Genes underlying repeated adaptive evolution in natural populations are still largely unknown. Stickleback fish (Gasterosteus aculeatus) have undergone a recent dramatic evolutionary radiation, ...generating numerous examples of marine-freshwater species pairs and a small number of benthic-limnetic species pairs found within single lakes 1. We have developed a new genome-wide SNP genotyping array to study patterns of genetic variation in sticklebacks over a wide geographic range, and to scan the genome for regions that contribute to repeated evolution of marine-freshwater or benthic-limnetic species pairs. Surveying 34 global populations with 1,159 informative markers revealed substantial genetic variation, with predominant patterns reflecting demographic history and geographic structure. After correcting for geographic structure and filtering for neutral markers, we detected large repeated shifts in allele frequency at some loci, identifying both known and novel loci likely contributing to marine-freshwater and benthic-limnetic divergence. Several novel loci fall close to genes implicated in epithelial barrier or immune functions, which have likely changed as sticklebacks adapt to contrasting environments. Specific alleles differentiating sympatric benthic-limnetic species pairs are shared in nearby solitary populations, suggesting an allopatric origin for adaptive variants and selection pressures unrelated to sympatry in the initial formation of these classic vertebrate species pairs.
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► A new genome-wide SNP array facilitates genetic studies of three-spine sticklebacks ► Survey of 34 populations reveals patterns of global geographic structure ► Large shifts in allele frequency underlie adaptive divergence of species pairs ► Allopatric populations share sets of benthic-limnetic species-pair adaptive alleles
Regulation of gene expression is thought to play a major role in adaptation, but the relative importance of
- and
- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using ...RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater ecotype pairs and their F1 hybrids, we show that
-acting (allele-specific) regulation consistently predominates gene expression divergence. Genes showing parallel marine-freshwater expression divergence are found near to adaptive genomic regions, show signatures of natural selection around their transcription start sites and are enriched for
regulatory control. For genes with parallel increased expression among freshwater fish, the quantitative degree of
and
regulation is also highly correlated across populations, suggesting a shared genetic basis. Compared to other forms of regulation,
regulation tends to show greater additivity and stability across different genetic and environmental contexts, making it a fertile substrate for the early stages of adaptive evolution.
Changes in bone size and shape are defining features of many vertebrates. Here we use genetic crosses and comparative genomics to identify specific regulatory DNA alterations controlling skeletal ...evolution. Armor bone-size differences in sticklebacks map to a major effect locus overlapping BMP family member GDF6. Freshwater fish express more GDF6 due in part to a transposon insertion, and transgenic overexpression of GDF6 phenocopies evolutionary changes in armor-plate size. The human GDF6 locus also has undergone distinctive regulatory evolution, including complete loss of an enhancer that is otherwise highly conserved between chimps and other mammals. Functional tests show that the ancestral enhancer drives expression in hindlimbs but not forelimbs, in locations that have been specifically modified during the human transition to bipedalism. Both gain and loss of regulatory elements can localize BMP changes to specific anatomical locations, providing a flexible regulatory basis for evolving species-specific changes in skeletal form.
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•Altered armor-plate size in sticklebacks maps to a cis-regulatory change in GDF6 gene•Increased GDF6 expression phenocopies armor evolution in transgenic fish•Humans have lost a conserved regulatory element controlling GDF6 expression•Mouse phenotypes suggest that deletion is related to digit shortening in human feet
The bone morphogenetic protein gene GDF6 has evolved species-specific regulatory changes in both sticklebacks and humans, with gain and loss of particular enhancers providing a likely regulatory mechanism for changing bony armor in fish and modifying hindlimb-specific digit morphology during the transition to bipedalism in humans.
Repeated adaptation to a new environment often leads to convergent phenotypic changes whose underlying genetic mechanisms are rarely known. Here, we study adaptation of color vision in threespine ...stickleback during the repeated postglacial colonization of clearwater and blackwater lakes in the Haida Gwaii archipelago. We use whole genomes from 16 clearwater and 12 blackwater populations, and a selection experiment, in which stickleback were transplanted from a blackwater lake into an uninhabited clearwater pond and resampled after 19 y to test for selection on cone opsin genes. Patterns of haplotype homozygosity, genetic diversity, site frequency spectra, and allele-frequency change support a selective sweep centered on the adjacent blue- and red-light sensitive opsins SWS2 and LWS. The haplotype under selection carries seven amino acid changes in SWS2, including two changes known to cause a red-shift in light absorption, and is favored in blackwater lakes but disfavored in the clearwater habitat of the transplant population. Remarkably, the same red-shifting amino acid changes occurred after the duplication of SWS2 198 million years ago, in the ancestor of most spiny-rayed fish. Two distantly related fish species, bluefin killifish and black bream, express these old paralogs divergently in black- and clearwater habitats, while sticklebacks lost one paralog. Our study thus shows that convergent adaptation to the same environment can involve the same genetic changes on very different evolutionary time scales by reevolving lost mutations and reusing them repeatedly from standing genetic variation.
Ecological differences often evolve early in speciation as divergent natural selection drives adaptation to distinct ecological niches, leading ultimately to reproductive isolation. Although this ...process is a major generator of biodiversity, its genetic basis is still poorly understood. Here we investigate the genetic architecture of niche differentiation in a sympatric species pair of threespine stickleback fish by mapping the environment-dependent effects of phenotypic traits on hybrid feeding and performance under semi-natural conditions. We show that multiple, unlinked loci act largely additively to determine position along the major niche axis separating these recently diverged species. We also find that functional mismatch between phenotypic traits reduces the growth of some stickleback hybrids beyond that expected from an intermediate phenotype, suggesting a role for epistasis between the underlying genes. This functional mismatch might lead to hybrid incompatibilities that are analogous to those underlying intrinsic reproductive isolation but depend on the ecological context.
