RESUMO

The mechanisms underlying regeneration of the central nervous system (CNS) following lesions have been studied extensively in both vertebrate and invertebrate models. To shed light on regeneration, ascidians, a sister group of vertebrates and with remarkable ability to regenerate their brains, constitute an appropriate model system. Glial cells have been implicated in regeneration in vertebrates; however, their role in the adult ascidian CNS regeneration is unknown. A model of degeneration and regeneration using the neurotoxin 3-acetylpyridine (3AP) in the brain of the ascidian Styela plicata was used to identify astrocyte-like cells and investigate their role. We studied the CNS of control ascidians (injected with artificial sea water) and of ascidians whose CNS was regenerating (1 and 10 days after the injection with 3AP). Our results show that the mRNA of the ortholog of glutamine synthetase (GS), a glial-cell marker in vertebrates, is increased during the early stages of regeneration. Confirming the identity of GS, the protein was identified via immunostaining in a cell population during the same regeneration stage. Last, a single ortholog of GS (GSII) is present in ascidian and amphioxus genomes, while two types exist in fungi, some invertebrates, and vertebrates, suggesting that ascidians have lost the GSI type. Taken together, our findings revealed that a cell population expressing glial-cell markers may play a role in regeneration in adult ascidians. This is the first report of astrocyte-like cells in the adult ascidian CNS, and contributes to understanding of the evolution of glial cells among metazoans.

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Adult ascidians have the capacity to regenerate the central nervous system (CNS) and are therefore excellent models for studies on neuroregeneration. The possibility that undifferentiated blood cells are involved in adult neuroregeneration merits investigation. We analyzed the migration, circulation, and role of hemocytes of the ascidian Styela plicata in neuroregeneration. Hemocytes were removed and incubated with superparamagnetic iron oxide nanoparticles (SPION), and these SPION-labeled hemocytes were injected back into the animals (autologous transplant), followed by neurodegeneration with the neurotoxin 3-acetylpyridine (3AP). Magnetic resonance imaging showed that 1, 5, and 10 days after injury, hemocytes migrated to the intestinal region, siphons, and CNS. Immunohistochemistry revealed that the hemocytes that migrated to the CNS were putative stem cells (P-element-induced wimpy testis + or PIWI + cells). In the cortex of the neural ganglion, migrated hemocytes started to lose their PIWI labeling 5 days after injury, and 10 days later started to show ß-III tubulin labeling. In the neural gland, however, the hemocytes remained undifferentiated during the entire experimental period. Transmission electron microscopy revealed regions in the neural gland with characteristics of neurogenic niches, not previously reported in ascidians. These results showed that migration of hemocytes to the hematopoietic tissue and to the 3AP-neurodegenerated region is central to the complex mechanism of neuroregeneration.

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The developmental and evolutionary principles of coloniality in marine animals remain largely unexplored. Although many common traits have evolved independently in different groups of colonial animals, questions about their significance for colonial life histories remain unanswered. In 2018 (Nov. 25 - Dec. 8), the inaugural course on the Evolution of Coloniality and Modularity took place at the Center for Marine Biology of the University of São Paulo (CEBIMAR-USP), Brazil. During the intensive two-week graduate-level course, we addressed some of the historical ideas about animal coloniality by focal studies in bryozoans, tunicates, cnidarians, and sponges. We discussed many historical hypotheses and ways to test these using both extant and paleontological data, and we carried direct observations of animal colonies in the different phyla to address questions about coloniality. We covered topics related to multi-level selection theory and studied colonial traits, including modular miniaturization, polymorphism, brooding, and allorecognition. Course participants carried out short research projects using local species of animals to address questions on allorecognition and regeneration in ascidians and sponges, fusion and chimerism in anthoathecate hydrozoans, and evolution of polymorphism in bryozoans. Although many questions remain unanswered, this course served as a foundation to continue to develop a developmental and evolutionary synthesis of clonal and modular development in colonial marine organisms.

