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Genetic Diversity, Biogeography and the Morpho-Genetic Relationship in Extant Planktonic Foraminifera

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Genetic Diversity, Biogeography and the Morpho-Genetic Relationship in Extant Planktonic Foraminifera Genetic diversity, biogeography and the morpho-genetic relationship in extant planktonic foraminifera Dissertation zur Erlangung des Doktorgrades in den Naturwissenschaften (Dr. rer. nat.) im Fachbereich Geowissenschaften der Universität Bremen vorgelegt von Agnes Katharina Maria Weiner Bremen, Mai 2014 1. Gutachter: Prof. Dr. Michal Kucera, MARUM – Zentrum für marine Umweltwissenschaften, Universität Bremen, Deutschland 2. Gutachter: Prof. Dr. Kate Darling, School of GeoSciences, University of Edinburgh and School of Geography and GeoSciences, University of St Andrews, Großbritannien Datum der Abgabe: 05.05.2014 Datum der Verteidigung: 11.07.2014 (Photos on title page: WG Kucera) PREFACE Preface The present PhD thesis was prepared at the Department of Geosciences at the University of Tübingen and the MARUM – Center for Marine Environmental Sciences at the University of Bremen, Germany. The work was financed by the “Landesgraduiertenförderung Baden- Württemberg” and by grant KU 2259/19 from the Deutsche Forschungsgemeinschaft (DFG) as part of the OPOCA project. Planktonic foraminifera samples for genetic analysis were collected and processed during five research expeditions to the Mediterranean Sea, Atlantic, South China Sea and the Southern Pacific on the research vessels R/V MARIA S. MERIAN (cruise MSM15/5), R/V POSEIDON (cruises P411 and P413) and R/V SONNE (cruises SO221 and SO226/3). In addi- tion, four research stays were carried out at the marine laboratories at Villefranche sur Mer, France, the Interuniversity Institute in Eilat, Israel, the Estación Costera de Investigaciones Marinas in Las Cruces, Chile and the Isla Magueyes Laboratories in La Parguera, Puerto Rico. The visits to the marine stations in Chile and Israel were financed by the EU FP7 research infrastructure initiative ASSEMBLE and the field trip to Puerto Rico was part of the OPOCA DFG project. The obtained planktonic foraminifera dataset was enlarged with samples from the collections of the working group and from various coauthors, as indicated for each study separately. The eight chapters of this thesis comprise four research papers dealing with the genetic diversity, biogeography and a potential correlation of morphology and genetics in living planktonic foraminifera. Chapter 1 introduces the model organisms from a biological as well as paleontological perspective. It describes the marker gene that is used in the genetic analysis of planktonic foraminifera and elaborates the problem of cryptic diversity within the traditional morphospecies. The following section presents different modes of speci- ation and biogeographical distribution patterns that can be found in plankton organisms. Chapter 2 outlines the motivation and major research questions of this thesis and Chapter 3 describes the methods applied in the molecular analysis of planktonic foraminifera. Chapters 4–7 include the actual case studies that were carried out in the framework of this thesis, in the form of published or submitted research papers and Chapter 8 presents a general conclusion on the results of the studies and an outlook for future work. 3 EXTANT PLANKTONIC FORAMINIFERA 4 CONTENTS Table of Contents Abstract 07 Zusammenfassung 19 Chapter 1: Introduction 11 1.1. The biology of extant planktonic foraminifera 11 1.2. The fossil record of planktonic foraminifera 15 1.3. Genetic diversity of planktonic foraminifera 18 1.4. Speciation and biogeographic distribution patterns in plankton 24 Chapter 2: Motivation and Objectives 29 Chapter 3: Methods applied in single-cell foraminifera genetics 31 3.1. Sampling of planktonic foraminifera 31 3.2. Culturing of planktonic foraminifera 32 3.3. DNA extraction and molecular analysis 33 Chapter 4: First case study: Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protist. Molecular Ecology 35 Chapter 5: Second case study: The cryptic and the apparent reversed: lack of genetic differentiation within the morphologically diverse plexus of the planktonic foraminifer Globigerinoides sacculifer. Paleobiology 49 Chapter 6: Third case study: Phylogeography of the tropical planktonic foraminifera lineage Globigerinella reveals isolation inconsistent with passive dispersal by ocean currents. PLoS ONE 71 Chapter 7: Fourth case study: Genetic and morphometric evidence for parallel evolution of the Globigerinella calida morphotypes. Marine Micropaleontology 85 Chapter 8: Concluding remarks and Perspectives 119 8.1. Implications of the results 119 8.2. Remaining limitations 125 8.3. Future perspectives 126 References 129 Acknowledgements 141 Erklärung 143 5 EXTANT PLANKTONIC FORAMINIFERA 6 ABSTRACT