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Phylogenetic Hypotheses of Octocoral Species Using Predicted RNA Secondary Structures of the Internal Transcribed Spacer 2 (ITS2)

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Phylogenetic Hypotheses of Octocoral Species Using Predicted RNA Secondary Structures of the Internal Transcribed Spacer 2 (ITS2) Phylogenetic hypotheses of octocoral species using predicted RNA secondary structures of the internal transcribed spacer 2 (ITS2) Catalina Aguilar Hurtado UNIVERSIDAD DE LOS ANDES FACULTAD DE CIENCIAS DEPARTAMENTO DE CIENCIAS BIOLOGICAS BOGOTA D.C. 2006 Phylogenetic hypotheses of octocoral species using predicted RNA secondary structures of the internal transcribed spacer 2 (ITS2) Catalina Aguilar Hurtado A thesis submitted in partial fulfillment of the requirements for the degree of BIOLOGIST Director JUAN ARMANDO SANCHEZ Marine Biologist Ph.D Codirector SILVIA RESTREPO Biologist Ph.D UNIVERSIDAD DE LOS ANDES FACULTAD DE CIENCIAS DEPARTAMENTO DE CIENCIAS BIOLOGICAS BOGOTA D.C. 2006 2 ABS TRACT Octocoral systematics is a relatively new field of study. Morphological aspects together with molecular identification are tools that have been recently applied to solve systematic questions in octocorals due to their intricate morphology. For this group, as for many others, the use of a molecular marker that solves systematic problems at different taxonomic levels would be extremely useful for species identification and classification. Here we use the internal transcribed spacer 2 (ITS2) predicted RNA secondary structure for reconstructing phylogenetic hypotheses at different taxonomic levels. These structures are very important for the ribosome assembly since they are involved in mRNA folding and processing. For this reason, mutations that do not enable the proper folding of the sequence have to be compensated or suppressed. Hence, ITS2 are said to evolve in concert, which leads to a homogenization of all the copies of this gene throughout the genome. ITS2 secondary structures are useful for higher taxonomy systematics because a common core of the structures has being found. The secondary structures presented here, in the majority of octocoral species, have the six helicoidal ring model presented in Acropora spp. and other eukaryotes such as yeast, dinoflagellates, arthropods and mammals among others, they have the typical hallmarks that are standard for ITS2 . With these molecular and structural guides, a molecular morphometrics approach was made for solving phylogenies. In this study there were three taxonomic levels: (1) interfamily, between Plexauridae and Gorgoniidae, (2) intrafamily, within Gorgoniidae species, and (3) intrageneric, within the Eunicea genus. The tree parts of this thesis are presented as standing alone chapters, which correspond to articles in press or recently submitted to peer review at indexed journals. For all of these analyses, saturation plots were made. In the first approach, saturation was complete since transversions were considerably more frequent than transitions; in the last two approaches, saturation was also found but in a lesser degree. This was made for reassuring the importance of using secondary structure and not the primary sequence alignment for phylogenetic reconstruction at this level. Moreover, direct 3 comparisons between primary and secondary alignment (e.g., molecular morphometrics) phylogenies were made in order to find differences between these two approaches. M olecular morphometrics interfamily analyses gave high support to the recently described species Alaskagorgia aleutiana as a member of the Plexauridae family, in consequence with previous mtDNA results. This analysis also retained clades from the two families of octocorals that were studied. At the intrafamily level the phylogenetic hypotheses using molecular morphometrics gave high support to the placement of Africagorgia schoutedeni and A. africana within a Gorgoniidae clade. Whereas, the same species were placed as a basal clade in the non-morphometrics phylogram using the primary sequence alignment. Muriceopsis spp. had certain secondary structure characteristics that drove this taxon as a basal clade in respect with other gorgoniids in the molecular morphometrics analysis. Moreover, long-branch attraction was found for Plexaurella nutans and Pterogorgia citrina species, which mean that they had to be excluded from the analysis. For this reason, the systematic positioning of Plexaurella spp., Pterogorgia citrina and Muriceopsis spp. is still unresolved. For the lowest taxonomical level analyzed, molecular morphometrics was combined with secondary structure alignment using Bayesian inference and partitions for each helix producing a well-supported phylogram. Eunicea flexuosa, a divergent species previously classified within the outgroup Plexaura, was given high support as part of Eunicea, which corroborated what has been found with the primary alignment