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Higher diversity and dominance at lower latitudes has been suggested for colonial species. We verified this pattern in species richness of ascidians, finding that higher colonial-to-solitary species ratios occur in the tropics and subtropics. At the latitudinal region with the highest ratio, in southeastern Brazil, we confirmed that colonial species dominate space on artificial plates in two independent studies of five fouling communities. We manipulated settlement plates to measure effects of predation and competition on growth and survivorship of colonial versus solitary ascidians. Eight species were subjected to a predation treatment, i.e. caged versus exposed to predators, and a competition treatment, i.e. leaving versus removing competitors, to assess main and interactive effects. Predation had a greater effect on growth and survivorship of colonial compared to solitary species, whereas competition did not show consistent patterns. We hypothesize that colonial ascidians dominate at this subtropical site despite being highly preyed upon because they regrow when partially consumed and can adjust in shape and space to grow into refuges. We contend that these means of avoiding mortality from predation can have large influences on diversification patterns of colonial species at low latitudes, where predation intensity is greater.

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Individuals of colonial animals (e.g. zooids) are in continuous turnover. In ascidians colonial or solitary species have evolved by convergence multiple times. Colonial Botryllus and Botrylloides are well-studied genera that exhibit colony-wide developmental mechanisms that regulate synchronous and orchestrated cycles of budding and turnover of zooids. The origins of modular developmental mechanisms that facilitated the evolution of coloniality in this group remain unclear. To reconstruct ancestral states of coloniality we studied Symplegma brakenhielmi, a sister taxon of the botryllids. S. brakenhielmi zooids are embedded in a common tunic and present a similar vascular system as the botrylloides, however development and turnover of zooids occurs asynchronously and in a more independent manner. We generated a table of common stages of budding in Symplegma and Botryllus for comparative studies of asexual development. We tested dependent processes of budding among individuals of the colony by systemic bud or zooid removals. Although our results showed a higher degree of independence in bud development in S. brakenhielmi, we found a subtle colony-wide regulatory mechanism of modular development, i.e. new buds expedited development after the removal of all buds in the colony. Next, we characterized external morphology, ultrastructure, and abundance of circulatory blood cells in the vascular system of S. brakenhielmi. Macrophage-like cells (MLCs) are involved in zooid resorption and turnover. Proportions of MLCs in the blood of S. brakenhielmi corresponded to the peak of occurrence of this cell type during the budding cycle of B. schlosseri. We found several new blood cell types in S. brakenhielmi, including two cell types that resemble circulatory progenitor stem cells of other botryllid colonial ascidians. These cells showed features of undifferentiated cells and expressed mitotic marker Phospho-histone H3. Comparative studies of S. brakenhielmi and B. schlosseri allow us to discuss possible changes in the regulation of modular development (i.e. regulation of life and death in the colony), and a possible contribution of circulatory blood cells in budding processes. We propose that the higher degree of developmental independence in S. brakenhielmi budding is a result of its ancestral solitary mode of development.

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Cysteine (Cys) is regarded as the most conservative amino acid in nature, something that does not occur in the tunicate Oikopleura dioica, where this amino acid is one of the fastest evolving. In this work we analyze some of the causes of this intriguing absence of conservation. Considering the well-known stabilizing role of Cys, it was first investigated whether the lack of conservation was accompanied by an increase in intrinsic protein disorder. In contrast to expectations, it was found that O. dioica is the chordate that has the lowest levels of intrinsic disorder, while vertebrates (represented by Bos taurus) contain the most disordered proteins. Oikopleura proteins are shorter than their homologs in other Chordates (Ciona and B. taurus proteins are respectively 11% and 18% longer). This process of protein shortening was more intense in intrinsic disordered regions. As a result proteins became not only shorter but also more compact. It is also reported here that the conservation/divergence behavior of Cys depends on whether they are located in ordered or disordered regions. In the four species analyzed, disordered Cys are majorly (> 75%) not conserved at all. Ordered Cys instead, are much more free to diverge in Oikopleura than in the other chordates. We hypothesize that the preferential deletion of disordered regions resulted in a decreased protein disorder and a direct elimination (by deletion) of many ancestral Cys. Besides, the alterations (shortening or complete elimination) of some disordered regions (loops/random coils) probably promoted further Cys evolutionary volatility, because some ancestral Cys (and other amino acids which play a role in stability like Trp) located outside deleted regions became redundant due to the loss of their stabilizing partners.

