Selective Sweeps and Polygenic Adaptation Drive Local Adaptation along Moisture and Temperature Gradients in Natural Populations of Coast Redwood and Giant Sequoia

Dissecting the genomic basis of local adaptation is a major goal in evolutionary biology and conservation science. Rapid changes in the climate pose significant challenges to the survival of natural populations, and the genomic basis of long-generation plant species is still poorly understood. Here, we investigated genome-wide climate adaptation in giant sequoia and coast redwood, two iconic and ecologically important tree species. We used a combination of univariate and multivariate genotype–environment association methods and a selective sweep analysis using non-overlapping sliding windows. We identified genomic regions of potential adaptive importance, showing strong associations to moisture variables and mean annual temperature. Our results found a complex architecture of climate adaptation in the species, with genomic regions showing signatures of selective sweeps, polygenic adaptation, or a combination of both, suggesting recent or ongoing climate adaptation along moisture and temperature gradients in giant sequoia and coast redwood. The results of this study provide a first step toward identifying genomic regions of adaptive significance in the species and will provide information to guide management and conservation strategies that seek to maximize adaptive potential in the face of climate change.

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Climate adaptation shaped by subtle to moderate allele frequency shifts in loblolly pine

10.1101/635862 ◽

2019 ◽

Cited By ~ 1

Author(s):

Amanda R. De La Torre ◽

David B Neale

Keyword(s):

Allele Frequency ◽

Local Adaptation ◽

Loblolly Pine ◽

Climate Adaptation ◽

Geographic Location ◽

Woody Species ◽

Climatic Variables ◽

Whole Genome ◽

Temperature And Precipitation ◽

Genomic Regions

ABSTRACTUnderstanding the genomic basis of local adaptation is crucial to determine the potential of long-lived woody species to withstand changes in their natural environment. In the past, efforts to dissect the genomic architecture in gymnosperms species have been limited due to the absence of reference genomes. Recently, the genomes of some commercially important conifers, such as loblolly pine, have become available, allowing whole-genome studies of these species. In this study, we test for associations between 87k SNPs, obtained from whole-genome re-sequencing of loblolly pine individuals, and 270 environmental variables and combinations of them. We determine the geographic location of significant alleles and identify their genomic location using our newly constructed ultra-dense 26k SNP linkage map. We found that water availability is the main climatic variable shaping local adaptation of the species, and found 492 SNPs showing significant associations with climatic variables or combinations of them. Our results suggest that adaptation to climate in the species might have occurred by many changes in the allele frequency of alleles with moderate to small effect sizes, and by the smaller contribution of large effect alleles in genes related to moisture deficit, temperature and precipitation. Genomic regions of low recombination and high population differentiation harbored SNPs associated with principal components but not with individual climatic variables, suggesting climate adaptation might have evolved as a result of different selection pressures acting on groups of genes associated with an aspect of climate rather than on individual climatic variables.

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Genomics of clinal local adaptation in Pinus sylvestris under continuous environmental and spatial genetic setting

10.1101/647412 ◽

2019 ◽

Cited By ~ 1

Author(s):

Jaakko S. Tyrmi ◽

Jaana Vuosku ◽

Juan J. Acosta ◽

Zhen Li ◽

Lieven Sterck ◽

...

Keyword(s):

Pinus Sylvestris ◽

Local Adaptation ◽

Large Scale ◽

Molecular Genetic ◽

Natural Populations ◽

Keystone Species ◽

Evolutionary Genetics ◽

Genomic Diversity ◽

Landscape Genomics ◽

Polygenic Adaptation

AbstractUnderstanding the consequences of local adaptation at the genomic diversity is a central goal in evolutionary genetics of natural populations. In species with large continuous geographical distributions the phenotypic signal of local adaptation is frequently clear, but the genetic background often remains elusive. We examined the patterns of genetic diversity in Pinus sylvestris, a keystone species in many Eurasian ecosystems with a huge distribution range and decades of forestry research showing that it is locally adapted to the vast range of environmental conditions. Making P. sylvestris an even more attractive subject of local adaptation study, population structure has been shown to be weak previously and in this study. However, little is known about the molecular genetic basis of adaptation, as the massive size of gymnosperm genomes has prevented large scale genomic surveys. We generated a both geographically and genomically extensive dataset using a targeted sequencing approach. By applying divergence-based and landscape genomics methods we found that several coding loci contribute to local adaptation. We also discovered a very large (ca. 300 Mbp) putative inversion with a signal of local adaptation, which to our knowledge is the first such discovery in conifers. Our results call for more detailed analysis of structural variation in relation to genomic basis of local adaptation, emphasize the lack of large effect loci contributing to local adaptation in the coding regions and thus point out to the need for more attention towards multi-locus analysis of polygenic adaptation.