and morphological characters. M olecular morphometrics results differed from the primary alignment at species from the Euniceopsis subgenus that were placed grouping the outgroups Pseudoplexaura and Plexaura whereas E. mammosa was placed inside the Eunicea subgenus. As morphological characters have been found to be highly homoplasic in octocorals, molecular data are important to reconstruct octocoral systematics. For this reason, the addition of 4 ITS2 secondary structures brings more characters and hence more credibility to Eunicea systematics. ITS2 molecular morphometrics is presented here as a new and promising phylogenetic tool. This sequence has proven to be important for the organism ribosome’s proper function and it turned out to be a useful marker for studying octocoral systematics. Even though more octocorals representatives are needed to resolve most of this subclass systematics, this study relying on ITS2 secondary structures for reconstructing phylogenies at different taxonomic levels demonstrated the great potential of ITS2 and molecular morphometrics for diverse systematic applications. 5 Hipótesis filogenética de especies de octocorales utilizando estructuras secundarias del espaciador interno transcrito 2 (ITS2) RESUMEN Debido a su compleja morfología la sistemática de octocorales es una nueva área de estudio; recientemente han sido aplicadas herramientas como identificación molecular, junto con aspectos morfológicos, para resolver preguntas sobre la sistemática de los octocorales. Para este grupo, como para muchos otros, se podría utilizar marcadores moleculares para resolver problemas sistemáticos a diferentes niveles taxonómicos, estos serían de gran ayuda para la identificación y clasificación de especies. En este estudio se utilizó el modelo de estructura secundaria del espaciador interno transcrito 2 (ITS2) del ARN para construir hipótesis filogenéticas a diferentes niveles taxonómicos. Estas estructuras son muy importantes para el ensamblaje de ribosomas, ya que estan involucradas en el pliegue y procesamiento correcto del ARNm. Por esta razón, mutaciones que no permitan la adecuada formación de estas estructuras serán compensadas o eliminadas. Como consecuencia de lo anterior se ha propuesto que el ITS2 evoluciona en concierto, lo que lleva a una homogenización de todas las copias de este gen en el genoma. Las estructuras secundarias del ITS son útiles para la identificación taxonómica, ya que se a encontrado una forma común en todas las estructuras construidas. Según los resultados en la mayoría de especies de octocorales las estructuras secundarias del ITS2 mostraron las típicas marcas presentes en ciertos corales y otros eucariotas como levaduras, dinoflagelados, artrópodos, y mamíferos entre otros, estos presentan un modelo de seis hélices con un anillo central. Estas guías moleculares y estructurales se utilizaron para resolver filogenias por medio de morfometría molecular. En este estudio se analizaron tres niveles taxonómicos: (1) interfamiliar, entre la familia Plexauridae y Gorgoniidae, (2) intrafamiliar, entre las especies de Gorgoniidae, e 6 (3) intragenérico, dentro del género Eunicea. Las tres partes de esta tesis son presentadas por capítulos separados, que corresponden a artículos publicados o recientemente sometidos a revisión en revistas indexadas. Para estos análisis se realizaron gráficas de saturación. En el mayor nivel (interfamiliar) la saturación del alineamiento primario fue completa, ya que las transversiones fueron considerablemente más frecuentes que las transiciones, en los dos niveles restantes también se presentó saturación pero en menor grado. Esto se realizó con el fin de comprobar la importancia de utilizar estructuras secundarias y no el alineamiento primario para la reconstrucción filogenética en estos niveles. Adicionalmente, se realizaron comparaciones directas entre las filogenias del alineamiento primario y secundario (e.g., morfometría molecular) para encontrar diferencias entre las dos metodologías. El análisis de morfometría molecular interfamiliar mostró altos soportes a la especie recientemente descrita Alaskagorgia aleutiana que hace parte de la familia Plexauridae, lo cual es consecuente con resultados obtenidos anteriormente con ADN mitocondrial. Este análisis también retiene clados de las dos familias de octocorales estudiadas. Las hipótesis filogenéticas utilizando morfometría molecular a nivel intrafamiliar mostraron un alto soporte de las especies Africagorgia schoutedeni y A. africana dentro del clado de Gorgoniidae. Por otro lado estas mismas especies se encontraron básales en filogramas que no eran de morfometría sino de alineamiento primario de las secuencias. Las especies del género Muriceopsis presentaron ciertas características en sus estructuras secundarias que las llevaron a posicionarse basalmente con respecto a las demás gorgonias en el análisis de morfometría molecular. Así mismo,
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