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This study describes the results from transcriptomes sequenced by 454-pyrosequencing from two populations separated by 10° of latitude of the endemic tunicate Pyura chilensis. Most transcripts were assembled in 43,972 contigs with an average length of 842 nucleotides. De novo assembly revealed that less than 30% of the contigs were annotated to Gene Ontology terms. A total of 71,662 single nucleotide polymorphisms (SNPs) were detected in 14,712 contigs. In silico differential expression of contigs annotated for SNPs revealed several genes differentially expressed in individuals collected from both populations. The present genomic resource will provide the basis to perform functional genomics on the species via the localization of genomic markers that can aid in determining levels of local adaptation, overall genetic structure and the genetic assessment of restocking programs for this species.

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Gorgona National Park protects fertile waters that support large vertebrates, including green sea turtles (Chelonia mydas), and for them, gelatinous zooplankton constitute a food resource that can be found year-round in Gorgona Island´s coastal waters. This study was carried out to determine the abundance of salps and doliolids around Gorgona Island over a year, and to determine whether this is a resource that could be used reliably year-round by green turtles and other large plankton-feeding predators. The monthly abundance of salps and doliolids at eight coastal stations around Gorgona Island (Colombian Pacific) was determined between September 2005 and August 2006. Oblique tows were carried out from 50m to the surface, total zooplankton biomass was measured and the number of salps and doliolids per tow, and frequency of occurrence per station and month were determined. Superficial and bottom sea temperature, superficial and bottom salinity, and chlorophyll-a concentration were recorded at each station. There were tunicate abundance peaks in September 2005 and March 2006. The high abundances in March were probably due to a cold water intrusion into the study area, which resulted in colder saltier water and a shallower thermocline. Tunicates were probably advected to the area by currents from the southwest and aggregated due to the underwater topography. In September, the influence of continental river discharge as well as inputs from rainfall over the island could have provided increased nutrients and resulted in higher abundances. The large filter-feeding vertebrates that feed on tunicates include green sea turtle juveniles, which use coastal waters of Gorgona Island as feeding grounds, as part of their migration route in the Eastern Tropical Pacific. These turtles could be using tunicates opportunistically, as a sporadic resource that is available at certain times of the year. Rev. Biol. Trop. 62 (Suppl. 1): 149-159. Epub 2014 February 01.

Se determinó la abundancia de salpas y doliólidos en ocho estaciones costeras alrededor de Isla Gorgona (Pacífico colombiano), entre septiembre 2005 y agosto 2006. Se hicieron arrastres oblicuos desde 50m hasta la superficie; se midió la biomasa zooplanctónica total, el número de salpas y doliólidos por arrastres, y la frecuencia de ocurrencia por estación y por mes. Se registró la temperatura superficial y de fondo, la salinidad superficial y de fondo, así como la concentración de clorofila a en cada estación. Se observaron picos de abundancia de tunicados en septiembre 2005 y marzo 2006. Las altas abundancias en marzo fueron probablemente debidas a una intrusión de agua fría a la zona de estudio, la cual resultó en aguas más frías y saladas, y en una termoclina más somera. Los tunicados fueron probablemente advectados hacia el área por corrientes provenientes del suroeste, y la topografía subacuática causó una agregación de estos organismos. En septiembre, la influencia de las descargas de los ríos continentales, así como aportes por la precipitación sobre la isla pudieron haber provisto mayor cantidad de nutrientes y resultado en mayores abundancias. Los grandes vertebrados marinos filtradores que se alimentan de tunicados incluyen tortugas verdes juveniles, las cuales usan las aguas de Isla Gorgona como zona de forrajeo, como parte de su ruta de migración en el Pacífico Oriental Tropical. Estas tortugas podrían estar utilizando los tunicados oportunistamente, como un recurso esporádico que está disponible en ciertas épocas del año.

