Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus
Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (Gasterosteus aculeatus) is...
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| Published in: | PLoS genetics Vol. 10; no. 10; p. e1004696 |
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| Main Authors: | , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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01-10-2014
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| Abstract | Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (Gasterosteus aculeatus) is a well-studied model organism with a short generation time, small genome size, and many genetic and genomic tools available. Within this originally marine species, populations have recurrently adapted to freshwater all over its range. This evolution involved extensive parallelism: pre-existing alleles that adapt sticklebacks to freshwater habitats, but are also present at low frequencies in marine populations, have been recruited repeatedly. While a number of genomic regions responsible for this adaptation have been identified, the details of selection remain poorly understood. Using whole-genome resequencing, we compare pooled genomic samples from marine and freshwater populations of the White Sea basin, and identify 19 short genomic regions that are highly divergent between them, including three known inversions. 17 of these regions overlap protein-coding genes, including a number of genes with predicted functions that are relevant for adaptation to the freshwater environment. We then analyze four additional independently derived young freshwater populations of known ages, two natural and two artificially established, and use the observed shifts of allelic frequencies to estimate the strength of positive selection. Adaptation turns out to be quite rapid, indicating strong selection acting simultaneously at multiple regions of the genome, with selection coefficients of up to 0.27. High divergence between marine and freshwater genotypes, lack of reduction in polymorphism in regions responsible for adaptation, and high frequencies of freshwater alleles observed even in young freshwater populations are all consistent with rapid assembly of G. aculeatus freshwater genotypes from pre-existing genomic regions of adaptive variation, with strong selection that favors this assembly acting simultaneously at multiple loci. |
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| AbstractList | Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (
Gasterosteus aculeatus
) is a well-studied model organism with a short generation time, small genome size, and many genetic and genomic tools available. Within this originally marine species, populations have recurrently adapted to freshwater all over its range. This evolution involved extensive parallelism: pre-existing alleles that adapt sticklebacks to freshwater habitats, but are also present at low frequencies in marine populations, have been recruited repeatedly. While a number of genomic regions responsible for this adaptation have been identified, the details of selection remain poorly understood. Using whole-genome resequencing, we compare pooled genomic samples from marine and freshwater populations of the White Sea basin, and identify 19 short genomic regions that are highly divergent between them, including three known inversions. 17 of these regions overlap protein-coding genes, including a number of genes with predicted functions that are relevant for adaptation to the freshwater environment. We then analyze four additional independently derived young freshwater populations of known ages, two natural and two artificially established, and use the observed shifts of allelic frequencies to estimate the strength of positive selection. Adaptation turns out to be quite rapid, indicating strong selection acting simultaneously at multiple regions of the genome, with selection coefficients of up to 0.27. High divergence between marine and freshwater genotypes, lack of reduction in polymorphism in regions responsible for adaptation, and high frequencies of freshwater alleles observed even in young freshwater populations are all consistent with rapid assembly of
G. aculeatus
freshwater genotypes from pre-existing genomic regions of adaptive variation, with strong selection that favors this assembly acting simultaneously at multiple loci.