Mutations of small effect underlie most adaptation to new environments, but beneficial variants with large fitness effects are expected to contribute under certain conditions. Genes and genomic ...regions having large effects on phenotypic differences between populations are known from numerous taxa, but fitness effect sizes have rarely been estimated. We mapped fitness over a generation in an F2 intercross between a marine and a lake stickleback population introduced to a freshwater pond. A quantitative trait locus map of the number of surviving offspring per F2 female detected a single, large-effect locus near
(
), a gene having an ancient freshwater allele causing reduced bony armor and other changes. F2 females homozygous for the freshwater allele had twice the number of surviving offspring as homozygotes for the marine allele, producing a large selection coefficient,
= 0.50 ± 0.09 SE. Correspondingly, the frequency of the freshwater allele increased from 0.50 in F2 mothers to 0.58 in surviving offspring. We compare these results to allele frequency changes at the
gene in an Alaskan lake population colonized by marine stickleback in the 1980s. The frequency of the freshwater
allele rose steadily over multiple generations and reached 95% within 20 y, yielding a similar estimate of selection,
= 0.49 ± 0.05, but a different degree of dominance. These findings are consistent with other studies suggesting strong selection on this gene (and/or linked genes) in fresh water. Selection on ancient genetic variants carried by colonizing ancestors is likely to increase the prevalence of large-effect fitness variants in adaptive evolution.
Meiotic recombination rates vary across the genome, often involving localized crossover hotspots and coldspots. Studying the molecular basis and mechanisms underlying this variation has been ...challenging due to the high cost and effort required to construct individualized genome-wide maps of recombination crossovers. Here we introduce a new method, called ReMIX, to detect crossovers from gamete DNA of a single individual using Illumina sequencing of 10X Genomics linked-read libraries. ReMIX reconstructs haplotypes and identifies the valuable rare molecules spanning crossover breakpoints, allowing quantification of the genomic location and intensity of meiotic recombination. Using a single mouse and stickleback fish, we demonstrate how ReMIX faithfully recovers recombination hotspots and landscapes that have previously been built using hundreds of offspring. ReMIX provides a high-resolution, high-throughput, and low-cost approach to quantify recombination variation across the genome, providing an exciting opportunity to study recombination among multiple individuals in diverse organisms.
Adaptation is typically studied by comparing modern populations with contrasting environments. Individuals persisting in the ancestral habitat are typically used to represent the ancestral founding ...population; however, it has been questioned whether these individuals are good proxies for the actual ancestors.1 To address this, we applied a paleogenomics approach2 to directly access the ancestral genepool: partially sequencing the genomes of two 11- to 13,000-year-old stickleback recovered from the transitionary layer between marine and freshwater sediments of two Norwegian isolation lakes3 and comparing them with 30 modern stickleback genomes from the same lakes and adjacent marine fjord, in addition to a global dataset of 20 genomes.4 The ancient stickleback shared genome-wide ancestry with the modern fjord population, whereas modern lake populations have lost substantial ancestral variation following founder effects, and subsequent drift and selection. Freshwater-adaptive alleles found in one ancient stickleback genome have not risen to high frequency in the present-day population from the same lake. Comparison to the global dataset suggested incomplete adaptation to freshwater in our modern lake populations. Our findings reveal the impact of population bottlenecks in constraining adaptation due to reduced efficacy of selection on standing variation present in founder populations.
•Sequencing of two threespine stickleback genomes dated to the Late Pleistocene•These genomes show mostly marine-adapted ancestry•Present-day lake stickleback genomes indicate ancestral founder bottleneck•This demographic history constrains natural selection
Kirch et al. sequence genomes of two Late Pleistocene stickleback collected from the sediment layer corresponding to the transition from marine to freshwater habitat. Comparison with present-day lake and fjord populations highlights that demography can constrain natural selection’s action upon standing genetic variation in the ancestral gene pool.
Sexual antagonism, or conflict between the sexes, has been proposed as a driving force in both sex-chromosome turnover and speciation. Although closely related species often have different ...sex-chromosome systems, it is unknown whether sex-chromosome turnover contributes to the evolution of reproductive isolation between species. Here we show that a newly evolved sex chromosome contains genes that contribute to speciation in threespine stickleback fish (Gasterosteus aculeatus). We first identified a neo-sex chromosome system found only in one member of a sympatric species pair in Japan. We then performed genetic linkage mapping of male-specific traits important for reproductive isolation between the Japanese species pair. The neo-X chromosome contains loci for male courtship display traits that contribute to behavioural isolation, whereas the ancestral X chromosome contains loci for both behavioural isolation and hybrid male sterility. Our work not only provides strong evidence for a large X-effect on reproductive isolation in a vertebrate system, but also provides direct evidence that a young neo-X chromosome contributes to reproductive isolation between closely related species. Our data indicate that sex-chromosome turnover might have a greater role in speciation than was previously appreciated.
Genomics and the origin of species Seehausen, Ole; Butlin, Roger K; Keller, Irene ...
Nature reviews. Genetics,
03/2014, Letnik:
15, Številka:
3
Journal Article
Recenzirano
Odprti dostop
Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this ...research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.
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