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Sexual and asexual reproduction and associated population dynamics were investigated in the colonial ascidian Didemnum rodriguesi Rocha & Monniot, 1993 (Didemnidae) in southern Brazil. Investment in sexual (production of new individuals) and asexual (colony growth) reproduction was compared between seasons. Permanently marked quadrats were repeatedly photographed to measure changes in colonies. Eggs and larvae were counted monthly in collected colonies. This species alternates seasonally between sexual (summer) and asexual (winter) reproduction. In summer, colonies were smaller, brooded eggs and larvae and recruitment rates were greater, while in winter, colony size was larger and eggs and larvae were absent. There is a relationship between fecundity and colony area. Fragmentation and fusion of colonies were similar in summer and winter, as well as mortality. In conclusion, D. rodriguesi has a lifecycle usual for high latitude ascidians with a limited time length for sexual reproduction and alternate investment in sexual and asexual reproduction along the year.

Reprodução sexuada e assexuada, mortalidade e a dinâmica de fusões e fissões de colônias de Didemnum rodriguesi Rocha & Monniot, 1993 foram investigados e comparados no sul do Brasil, no inverno e verão. Tais eventos foram analisados por fotografias de áreas permanentemente demarcadas e coletas mensais de colônias. Os resultados indicam que esta espécie alterna sazonalmente a reprodução sexuada (verão) e assexuada (inverno). Durante o verão as colônias são mais abundantes e menores, com ovos e larvas incubados e taxas de recrutamento maiores. No inverno há um menor número de colônias, porém de maior tamanho e inférteis. Existe uma relação entre fecundidade e tamanho da colônia. Não foram encontradas diferenças estatísticas no número de eventos de fragmentação e fusão entre o verão e inverno, bem como para mortalidade. Conclui-se que esta espécie tem um ciclo de vida típico de espécies de maiores latitudes, com tempo limitado para a reprodução sexuada e alternância no investimento entre reprodução sexuada e assexuada.

RESUMO

Sexual and asexual reproduction and associated population dynamics were investigated in the colonial ascidian Didemnum rodriguesi Rocha & Monniot, 1993 (Didemnidae) in southern Brazil. Investment in sexual (production of new individuals) and asexual (colony growth) reproduction was compared between seasons. Permanently marked quadrats were repeatedly photographed to measure changes in colonies. Eggs and larvae were counted monthly in collected colonies. This species alternates seasonally between sexual (summer) and asexual (winter) reproduction. In summer, colonies were smaller, brooded eggs and larvae and recruitment rates were greater, while in winter, colony size was larger and eggs and larvae were absent. There is a relationship between fecundity and colony area. Fragmentation and fusion of colonies were similar in summer and winter, as well as mortality. In conclusion, D. rodriguesi has a lifecycle usual for high latitude ascidians with a limited time length for sexual reproduction and alternate investment in sexual and asexual reproduction along the year.

Reprodução sexuada e assexuada, mortalidade e a dinâmica de fusões e fissões de colônias de Didemnum rodriguesi Rocha & Monniot, 1993 foram investigados e comparados no sul do Brasil, no inverno e verão. Tais eventos foram analisados por fotografias de áreas permanentemente demarcadas e coletas mensais de colônias. Os resultados indicam que esta espécie alterna sazonalmente a reprodução sexuada (verão) e assexuada (inverno). Durante o verão as colônias são mais abundantes e menores, com ovos e larvas incubados e taxas de recrutamento maiores. No inverno há um menor número de colônias, porém de maior tamanho e inférteis. Existe uma relação entre fecundidade e tamanho da colônia. Não foram encontradas diferenças estatísticas no número de eventos de fragmentação e fusão entre o verão e inverno, bem como para mortalidade. Conclui-se que esta espécie tem um ciclo de vida típico de espécies de maiores latitudes, com tempo limitado para a reprodução sexuada e alternância no investimento entre reprodução sexuada e assexuada.