Adaptation to novel environments is a keystone of evolution. There is only a handful of natural and experimental systems in which the process of adaptation has been studied in detail, and each studied system brings its own surprises with regard to the number of loci involved, dynamics of adaptation, extent of interactions between loci and of parallelism between different adapting populations. The threespine stickleback is an excellent model organism for evolutionary studies. Marine-derived freshwater populations of this species have consistently acquired a specific set of morphological, physiological and behavioral traits allowing them to reside in freshwater for their whole lifespan. Previous studies identified several genomic regions responsible for this adaptation. Here, using whole-genome sequencing, we compare the allele frequencies at such regions in four derived freshwater populations of known ages: two natural, and two artificially established in 1978. Knowledge of population ages allows us to infer the strength of selection that acted at these loci. Adaptation of threespine stickleback to freshwater is typically fast, and is driven by strong selection favoring pre-existing alleles that are likely present in the ancestral marine population at low frequencies; however, some of the adaptation may also be due to young population-specific alleles. Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (Gasterosteus aculeatus) is a well-studied model organism with a short generation time, small genome size, and many genetic and genomic tools available. Within this originally marine species, populations have recurrently adapted to freshwater all over its range. This evolution involved extensive parallelism: pre-existing alleles that adapt sticklebacks to freshwater habitats, but are also present at low frequencies in marine populations, have been recruited repeatedly. While a number of genomic regions responsible for this adaptation have been identified, the details of selection remain poorly understood. Using whole-genome resequencing, we compare pooled genomic samples from marine and freshwater populations of the White Sea basin, and identify 19 short genomic regions that are highly divergent between them, including three known inversions. 17 of these regions overlap protein-coding genes, including a number of genes with predicted functions that are relevant for adaptation to the freshwater environment. We then analyze four additional independently derived young freshwater populations of known ages, two natural and two artificially established, and use the observed shifts of allelic frequencies to estimate the strength of positive selection. Adaptation turns out to be quite rapid, indicating strong selection acting simultaneously at multiple regions of the genome, with selection coefficients of up to 0.27. High divergence between marine and freshwater genotypes, lack of reduction in polymorphism in regions responsible for adaptation, and high frequencies of freshwater alleles observed even in young freshwater populations are all consistent with rapid assembly of G. aculeatus freshwater genotypes from pre-existing genomic regions of adaptive variation, with strong selection that favors this assembly acting simultaneously at multiple loci. Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (Gasterosteus aculeatus) is a well-studied model organism with a short generation time, small genome size, and many genetic and genomic tools available. Within this originally marine species, populations have recurrently adapted to freshwater all over its range. This evolution involved extensive parallelism: pre-existing alleles that adapt sticklebacks to freshwater habitats, but are also present at low frequencies in marine populations, have been recruited repeatedly. While a number of genomic regions responsible for this adaptation have been identified, the details of selection remain poorly understood. Using whole-genome resequencing, we compare pooled genomic samples from marine and freshwater populations of the White Sea basin, and identify 19 short genomic regions that are highly divergent between them, including three known inversions. 17 of these regions overlap protein-coding genes, including a number of genes with predicted functions that are relevant for adaptation to the freshwater environment. We then analyze four additional independently derived young freshwater populations of known ages, two natural and two artificially established, and use the observed shifts of allelic frequencies to estimate the strength of positive selection. Adaptation turns out to be quite rapid, indicating strong selection acting simultaneously at multiple regions of the genome, with selection coefficients of up to 0.27. High divergence between marine and freshwater genotypes, lack of reduction in polymorphism in regions responsible for adaptation, and high frequencies of freshwater alleles observed even in young freshwater populations are all consistent with rapid assembly of G. aculeatus freshwater genotypes from pre-existing genomic regions of adaptive variation, with strong selection that favors this assembly acting simultaneously at multiple loci. |
| Audience | Academic |
| Author | Penin, Aleksey A Mugue, Nikolai S Neretina, Tatiana V Kondrashov, Alexey S Logacheva, Maria D Terekhanova, Nadezhda V Barmintseva, Anna E Bazykin, Georgii A |
