling of marine and freshwater taxa. A more tractable approach to understanding the marine–freshwater barrier is to study a group of diatoms with high diversity in each habitat. The "centric" diatom order Thalassiosirales affords an excellent opportunity to study the origin and evolution of diatoms in fresh waters. Thalassiosirales is a well-supported monophyletic group common in marine, brackish, and freshwater habitats. Thalassiosirales species historically are classified into the marine Thalassiosiraceae or freshwater Stephanodiscaceae, reflecting the more generally held hypothesis that diatoms are naturally split along marine–freshwater lines. The fossil record suggests that Stephanodiscaceae traces to a single colonization of freshwater in the mid-Miocene, and in addition, Stephanodiscaceae species share a suite of complex cell iv wall characters, which has been interpreted as corroborating evidence for their monophyly. I reconstructed the phylogeny of Thalassiosirales and used the phylogeny to test these and other hypotheses and to address a number of other problems related to the marine–freshwater boundary in diatoms. Phylogenetic analyses showed strong evidence for multiple colonizations of freshwater and reject all previous colonization hypotheses. Results further show that part of Stephanodiscaceae is an early diverging lineage within Thalassiosirales, indicating that these two distantly related and separately derived Stephanodiscaceae lineages independently evolved a similar set of complex morphological features upon or shortly after the colonization of fresh waters. Finally, marine and freshwater diatoms, including Thalassiosirales, show several important differences in silicon physiology. In addition to containing an order of magnitude more silica in their cell walls, freshwater diatoms have a drastically lower enzymatic affinity for silicic acid, the dissolved form of silica used by diatoms. I sequenced the silicon transporter genes from marine and freshwater Thalassiosirales and show that physiological differences are not due to differences in the coding sequence. v Table of Contents List of tables......................................................................................................................vii List of figures....................................................................................................................viii Chapter 1. Introduction........................................................................................................1 Chapter 2. Stampeding the Rubicon: phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms...............8 Introduction...................................................................................................................9 Materials and Methods................................................................................................13 Results.........................................................................................................................20 Discussion....................................................................................................................25 Literature Cited............................................................................................................32 Chapter 3. Massive convergent evolution in morphology associated with the colonization of fresh waters in diatoms...............................................................................74 Introduction.................................................................................................................75 Materials and Methods................................................................................................79 Results.........................................................................................................................83 Discussion....................................................................................................................87 Literature Cited............................................................................................................93 Chapter 4. Strong purifying selection in the silicon transporters of marine and freshwater diatoms..........................................................................................................107 Introduction...............................................................................................................108 Materials and Methods..............................................................................................113 Results.......................................................................................................................117 Discussion..................................................................................................................121 Literature Cited..........................................................................................................127 Chapter 5. Cell wall morphology and systematic importance of Thalassiosira ritscheri (Hustedt) Hasle, with a description of Shionodiscus gen. nov......................147 Introduction...............................................................................................................148 Materials and Methods..............................................................................................149 Results.......................................................................................................................151 Discussion..................................................................................................................153 Literature Cited..........................................................................................................162 Appendix..........................................................................................................................172 Bibliography....................................................................................................................176 Vita...................................................................................................................................198 vi List of Tables Table 2.1. Taxa, culture strains, and GenBank accession numbers for chloroplast psbC and rbcL sequences used in Chapter 2................................................. 56 Table 2.2. Taxa, culture strains, and GenBank accession numbers for nuclear SSU and partial LSU rDNA sequences used in Chapter 2..................................... 64 Table 2.3. Oligonucleotide primers used to amplify and sequence SSU rDNA, partial LSU rDNA, psbC, and rbcL fragments from Thalassiosirales..............................................................................................72 Table 2.4. Data partitions, models of DNA sequence evolution, and results of Bayesian analyses, including Bayes factor comparisons of alternative models............................................................................................................73 Table 3.1. Maximum likelihood assessment of correlated evolution between habitat type and each of five morphological characters traditionally used to diagnose the predominantly freshwater Stephanodiscaceae..........................106 Table 4.1. Taxon, culture strain, habitat, and GenBank accession number for silicon transporter sequences analyzed in Chapter 4.................................................139 Table 4.2. Number of free parameters (p), log-likelihood (l), and parameter estimates for random-sites and clade models................................................................ 143 Table 4.3. Likelihood ratio test statistics (2Δ l), degrees of freedom (df), and p-values for comparisons of random-sites and clade models.......................................144 Table 4.4. Number of free parameters (p, including parameters for codon frequencies), log-likelihood (l), and parameter estimates for fixed-sites models that distinguished internal and external segments (partition 1) from transmembrane segments (partition 2)...........................................................145
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