RESUMO

Simple and colonial ascidians were collected at different depths at Arraial do Cabo, Rio de Janeiro, between 2000 and 2003. The collection here presented includes representatives of the families Clavelinidae (Clavelina oblonga), Polycitoridae (Cystodytes dellechiajei), Polyclinidae (Polyclinum constellatum and Polyclinum molle sp. nov.), Holozoidae (Distaplia bermudensis), Ascidiidae (Ascidia sydneiensis and Phallusia nigra), Styelidae (Botrylloides giganteum, Botrylloides nigrum, Symplegma brakenhielmi, Symplegma rubra, Polyandrocarpa anguinea, Eusynstyela floridana, Eusynstyela tincta and Styela plicata), Pyuridae (Herdmania pallida and Microcosmus exasperatus). Didemnids were also collected in the area but were not considered here. Of the 17 species found, one (Polyclinum molle sp. nov.) is a new species in the family Polyclinidae and the others are all species with tropical distribution.

Ascídias simples e coloniais foram coletadas em diferentes profundidades em Arraial do Cabo, Rio de Janeiro, entre 2000 e 2003. A coleção aqui apresentada inclui representantes das famílias Clavelinidae (Clavelina oblonga), Polycitoridae (Cystodytes dellechiajei), Polyclinidae (Polyclinum constellatum e Polyclinum molle sp. nov.), Holozoidae (Distaplia bermudensis), Ascidiidae (Ascidia sydneiensis e Phallusia nigra), Styelidae (Botrylloides giganteum, Botrylloides nigrum, Symplegma brakenhielmi, Symplegma rubra, Polyandrocarpa anguinea, Eusynstyela floridana, Eusynstyela tincta e Styela plicata), Pyuridae (Herdmania pallida e Microcosmus exasperatus). Espécimes de Didemnidae também foram coletados na região, mas não serão reportados neste trabalho. Entre as 17 espécies encontradas, uma (Polyclinum molle sp. nov.) é uma nova espécie da família Polyclinidae e todas as outras apresentam distribuição tropical.

RESUMO

Simple and colonial ascidians were collected at different depths at Arraial do Cabo, Rio de Janeiro, between 2000 and 2003. The collection here presented includes representatives of the families Clavelinidae (Clavelina oblonga), Polycitoridae (Cystodytes dellechiajei), Polyclinidae (Polyclinum constellatum and Polyclinum molle sp. nov.), Holozoidae (Distaplia bermudensis), Ascidiidae (Ascidia sydneiensis and Phallusia nigra), Styelidae (Botrylloides giganteum, Botrylloides nigrum, Symplegma brakenhielmi, Symplegma rubra, Polyandrocarpa anguinea, Eusynstyela floridana, Eusynstyela tincta and Styela plicata), Pyuridae (Herdmania pallida and Microcosmus exasperatus). Didemnids were also collected in the area but were not considered here. Of the 17 species found, one (Polyclinum molle sp. nov.) is a new species in the family Polyclinidae and the others are all species with tropical distribution.

Ascídias simples e coloniais foram coletadas em diferentes profundidades em Arraial do Cabo, Rio de Janeiro, entre 2000 e 2003. A coleção aqui apresentada inclui representantes das famílias Clavelinidae (Clavelina oblonga), Polycitoridae (Cystodytes dellechiajei), Polyclinidae (Polyclinum constellatum e Polyclinum molle sp. nov.), Holozoidae (Distaplia bermudensis), Ascidiidae (Ascidia sydneiensis e Phallusia nigra), Styelidae (Botrylloides giganteum, Botrylloides nigrum, Symplegma brakenhielmi, Symplegma rubra, Polyandrocarpa anguinea, Eusynstyela floridana, Eusynstyela tincta e Styela plicata), Pyuridae (Herdmania pallida e Microcosmus exasperatus). Espécimes de Didemnidae também foram coletados na região, mas não serão reportados neste trabalho. Entre as 17 espécies encontradas, uma (Polyclinum molle sp. nov.) é uma nova espécie da família Polyclinidae e todas as outras apresentam distribuição tropical.