Patterns of genetic and morphologic diversity in Antarctic sponges = Modelos de diversidad genética y morfológicas en las esponjas antárcticas

Abstract

The Antarctic bottoms harbour rich communities of sponges, which play an important role in structuring benthic habitats. Many Antarctic sponge species have been discovered in the past but most of them were poorly described or incorrectly ascribed to species or genera. Thus, the biodiversity this area is still incompletely explored. However, in the last 20 years the taxonomic and ecological studies of marine benthic invertebrates have benefited from the use of molecular tools, such a mitochondrial and nuclear markers or species-specific markers obtained from sequencing a part of the sponge genome. The present thesis contributed to improve the systematic of an Antarctic sponge group and its phylogenetic relationships with other members of the family (Tetillidae) spread all over the world, and to assess the asexual reproduction rate of an Antarctic sponge species (Stylocordyla chupachups). The phylogeny of Tetillidae has been previously approached using several nuclear and mitochondrial markers but including an incomplete number of Antarctic species. This study, did not resolve completely the family phylogeny and lacked a deep morphological revision of the species sequenced. Hence, in this thesis we performed a new phylogenetic analysis of the family by adding more Antarctic specimens and additional mitochondrial and nuclear markers. Moreover, the morphological characters plus the secondary structure of the (V4) region of the 18S rDNA were analyzed under the principle of maximum parsimony. The resulting trees retrieved seven monophyletic well-supported clades in both the molecular and morphological phylogenies, which correspond to the genera: Cinachyra, Acanthotetilla, Tetilla, Cinachyrella, Craniella, Antarctotetilla and Levantiniella. However, the mitochondrial and nuclear markers used were very conserved and could not discriminate Antarctic species of their corresponding genera (Antarctotetilla and Cinachyra). The revision of the species type of Tethya coactifera and Tethya crassispicula with the COI minibarcode sequence (useful for sequences with degraded DNA) confirmed that these two species were within the Antarctic clade, but the minibarcode was not informative at genus or species levels. Antarctotetilla and Levantiniella are described for the first time in this thesis. The main diagnostic traits of these genera are: pores grouped in small surface depressions and a slight cortical region (pseudocortex) in Antarctotetilla, and small surface cavities that resemble porocalices in Levantiniella. A detailed morphological revision of the types T. coactifera and T. crassispicula, confirmed that they belong to Antarctotetilla and Cinachyra, respectively. A new Antarctotetilla species (Antarctotetilla pilosa) was also described. On the other hand, we performed a genetic study of three populations of S. chupachups, using microsatellites, to test the hypothesis of a relatively higher asexual reproduction rate in Antarctic sponges due to the Antarctic stable environment and the selection of adapted genotypes. Our analysis proved that the 25% of the populations reproduce asexually, which represents a higher rate with respect to that reported for non-Antarctic sponge species. The three populations were slightly but significantly structured, which indicates a low genetic connectivity. Heterozygote excess was found in the three study populations. Relatively elevated rates of clonal reproduction and heterozygote excess are traits rarely found in sponge species from other latitudes and can be related to the particular environmental characteristics and the evolutionary history of the Antarctic. A founder effect was found in two of the study populations, which agrees with the pioneer nature reported for the species. At first sight, low genetic diversity resulting from a high rate of clonal reproduction would suggest vulnerability of sponge populations in the Antarctic ecosystems. However, compensatory genetic mechanisms, such an ancestral selection for heterozygotes, may be acting, and together with sexual reproduction, may preserve the minimal genetic diversity in S. chupachups populations to success in the Antarctic.

Esta tesis estudia las esponjas antárticas desde varios puntos de vista, utilizando especies ad hoc como “casos de estudio”. En primer lugar, analiza la sistemática y filogenia de la familia Tetillidae, muy bien representada en la Antártida. La filogenia molecular de Tetillidae había sido previamente estudiada pero los resultados no resolvieron las relaciones filogenéticas de todos los géneros analizados. Además, el estudio incluía un bajo número de especies antárticas. En esta tesis se pretende mejorar la filogenia de Tetillidae, incluyendo un número mayor de especies antárticas y utilizando marcadores moleculares adicionales. La filogenia molecular se complementó con un análisis filogenético de caracteres morfológicos bajo el criterio de máxima parsimonia. Los resultados mostraron que la familia está dividida en siete clados, dos de los cuales corresponden a los nuevos géneros: Antarctotetilla y Levantiniella. Los marcadores moleculares utilizados no discriminan las especies de los géneros Cinachyra y Antarctotetilla. Revisiones morfológicas y moleculares (partición minibarcode del COI) de los tipos de las especies Tethya coactifera y Tethya crassispicula confirmaron que estas especies pertenecen a los géneros Antarctotetilla y Cinachyra, respectivamente. Además, se describió una nueva especie de Antarctotetilla denominada A. pilosa. Una segunda parte de la tesis aborda el estudio genético de tres poblaciones de la especie Stylocordyla chupachups (Demospongiae, Suberitida), con un particular enfoque en la importancia de la reproducción asexual en las esponjas antárcticas, como adaptación al ambiente estable de los fondos antárticos. Se utilizaron ocho marcadores microsatélites seleccionados a partir de la secuenciación masiva de una parte del genoma de la especie. Los resultados mostraron que el 25% de la población se reproduce asexualmente, lo que representa una tasa alta comparada con las de esponjas de otras latitudes. Contrariamente a lo que se ha descrito en otras poblaciones de esponjas, las poblaciones de S. chupachups mostraron un exceso de heterocigotos. Las poblaciones estaban estructuradas, indicando un bajo flujo génico. Dos poblaciones presentaban un efecto fundador lo que confirma la naturaleza colonizadora de esta especie, sugerida en base a observaciones de su rápida colonización de áreas arrasadas por el efecto de los icebergs.