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The Pennsylvania State University the Graduate School Eberly The Pennsylvania State University The Graduate School Eberly College of Science SPECIES DISTRIBUTIONS AND POPULATION STRUCTURE IN COLD SEEP VESTIMENTIFERAN TUBEWORMS OF THE GENERA ESCARPIA AND LAMELLIBRACHIA (POLYCHAETA, SIBOGLINIDAE) A Dissertation in Biology by Dominique Alexandria Cowart © 2013 Dominique Alexandria Cowart Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy August 2013 The dissertation of Dominique Alexandria Cowart was reviewed and approved* by the following: Charles R. Fisher Professor of Biology Dissertation Co-Adviser Stephen W. Schaeffer Professor of Biology Dissertation Co-Adviser Kateryna Makova Professor of Biology Chair of Committee Christopher House Professor of Geosciences Douglas R. Cavener Professor of Biology Head of the Department of Biology *Signatures are on file in the Graduate School iii ABSTRACT Deep-sea cold seeps support diverse biological communities that rely on the seepage of hydrocarbon gases and fluids. Due to their dependence on irregularly occurring seepage, vestimentiferan tubeworms (Family: Siboglinidae) have patchy distributions on the seafloor. Tubeworms of the genera Escarpia and Lamellibrachia are important components of seep ecosystems, as they form long-lived aggregations that provide habitat for a variety of other deep- sea fauna. Three described species of Escarpia, E. spicata (Gulf of California), E. laminata (Gulf of Mexico) and E. southwardae (West African Cold Seeps), have been identified as one species through the use of mitochondrial markers Cytochrome Oxidase subunit 1 (mtCOI) and large ribosomal subunit rDNA, (mt16S), despite their geographic differences and dissimilar morphologies. Three morphologically distinct groups of Lamellibrachia are present over a bathymetric range of almost 3000m in the Gulf of Mexico; these include L. luymesi (<1000m) and two unnamed groups, L. sp. 1 and L. sp. 2 (>1000m). As with the Escarpia, mtCOI and mt16S identifies L. luymesi and L. sp. 1 as one species despite their differing depth ranges and dissimilar morphologies. This dissertation seeks to define the geographic and bathymetric ranges of Escarpia and Lamellibrachia by determining if geographically differentiated Escarpia and depth differentiated Lamellibrachia are genetically distinct within each respective group. For these investigations, we make use of molecular, morphological and environmental data, all of which are necessary to ascertain population boundaries and evolutionary processes occurring in the deep sea. Here we use Exon Priming Intron Crossing (EPIC) sequencing of a nuclear gene, and develop microsatellite markers with the aid of 454 and Illumina next generation sequencing to 1) iv determine if the described taxa are genetically differentiated and 2) identify possible population structure at the regional scale within the Gulf of Mexico and West Africa, respectively. To identify if the three Escarpia groups are genetically distinct, we have tested the mitochondrial gene Cytochrome B (CYTB) for its utility as a phylogenetically informative marker, as well as developed and analyzed the EPIC marker Hemoglobin subunit B2 intron (HbB2i) and 28 microsatellites in 229 Escarpia individuals collected from 12 seep sites around the world. Nine of the microsatellites were amplified across the three Escarpia taxa, and while CYTB identifies two groups rather than three, both HbB2i and the cross-amplified microsatellites support the occurrence of three genetically distinct groups of Escarpia based on geography. At the regional scale among eight sampling sites of E. laminata (n =129) and among three sampling sites of E. southwardae (n =80), no population structure was detected. To identify if the two Lamellibrachia groups are genetically distinct, we also tested CYTB, HbB2i and eight microsatellites in 76 Lamellibrachia individuals collected from 13 seep sites in the Gulf of Mexico. All eight of the microsatellites were amplified across 45 L. luymesi and L. sp.1, and while both CYTB and HbB2i identify L. luymesi and L. sp. 1 as a single group, the cross-amplified microsatellites support the occurrence of two genetically distinct groups. At the regional scale among eight sampling sites of L.sp.1 (n =24) and among six sampling sites of L. sp.2 (n =31), no population structure was detected. Findings in this dissertation illustrate that 1) nuclear markers support original morphological descriptions of Escarpia and Lamellibrachia, suggesting that each group is constrained to their respective geographic or bathymetric region, 2) despite the patchiness and isolation of seep habitats, connectivity is high on regional scales, 3) mitochondrial markers should be used with extreme caution when attempting to detect differentiation in seep vestimentiferan groups, and lastly 4) microsatellites may be another useful tool to determine v genetic differentiation between described species when divergence is insufficient or too recent to be detected using gene sequences alone. vi TABLE OF CONTENTS LIST OF FIGURES ................................................................................................................. ix LIST OF TABLES................................................................................................................... xii LIST OF ABBREVIATIONS.................................................................................................. xvi ACKNOWLEDGEMENTS..................................................................................................... xix CHAPTER1 Introduction and Motivation .............................................................................. 1 Cold seeps ........................................................................................................................ 2 Vestimentiferan tubeworms ............................................................................................. 4 The Escarpia tubeworms ................................................................................................. 5 The Lamellibrachia tubeworms ....................................................................................... 6 Larval biology and the influence of ocean currents on dispersal..................................... 8 Distributional ranges of deep sea invertebrates ............................................................... 9 Ecological genetics of cold seep vestimentiferans........................................................... 10 CHAPTER 2 Identification and amplification of microsattelite loci in deep-sea tubeworms of the genus Escarpia (Polychaeta, Siboglinidae)......................................... 13 Introduction...................................................................................................................... 14 Materials and Methods..................................................................................................... 15 Results and Discussion..................................................................................................... 16 Acknowledgements.......................................................................................................... 19 CHAPTER 3 Restriction to large-scale gene flow versus regional panmixia among cold seep Escarpia spp. (Polychaeta, Siboglinidae) ................................................................ 20 Abstract ............................................................................................................................ 21 Introduction...................................................................................................................... 22 Escarpia vestimentiferan tubeworms....................................................................... 23 Vestimentiferan larval biology................................................................................. 26 Defining vestimentiferan population structure......................................................... 27 Materials and Methods..................................................................................................... 28 Sample collection and preperation ........................................................................... 28 Sequencing and EPIC development ......................................................................... 30 Sequencing analyses................................................................................................. 32 Microsattelite analyses ............................................................................................. 33 Results.............................................................................................................................. 35 Mitochondrial and EPIC sequencing analysis.......................................................... 35 Genetic differentiation between Escarpia groups.................................................... 37 Escarpia laminata population genetics.................................................................... 39 Escarpia southwardae population genetics.............................................................. 41 Discussion ........................................................................................................................ 42 vii Barriers to gene flow across large scales ................................................................. 42 Influence of deep currents on dispersal and recruitment of Escarpia...................... 45 Conclusions.....................................................................................................................
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