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      Genomics of Rapid Incipient Speciation in Sympatric Threespine Stickleback

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Ecological speciation is the process by which reproductively isolated populations emerge as a consequence of divergent natural or ecologically-mediated sexual selection. Most genomic studies of ecological speciation have investigated allopatric populations, making it difficult to infer reproductive isolation. The few studies on sympatric ecotypes have focused on advanced stages of the speciation process after thousands of generations of divergence. As a consequence, we still do not know what genomic signatures of the early onset of ecological speciation look like. Here, we examined genomic differentiation among migratory lake and resident stream ecotypes of threespine stickleback reproducing in sympatry in one stream, and in parapatry in another stream. Importantly, these ecotypes started diverging less than 150 years ago. We obtained 34,756 SNPs with restriction-site associated DNA sequencing and identified genomic islands of differentiation using a Hidden Markov Model approach. Consistent with incipient ecological speciation, we found significant genomic differentiation between ecotypes both in sympatry and parapatry. Of 19 islands of differentiation resisting gene flow in sympatry, all were also differentiated in parapatry and were thus likely driven by divergent selection among habitats. These islands clustered in quantitative trait loci controlling divergent traits among the ecotypes, many of them concentrated in one region with low to intermediate recombination. Our findings suggest that adaptive genomic differentiation at many genetic loci can arise and persist in sympatry at the very early stage of ecotype divergence, and that the genomic architecture of adaptation may facilitate this.

          Author Summary

          Ecological speciation can be defined as the evolution of new, reproductively isolated, species driven by natural selection and ecologically-mediated sexual selection. Its genomic signature has mainly been studied in ecotypes and emerging species that started diverging hundreds to thousands of generations ago, while little is known about the very early stages of species divergence. To fill this knowledge gap, we studied whether and how threespine stickleback, which have adapted either to lake or to stream environments in less than 150 years, differ across their genomes. We found several segments of the genome to be clearly divergent between lake and stream ecotypes, even when both forms breed side by side in the same area. Strikingly, this genomic differentiation was mainly concentrated in one region with low to intermediate recombination rates and clustered around genes controlling ecotype-specific phenotypic traits. Our findings suggest that genomic differentiation can arise despite gene flow already very early at the onset of speciation, and that its occurrence may be facilitated by the genomic organization of genes that control traits involved in adaptation and reproductive isolation.

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          Most cited references 143

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          The Sequence Alignment/Map format and SAMtools

          Summary: The Sequence Alignment/Map (SAM) format is a generic alignment format for storing read alignments against reference sequences, supporting short and long reads (up to 128 Mbp) produced by different sequencing platforms. It is flexible in style, compact in size, efficient in random access and is the format in which alignments from the 1000 Genomes Project are released. SAMtools implements various utilities for post-processing alignments in the SAM format, such as indexing, variant caller and alignment viewer, and thus provides universal tools for processing read alignments. Availability: http://samtools.sourceforge.net Contact: rd@sanger.ac.uk
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            Fast gapped-read alignment with Bowtie 2.

            As the rate of sequencing increases, greater throughput is demanded from read aligners. The full-text minute index is often used to make alignment very fast and memory-efficient, but the approach is ill-suited to finding longer, gapped alignments. Bowtie 2 combines the strengths of the full-text minute index with the flexibility and speed of hardware-accelerated dynamic programming algorithms to achieve a combination of high speed, sensitivity and accuracy.
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              PLINK: a tool set for whole-genome association and population-based linkage analyses.

              Whole-genome association studies (WGAS) bring new computational, as well as analytic, challenges to researchers. Many existing genetic-analysis tools are not designed to handle such large data sets in a convenient manner and do not necessarily exploit the new opportunities that whole-genome data bring. To address these issues, we developed PLINK, an open-source C/C++ WGAS tool set. With PLINK, large data sets comprising hundreds of thousands of markers genotyped for thousands of individuals can be rapidly manipulated and analyzed in their entirety. As well as providing tools to make the basic analytic steps computationally efficient, PLINK also supports some novel approaches to whole-genome data that take advantage of whole-genome coverage. We introduce PLINK and describe the five main domains of function: data management, summary statistics, population stratification, association analysis, and identity-by-descent estimation. In particular, we focus on the estimation and use of identity-by-state and identity-by-descent information in the context of population-based whole-genome studies. This information can be used to detect and correct for population stratification and to identify extended chromosomal segments that are shared identical by descent between very distantly related individuals. Analysis of the patterns of segmental sharing has the potential to map disease loci that contain multiple rare variants in a population-based linkage analysis.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                29 February 2016
                February 2016
                : 12
                : 2
                Affiliations
                [1 ]Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
                [2 ]Department of Fish Ecology and Evolution, Centre of Ecology, Evolution & Biogeochemistry, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland
                [3 ]Computational and Molecular Population Genetics Lab, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
                [4 ]Swiss Institute of Bioinformatics, Lausanne, Switzerland
                [5 ]Biodiversity Institute, University of Wyoming, Wyoming, United States of America
                [6 ]Department of Animal and Plant Science, University of Sheffield, Sheffield, United Kingdom
                University of California Davis, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: OS DAM KL LE. Performed the experiments: DAM KL SM JIM OS. Analyzed the data: DAM. Contributed reagents/materials/analysis tools: OS LE KL JIM. Wrote the paper: DAM OS LE CEW KL JIM.

                ‡ These authors are joint senior authors on this work.

                Article
                PGENETICS-D-15-01459
                10.1371/journal.pgen.1005887
                4771382
                26925837
                © 2016 Marques et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 7, Tables: 1, Pages: 34
                Product
                Funding
                This research was supported by the Swiss National Science Foundation ( www.snf.ch) grant PDFMP3_134657 to OS and LE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Earth Sciences
                Marine and Aquatic Sciences
                Bodies of Water
                Lakes
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Fishes
                Osteichthyes
                Sticklebacks
                Biology and Life Sciences
                Genetics
                Heredity
                Gene Flow
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Gene Flow
                Biology and Life Sciences
                Genetics
                Population Genetics
                Gene Flow
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Gene Flow
                Biology and Life Sciences
                Cell Biology
                Chromosome Biology
                Chromosomes
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Ecology and Environmental Sciences
                Habitats
                Biology and Life Sciences
                Genetics
                Genomics
                Biology and life sciences
                Genetics
                DNA
                DNA recombination
                Biology and life sciences
                Biochemistry
                Nucleic acids
                DNA
                DNA recombination
                Custom metadata
                Raw data is accessible via the Sequence Read Archive ( www.ncbi.nlm.nih.gov/sra) under the study accession SRP069137.

                Genetics

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