Abstract The fossil record of planktonic foraminifera grants this group an exceptional position among marine microplankton. Foraminifera have a long tradition as proxies for the reconstruction of past ocean and climate conditions and therefore, the fossilized shells are very well studied, including evolutionary processes and phylogenetic relationships since their origin in the Jurassic. For their classification, the morphological species concept has been applied, which distinguishes about 50 different species among the modern representatives, based on the ultrastructure of their calcite shells. With the application of molecular genetic approaches on living planktonic foraminifera, the classical species concept has been challenged by the discovery of a large number of cryptic species “hidden” within the morphospecies. The total amount of cryptic diversity and its distribution between the different morphospecies, however, are still not completely resolved. In contrast to the mainly cosmopolitan occur- rences of the morphospecies, many of the cryptic species exhibit differentiated distribution patterns in the ocean, marked by local adaptations to environmental factors. A morphological separation of the sibling species, however, proved very difficult and was so far only possible after detailed morphometric studies. The present thesis aims at contributing to the ongoing research on living planktonic foraminifera, by studying the genetic diversity within three selected morphospecies, the biogeographical distribution patterns of their cryptic species and the relationship between genetic and morphological variability. The study on Hastigerina pelagica examined its genetic diversity and biogeographical dis- tribution in the Mediterranean Sea, Atlantic, Caribbean Sea and the Western Pacific. Only three already known cryptic species were discovered and they were shown to exhibit a global distribution in the ocean, but vertical segregation in the water column. For the analysis of Globigerinoides sacculifer, a high number of samples from around the world was amassed, including all different morphotypes of this highly variable plexus, that were, however, revealed to be genetically completely homogenous. The third species that was chosen for analysis was Globigerinella siphonifera that is marked by a high genetic as well as morphological variability. The examination of a large number of samples allowed the com- plete resolution of its cryptic diversity and a separation of the plexus into three species. Despite an extensive sampling effort, the number of newly detected cryptic species from these studies was unexpectedly low. This indicates that for the well-studied morpho- species most cryptic species might by now be detected and that genetic variability is not even prevalent in all morphospecies. The results presented in this thesis further imply that the amount of genetic diversity cannot be predicted from the characteristics of a morpho- species. The correlation of morphological traits with genetic variability appeared to be possible to some extent in the studied morphospecies, however, generally speaking, mor- phology and genetics of planktonic foraminifera appear to evolve rather independently of each other. The biogeographical distribution patterns of the cryptic species of the studied morphospecies speak for a prevalence of large scale dispersal and gene flow in planktonic foraminifera, while at the same time possibilities are given for the establishment of 7 EXTANT PLANKTONIC FORAMINIFERA reproductive isolation, such as in the vertical dimension in the water column or by local adaptations to different ecological parameters. 8 ZUSAMMENFASSUNG Zusammenfassung Der fossile Befund planktonischer Foraminiferen verleiht dieser Organismengruppe eine außergewöhnliche Position innerhalb des marinen Mikroplanktons. Ihre Nutzung als Proxies für die Rekonstruktion vergangener Ozean- und Klimabedingungen hat eine lange Tradition, was zur Folge hat, dass ihre fossilisierten Schalen sehr gut untersucht und ihre Evolution und phylogenetischen Verhältnisse seit ihres ersten Auftretens im Jura genau bekannt sind. Für die Klassifikation der Arten wurde das morphologische Artkonzept zu Grunde gelegt, das die modernen Vertreter basierend auf der Struktur ihrer kalzitischen Schale in ca. 50 Arten unterteilt. Die Anwendung molekulargenetischer Methoden an planktonischen Foraminiferen stellte das klassische Artkonzept allerdings in Frage, da eine große Zahl kryptischer Arten innerhalb der morphologischen Arten entdeckt wurde. Das komplette Ausmaß dieser kryptischen Diversität sowie seine Verteilung zwischen den morphologischen Arten konnten bisher nicht im Detail geklärt werden. Im Gegensatz zu den morphologischen Arten, die sich größtenteils durch eine globale Verbreitung aus- zeichnen, weisen die kryptischen Arten eher differenzierte Verbreitungsmuster
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