Parallel selection on gene copy number variations through evolution of three-spined stickleback genomes

Hirase, Shotaro; Ozaki, Haruka; Iwasaki, Wataru

doi:10.1186/1471-2164-15-735

Cited by 32 publications

(47 citation statements)

References 49 publications

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“…Of the 6664 regions with consistent copy number difference between stickleback ecotypes, 305 overlap protein-coding exons of 211 genes. This includes all 24 genes previously identified as having copy number variants under marine/ freshwater parallel selection in a separate study (Hirase et al 2014), as well as an additional 187 genes.…”

Section: Changes In Protein-coding Exonsmentioning

confidence: 99%

Detecting differential copy number variation between groups of samples

et al. 2017

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We present a method to detect copy number variants (CNVs) that are differentially present between two groups of sequenced samples. We use a finite-state transducer where the emitted read depth is conditioned on the mappability and GC-content of all reads that occur at a given base position. In this model, the read depth within a region is a mixture of binomials, which in simulations matches the read depth more closely than the often-used negative binomial distribution. The method analyzes all samples simultaneously, preserving uncertainty as to the breakpoints and magnitude of CNVs present in an individual when it identifies CNVs differentially present between the two groups. We apply this method to identify CNVs that are recurrently associated with postglacial adaptation of marine threespine stickleback () to freshwater. We identify 6664 regions of the stickleback genome, totaling 1.7 Mbp, which show consistent copy number differences between marine and freshwater populations. These deletions and duplications affect both protein-coding genes and -regulatory elements, including a noncoding intronic telencephalon enhancer of The functions of the genes near or included within the 6664 CNVs are enriched for immunity and muscle development, as well as head and limb morphology. Although freshwater stickleback have repeatedly evolved from marine populations, we show that freshwater stickleback also act as reservoirs for ancient ancestral sequences that are highly conserved among distantly related teleosts, but largely missing from marine stickleback due to recent selective sweeps in marine populations.

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Section: Changes In Protein-coding Exonsmentioning

confidence: 99%

Detecting differential copy number variation between groups of samples

et al. 2017

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“…Submarine terraces that encircled islands in the Gulf of Alaska and Prince William Sound were suddenly thrust above sea level in 1964 by the Great Alaska Earthquake (52)(53)(54), and the resulting changes in sediment deposition and erosion over the following years created new freshwater ponds (35). Threespine stickleback fish that now inhabit many of these ponds have become as morphologically distinct in degree and form from their immediate marine ancestors as have much older mainland Alaska freshwater stickleback populations (35,54,55), similar to phenomena documented in older freshwater populations throughout the northern hemisphere (33,36,(56)(57)(58).…”

Section: Introductionmentioning

confidence: 88%

Sweeping genomic remodeling through repeated selection of alternatively adapted haplotypes occurs in the first decades after marine stickleback colonize new freshwater ponds

Bassham

Catchen

Lescak

et al. 2017

Preprint

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Heterogeneous genetic divergence can accumulate across the genome when populations adapt to different habitats while still exchanging alleles. How long does diversification take and how much of the genome is affected? When divergence occurs in parallel from standing genetic variation, how often are the same haplotypes used? We explore these questions using RAD-seq genotyping data, and show that broadscale genomic re-patterning, fueled by standing variation, can emerge in just dozens of generations in replicate natural populations of threespine stickleback fish (Gasterosteus aculeatus). After the catastrophic 1964 Alaskan earthquake, marine stickleback colonized newly created ponds on seismically uplifted islands. We find that freshwater fish in these young ponds differ from their marine ancestors across the same genomic segments previously shown to have diverged in much older lake populations. Outside of these core divergent regions the genome shows no population structure across the ocean-freshwater divide, consistent with strong local selection acting in alternative environments on stickleback populations still connected by significant gene flow. Reinforcing this inference, a majority of divergent haplotypes that are at high frequency in ponds are shared across independent freshwater populations and are detectable, at low frequency, in the sea even across great geographic distances. Building upon previous work in this model species for population genomics, our data suggest that a long history of divergent selection and gene flow across stickleback in oceanic and freshwater habitats has created balanced polymorphism in large genomic blocks of alternatively adapted DNA sequences, ultimately stoking -and potentially channelingrapid, parallel evolution. contemporary evolution -ecological divergence -population genomics -Gasterosteus aculeatus -threespine stickleback 1

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“…Copy number changes occur at nearly the same rate as point mutations and seem much more likely than other types of mutations to have beneficial effects (Kondrashov ; Hirase et al . ; Żmieńko et al . ).…”

Section: The Devil In the Detailsmentioning

confidence: 99%

The devil is in the details: genetic variation in introduced populations and its contributions to invasion

et al. 2015

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The influence of genetic variation on invasion success has captivated researchers since the start of the field of invasion genetics 50 years ago. We review the history of work on this question and conclude that genetic variation-as surveyed with molecular markers-appears to shape invasion rarely. Instead, there is a significant disconnect between marker assays and ecologically relevant genetic variation in introductions. We argue that the potential for adaptation to facilitate invasion will be shaped by the details of genotypes affecting phenotypes, and we highlight three areas in which we see opportunities to make powerful new insights. (i) The genetic architecture of adaptive variation. Traits shaped by large-effect alleles may be strongly impacted by founder events yet more likely to respond to selection when genetic drift is strong. Large-effect loci may be especially relevant for traits involved in biotic interactions. (ii) Cryptic genetic variation exposed during invasion. Introductions have strong potential to uncover masked variation due to alterations in genetic and ecological environments. (iii) Genetic interactions during admixture of multiple source populations. As divergence among sources increases, positive followed by increasingly negative effects of admixture should be expected. Although generally hypothesized to be beneficial during invasion, admixture is most often reported among sources of intermediate divergence, supporting the possibility that incompatibilities among divergent source populations might be limiting their introgression. Finally, we note that these details of invasion genetics can be coupled with comparative demographic analyses to link genetic changes to the evolution of invasiveness itself.

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Parallel selection on gene copy number variations through evolution of three-spined stickleback genomes

Cited by 32 publications

References 49 publications

Detecting differential copy number variation between groups of samples

Detecting differential copy number variation between groups of samples

Sweeping genomic remodeling through repeated selection of alternatively adapted haplotypes occurs in the first decades after marine stickleback colonize new freshwater ponds

The devil is in the details: genetic variation in introduced populations and its contributions to invasion

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