| AuthorAffiliation | 7 Department of Ecology and Evolutionary Biology and Life Sciences Institute, University of Michigan, Ann Arbor, Michigan, United States of America Fred Hutchinson Cancer Research Center, United States of America 4 White Sea Biological Station, Biological faculty, M. V. Lomonosov Moscow State University, Moscow, Russia 2 A. N. Belozersky Institute of Physico-Chemical Biology, M. V. Lomonosov Moscow State University, Moscow, Russia 8 N. K. Koltsov Institute of Developmental Biology RAS, Moscow, Russia 3 Department of Genetics, Biological faculty, M. V. Lomonosov Moscow State University, Moscow, Russia 5 Laboratory of Molecular genetics, Russian Institute of Fisheries and Oceanology, Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia 1 Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia 6 Sector for Molecular Evolution, Institute for Information Transmission Problems of the RAS (Kharkevich Institute), Moscow, Russ |
| AuthorAffiliation_xml | – name: 1 Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia – name: 2 A. N. Belozersky Institute of Physico-Chemical Biology, M. V. Lomonosov Moscow State University, Moscow, Russia – name: 3 Department of Genetics, Biological faculty, M. V. Lomonosov Moscow State University, Moscow, Russia – name: 7 Department of Ecology and Evolutionary Biology and Life Sciences Institute, University of Michigan, Ann Arbor, Michigan, United States of America – name: 6 Sector for Molecular Evolution, Institute for Information Transmission Problems of the RAS (Kharkevich Institute), Moscow, Russia – name: 4 White Sea Biological Station, Biological faculty, M. V. Lomonosov Moscow State University, Moscow, Russia – name: 8 N. K. Koltsov Institute of Developmental Biology RAS, Moscow, Russia – name: Fred Hutchinson Cancer Research Center, United States of America – name: 5 Laboratory of Molecular genetics, Russian Institute of Fisheries and Oceanology, Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia |
| Author_xml | – sequence: 1 givenname: Nadezhda V surname: Terekhanova fullname: Terekhanova, Nadezhda V organization: Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia – sequence: 2 givenname: Maria D surname: Logacheva fullname: Logacheva, Maria D organization: Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia; A. N. Belozersky Institute of Physico-Chemical Biology, M. V. Lomonosov Moscow State University, Moscow, Russia – sequence: 3 givenname: Aleksey A surname: Penin fullname: Penin, Aleksey A organization: Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia; Department of Genetics, Biological faculty, M. V. Lomonosov Moscow State University, Moscow, Russia – sequence: 4 givenname: Tatiana V surname: Neretina fullname: Neretina, Tatiana V organization: Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia; White Sea Biological Station, Biological faculty, M. V. Lomonosov Moscow State University, Moscow, Russia – sequence: 5 givenname: Anna E surname: Barmintseva fullname: Barmintseva, Anna E organization: Laboratory of Molecular genetics, Russian Institute of Fisheries and Oceanology, Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia – sequence: 6 givenname: Georgii A surname: Bazykin fullname: Bazykin, Georgii A organization: Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia; Sector for Molecular Evolution, Institute for Information Transmission Problems of the RAS (Kharkevich Institute), Moscow, Russia – sequence: 7 givenname: Alexey S surname: Kondrashov fullname: Kondrashov, Alexey S organization: Department of Bioinformatics and Bioengineering, M. V. Lomonosov Moscow State University, Moscow, Russia; Department of Ecology and Evolutionary Biology and Life Sciences Institute, University of Michigan, Ann Arbor, Michigan, United States of America – sequence: 8 givenname: Nikolai S surname: Mugue fullname: Mugue, Nikolai S organization: Laboratory of Molecular genetics, Russian Institute of Fisheries and Oceanology, Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia; N. K. Koltsov Institute of Developmental Biology RAS, Moscow, Russia |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25299485$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2014 Public Library of Science 2014 Terekhanova et al 2014 Terekhanova et al 2014 Public Library of Science. 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: . PLoS Genet 10(10): e1004696. doi:10.1371/journal.pgen.1004696 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: NVT GAB ASK NSM. Performed the experiments: MDL AAP TVN AEB. Analyzed the data: NVT NSM. Contributed reagents/materials/analysis tools: MDL NSM. Wrote the paper: NVT MDL AAP TVN AEB GAB ASK NSM. The authors have declared that no competing interests exist. |
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| Snippet | Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study.... Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study.... |
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| SubjectTerms | Adaptation Adaptation, Physiological - genetics Animals Aquatic Organisms Biological Evolution Biology and Life Sciences Evolution Evolutionary genetics Female Fresh Water Gene Frequency Genetic aspects Genetic research Genetics, Population Genome Genomes Genomics Male Medical research Morphology Natural history Physiology Polymorphism, Single Nucleotide Population Russia Selection, Genetic Smegmamorpha - genetics Standard deviation Sticklebacks Studies |
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| Title | Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus |
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