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From landrace to modern hybrid broccoli: the genomic and morphological domestication syndrome within a diverse B. oleracea collection

Horticulture Research ◽

10.1038/s41438-020-00375-0 ◽

2020 ◽

Vol 7 (1) ◽

Author(s):

Zachary Stansell ◽

Thomas Björkman

Keyword(s):

Southern Italy ◽

Allelic Diversity ◽

Vegetable Crops ◽

Selective Sweeps ◽

Horticultural Traits ◽

Genotype By Sequencing ◽

Genomic Regions ◽

Landrace Accessions ◽

Genomic Basis ◽

Subsequent Improvement

Abstract Worldwide, broccoli (Brassica oleracea var. italica) is among the most economically important, nutritionally rich, and widely-grown vegetable crops. To explore the genomic basis of the dramatic changes in broccoli morphology in the last century, we evaluated 109 broccoli or broccoli/cauliflower intermediates for 24 horticultural traits. Genotype-by-sequencing markers were used to determine four subpopulations within italica: Calabrese broccoli landraces and hybrids, sprouting broccoli, and violet cauliflower, and to evaluate between and within group relatedness and diversity. While overall horticultural quality and harvest index of improved hybrid broccoli germplasm has increased by year of cultivar release, this improvement has been accompanied by a considerable reduction in allelic diversity when compared to the larger pool of germplasm. Two landraces are the most likely founding source of modern broccoli hybrids, and within these modern hybrids, we identified 13 reduction-in-diversity genomic regions, 53 selective sweeps, and 30 (>1 Mbp) runs of homozygosity. Landrace accessions collected in southern Italy contained 4.8-fold greater unique alleles per accessions compared to modern hybrids and provide a valuable resource in subsequent improvement efforts. This work broadens the understanding of broccoli germplasm, informs conservation efforts, and enables breeding for complex quality traits and regionally adapted cultivars.

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Assembled and annotated 26.5 Gbp coast redwood genome: a resource for estimating evolutionary adaptive potential and investigating hexaploid origin

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab380 ◽

2021 ◽

Author(s):

David B Neale ◽

Aleksey V Zimin ◽

Sumaira Zaman ◽

Alison D Scott ◽

Bikash Shrestha ◽

...

Keyword(s):

Climate Adaptation ◽

Sequencing Data ◽

Long Terminal Repeats ◽

Structural Annotation ◽

Coast Redwood ◽

Gene Expression Control ◽

Giant Sequoia ◽

Control Comparison ◽

Long Read ◽

Species Specific

Abstract Sequencing, assembly, and annotation of the 26.5 Gbp hexaploid genome of coast redwood (Sequoia sempervirens) was completed leading toward discovery of genes related to climate adaptation and investigation of the origin of the hexaploid genome. Deep-coverage short-read Illumina sequencing data from haploid tissue from a single seed were combined with long-read Oxford Nanopore Technologies sequencing data from diploid needle tissue to create an initial assembly, which was then scaffolded using proximity ligation data to produce a highly contiguous final assembly, SESE 2.1, with a scaffold N50 size of 44.9 Mbp. The assembly included several scaffolds that span entire chromosome arms, confirmed by the presence of telomere and centromere sequences on the ends of the scaffolds. The structural annotation produced 118,906 genes with 113 containing introns that exceed 500 Kbp in length and one reaching 2 Mb. Nearly 19 Gbp of the genome represented repetitive content with the vast majority characterized as long terminal repeats, with a 2.9:1 ratio of Copia to Gypsy elements that may aid in gene expression control. Comparison of coast redwood to other conifers revealed species-specific expansions for a plethora of abiotic and biotic stress response genes, including those involved in fungal disease resistance, detoxification, and physical injury/structural remodeling and others supporting flavonoid biosynthesis. Analysis of multiple genes that exist in triplicate in coast redwood but only once in its diploid relative, giant sequoia, supports a previous hypothesis that the hexaploidy is the result of autopolyploidy rather than any hybridizations with separate but closely related conifer species.

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Genomic Analysis of European Drosophila melanogaster Populations Reveals Longitudinal Structure, Continent-Wide Selection, and Previously Unknown DNA Viruses

Molecular Biology and Evolution ◽

10.1093/molbev/msaa120 ◽

2020 ◽

Vol 37 (9) ◽

pp. 2661-2678 ◽

Cited By ~ 10

Author(s):

Martin Kapun ◽

Maite G Barrón ◽

Fabian Staubach ◽

Darren J Obbard ◽

R Axel W Wiberg ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Genetic Variation ◽

Climate Adaptation ◽

Natural Populations ◽

Genomic Analysis ◽

Selective Sweeps ◽

Short Term ◽

Dna Viruses ◽

Local Climate ◽

Term Evolution

Abstract Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterize variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.

