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The population genomics of a fast evolver: high levels of diversity, functional constraint, and molecular adaptation in the tunicate Ciona intestinalis.

ABSTRACT: Phylogenomics has revealed the existence of fast-evolving animal phyla in which the amino acid substitution rate, averaged across many proteins, is consistently higher than in other lineages. The reasons for such differences in proteome-wide evolutionary rates are still unknown, largely because only a handful of species offer within-species genomic data from which molecular evolutionary processes can be deduced. In this study, we use next-generation sequencing technologies and individual whole-transcriptome sequencing to gather extensive polymorphism sequence data sets from Ciona intestinalis. Ciona is probably the best-characterized member of the fast-evolving Urochordata group (tunicates), which was recently identified as the sister group of the slow-evolving vertebrates. We introduce and validate a maximum-likelihood framework for single-nucleotide polymorphism and genotype calling, based on high-throughput short-read typing. We report that the C. intestinalis proteome is characterized by a high level of within-species diversity, efficient purifying selection, and a substantial percentage of adaptive amino acid substitutions. We conclude that the increased rate of amino acid sequence evolution in tunicates, when compared with vertebrates, is the consequence of both a 2-6 times higher per-year mutation rate and prevalent adaptive evolution.

SUBMITTER: Tsagkogeorga G

PROVIDER: S-EPMC3509891 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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The population genomics of a fast evolver: high levels of diversity, functional constraint, and molecular adaptation in the tunicate Ciona intestinalis.

Tsagkogeorga Georgia G Cahais Vincent V Galtier Nicolas N

Genome biology and evolution 20120628 8

Phylogenomics has revealed the existence of fast-evolving animal phyla in which the amino acid substitution rate, averaged across many proteins, is consistently higher than in other lineages. The reasons for such differences in proteome-wide evolutionary rates are still unknown, largely because only a handful of species offer within-species genomic data from which molecular evolutionary processes can be deduced. In this study, we use next-generation sequencing technologies and individual whole-t ...[more]

PMID: 22745226

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Project description:The tunicate Ciona intestinalis is an opportunistic invader with high potential for causing economic losses in aquaculture centers. Recent phylogenetic and population genetic analysis support the existence of a genetic complex described as C. intestinalis with two main dominant species (sp A and B) occurring worldwide. In Chile, the species has been observed around 30°S of latitude, but no official reports exist for the presence of C. intestinalis in southern regions (above 40°S), where most of the mollusk aquaculture centers are located. Here, we used occurrences from multiple invaded regions and extensive field sampling to model and validate the environmental conditions that allow the species to persist and to find the geographic areas with the most suitable environmental conditions for the spread of C. intestinalis in the Chilean coast. By studying the potential expansion of C. intestinalis southward in the Chilean Coast, we aimed to provide valuable information that might help the development of control plans before the species becomes a significant problem, especially above 40°S. Our results highlight that, by using portions of the habitat that are apparently distinguishable, the species seem to be not only genetically distinct, but ecologically distinct as well. The two regional models fitted for sp A and for sp B showed disagreement on which sections of Chilean coastline are considered more suitable for these species. While the model for sp A identifies moderately to highly suitable areas between 30° and 40°S, the model for sp B classifies the areas around 45°S as the most appropriate. Data from field sampling show a positive linear relationship between density of C. intestinalis and the index of suitability for sp A in aquaculture centers. Understanding the relation of the distinct species with the surrounding environment provided valuable insights about probable routes of dispersion in Chile, especially into those areas considered suitable for aquaculture activities but where the species has not yet been recorded. We discuss the implications of our findings as a useful tool to anticipate the invasion of such harmful invasive species with regard to the most relevant environmental variables.

Project description:Eight different types of sample (three samples each) were used in this study of cardiac cell migration in the tunicate Ciona intestinalis. The B7.5 lineage cells were isolated by Fluorescent Activated Cell Sorting (FACS) at the tailbud stage, when the cardiac precursors (anterior B7.5 lineage cells) are migrating into the trunk, while their sister cells (posterior 7.5 lineage cells) remain in the tail, where they form muscle cells. Cells were sorted at the late gastrula stage, prior to migration induction and after manipulation of the FGF-MAPK-Ets signaling pathway (targeted expression of dominant negative FGF receptor and Ets:VP16 fusion protein, targeted expression was achieved using the Mesp cis-regulatory DNA), FoxF function (a direct target of FGF-MAPK-Ets signaling, required primarily for cell migration) by targeted expression of FoxF:VP16 (constitutive activator) or FoxF:WRPW (constitutive repressor, dominant negative), Mesp function (over-expression of Mesp:VP16 inhibits primarily cell migration). Finally, the "whole embryo" samples were collected from dissociated whole tailbud embryos, without FACS. in summary the eight conditions are: "wt (files LC-wt-1,-2,-3)": wild_type B7.5 lineage cells, expressing GFP, sorted at the tailbud stage "Ets:VP16 (files LC-EV-1,-2,-3)": B7.5 lineage cells, expressing GFP and Ets:VP16, sorted at the tailbud stage "DnFGFR (files LC-dnFGFR-1,-2,-3)": B7.5 lineage cells, expressing GFP and dominant-negative FGF receptor, sorted at the tailbud stage. "FoxF:VP16 (files LC-FV-1,-2,-3)": B7.5 lineage cells, expressing GFP and FoxF:VP16, sorted at the tailbud stage. "FoxF:WRPW (files LC-FW-1,-2,-3)": B7.5 lineage cells, expressing GFP and FoxF:WRPW, sorted at the tailbud stage". "Mesp:VP16 (files LC-MV-1,-2,-3)": B7.5 lineage cells, expressing GFP and Mesp:VP16, sorted at the tailbud stage. "Late Gastrula (files LC-LG-1,-2,-3)": wild_type B7.5 lineage cells, expressing GFP, sorted at the late gastrula stage "whole embryo (files LC-whole-1,-2,-3": whole embryos, dissociated at the tailbud stage, not sorted.

Dataset Information

The population genomics of a fast evolver: high levels of diversity, functional constraint, and molecular adaptation in the tunicate Ciona intestinalis.

Publications

The population genomics of a fast evolver: high levels of diversity, functional constraint, and molecular adaptation in the tunicate Ciona intestinalis.

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