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Unravelling population structure heterogeneity within the genome of the malaria vector Anopheles gambiae

BMC Genomics ◽

10.1186/s12864-021-07722-y ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Melina Campos ◽

Luisa D. P. Rona ◽

Katie Willis ◽

George K. Christophides ◽

Robert M. MacCallum

Keyword(s):

Population Structure ◽

Anopheles Gambiae ◽

Malaria Vector ◽

Mosquito Species ◽

Gene Clusters ◽

Selective Sweeps ◽

Structure Heterogeneity ◽

Genomic Studies ◽

Time Required ◽

Genomic Regions

Abstract Background Whole genome re-sequencing provides powerful data for population genomic studies, allowing robust inferences of population structure, gene flow and evolutionary history. For the major malaria vector in Africa, Anopheles gambiae, other genetic aspects such as selection and adaptation are also important. In the present study, we explore population genetic variation from genome-wide sequencing of 765 An. gambiae and An. coluzzii specimens collected from across Africa. We used t-SNE, a recently popularized dimensionality reduction method, to create a 2D-map of An. gambiae and An. coluzzii genes that reflect their population structure similarities. Results The map allows intuitive navigation among genes distributed throughout the so-called “mainland” and numerous surrounding “island-like” gene clusters. These gene clusters of various sizes correspond predominantly to low recombination genomic regions such as inversions and centromeres, and also to recent selective sweeps. Because this mosquito species complex has been studied extensively, we were able to support our interpretations with previously published findings. Several novel observations and hypotheses are also made, including selective sweeps and a multi-locus selection event in Guinea-Bissau, a known intense hybridization zone between An. gambiae and An. coluzzii. Conclusions Our results present a rich dataset that could be utilized in functional investigations aiming to shed light onto An. gambiae s.l genome evolution and eventual speciation. In addition, the methodology presented here can be used to further characterize other species not so well studied as An. gambiae, shortening the time required to progress from field sampling to the identification of genes and genomic regions under unique evolutionary processes.

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Natural variation in fecundity is correlated with species-wide levels of divergence in Caenorhabditis elegans

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab168 ◽

2021 ◽

Author(s):

Gaotian Zhang ◽

Jake D Mostad ◽

Erik C Andersen

Keyword(s):

Life History ◽

Caenorhabditis Elegans ◽

Life History Traits ◽

Life History Trait ◽

Selective Sweeps ◽

C Elegans ◽

Genome Wide ◽

Genetic Complexity ◽

Genomic Regions ◽

Global Population

Abstract Life history traits underlie the fitness of organisms and are under strong natural selection. A new mutation that positively impacts a life history trait will likely increase in frequency and become fixed in a population (e.g. a selective sweep). The identification of the beneficial alleles that underlie selective sweeps provides insights into the mechanisms that occurred during the evolution of a species. In the global population of Caenorhabditis elegans, we previously identified selective sweeps that have drastically reduced chromosomal-scale genetic diversity in the species. Here, we measured the fecundity of 121 wild C. elegans strains, including many recently isolated divergent strains from the Hawaiian islands and found that strains with larger swept genomic regions have significantly higher fecundity than strains without evidence of the recent selective sweeps. We used genome-wide association (GWA) mapping to identify three quantitative trait loci (QTL) underlying the fecundity variation. Additionally, we mapped previous fecundity data from wild C. elegans strains and C. elegans recombinant inbred advanced intercross lines that were grown in various conditions and detected eight QTL using GWA and linkage mappings. These QTL show the genetic complexity of fecundity across this species. Moreover, the haplotype structure in each GWA QTL region revealed correlations with recent selective sweeps in the C. elegans population. North American and European strains had significantly higher fecundity than most strains from Hawaii, a hypothesized origin of the C. elegans species, suggesting that beneficial alleles that caused increased fecundity could underlie the selective sweeps during the worldwide expansion of C. elegans.

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Effects of Selection at Linked Sites on Patterns of Genetic Variability

Annual Review of Ecology Evolution and Systematics ◽

10.1146/annurev-ecolsys-010621-044528 ◽

2021 ◽

Vol 52 (1) ◽

pp. 177-197

Author(s):

Brian Charlesworth ◽

Jeffrey D. Jensen

Keyword(s):

Genetic Variability ◽

Population Genetic ◽

Selective Sweeps ◽

Recombination Rates ◽

Frequency Distributions ◽

A Genome ◽

Demographic Processes ◽

Dna Sequence Variants ◽

Genomic Regions ◽

Functional Components

Patterns of variation and evolution at a given site in a genome can be strongly influenced by the effects of selection at genetically linked sites. In particular, the recombination rates of genomic regions correlate with their amount of within-population genetic variability, the degree to which the frequency distributions of DNA sequence variants differ from their neutral expectations, and the levels of adaptation of their functional components. We review the major population genetic processes that are thought to lead to these patterns, focusing on their effects on patterns of variability: selective sweeps, background selection, associative overdominance, and Hill–Robertson interference among deleterious mutations. We emphasize the difficulties in distinguishing among the footprints of these processes and disentangling them from the effects of purely demographic factors such as population size changes. We also discuss how interactions between selective and demographic processes can significantly affect patterns of variability within genomes.

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