The combined use of raw and phylogenetically independent methods of outlier detection uncovers genome‐wide dynamics of local adaptation in a lizard

Local adaptation can lead to elevated genetic differentiation at the targeted genetic variant and nearby sites. Selective sweeps come in different forms, and depending on the initial and final frequencies of a favored variant, very different patterns of genetic variation may be produced. If local selection favors an existing variant that had already recombined onto multiple genetic backgrounds, then the width of elevated genetic differentiation (high FST) may be too narrow to detect using a typical windowed genome scan, even if the targeted variant becomes highly differentiated. We therefore used a simulation approach to investigate the power of SNP-level FST (specifically, the maximum SNP FST value within a window) to detect diverse scenarios of local adaptation, and compared it against whole-window FST and the Comparative Haplotype Identity statistic. We found that SNP FST had superior power to detect complete or mostly complete soft sweeps, but lesser power than window-wide statistics to detect partial hard sweeps. To investigate the relative enrichment and nature of SNP FST outliers from real data, we applied the two FST statistics to a panel of Drosophila melanogaster populations. We found that SNP FST had a genome-wide enrichment of outliers compared to demographic expectations, and though it yielded a lesser enrichment than window FST, it detected mostly unique outlier genes and functional categories. Our results suggest that SNP FST is highly complementary to typical window-based approaches for detecting local adaptation, and merits inclusion in future genome scans and methodologies.

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Genomics of sorghum local adaptation to a parasitic plant

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1908707117 ◽

2020 ◽

Vol 117 (8) ◽

pp. 4243-4251 ◽

Cited By ~ 3

Author(s):

Emily S. Bellis ◽

Elizabeth A. Kelly ◽

Claire M. Lorts ◽

Huirong Gao ◽

Victoria L. DeLeo ◽

...

Keyword(s):

Genetic Diversity ◽

Local Adaptation ◽

Species Interactions ◽

Balancing Selection ◽

Control Plant ◽

Farming Systems ◽

Striga Hermonthica ◽

Loss Of Function ◽

Trade Offs ◽

Genome Wide

Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

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Genome-wide scan for runs of homozygosity identifies potential candidate genes associated with local adaptation in Valle del Belice sheep

Genetics Selection Evolution ◽

10.1186/s12711-017-0360-z ◽

2017 ◽

Vol 49 (1) ◽

Cited By ~ 35

Author(s):

Salvatore Mastrangelo ◽

Marco Tolone ◽

Maria T. Sardina ◽

Gianluca Sottile ◽

Anna M. Sutera ◽

...

Keyword(s):

Candidate Genes ◽

Local Adaptation ◽

Potential Candidate ◽

Runs Of Homozygosity ◽

Genome Wide ◽

Genome Wide Scan

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Linking genomic signatures of selection to expression variation and direct evidence of local adaptation

10.1101/2020.08.22.262394 ◽

2020 ◽

Author(s):

Nicholas Price ◽

Jack L. Mullen ◽

Junjiang Lin ◽

Christina Boucher ◽

John K. McKay

Keyword(s):

Cold Acclimation ◽

Local Adaptation ◽

Freezing Tolerance ◽

Evolutionary Biology ◽

Species Conservation ◽

Selective Constraint ◽

Expression Variation ◽

Genomic Signatures ◽

Genome Wide ◽

Signatures Of Selection

AbstractUnderstanding how genomic and expression variation is linked to adaptation of plants to local environments is fundamental to the fields of evolutionary biology and species conservation. Using locally adapted Arabidopsis thaliana Italy and Sweden populations, we examine how variation in gene expression under control and cold acclimation conditions, is linked to allele frequency differentiation (AFD); linkage disequilibrium (LD); selective constraint at nonsynonymous sites; and genetic-tradeoff quantitative trait loci (GT-QTL). Our results indicate that contrary to genes showing a main effect in environment (E), expression genotype by environment interactions (GxE) show significantly higher AFD along cis-regulatory and nonsynonymous sites than the neutral expectation; and interestingly, highly differentiated GxE genes show higher expression and inter-species selective constraint than the rest of the genes. When examining the association between genomic signatures of selection along GxE/E genes and GT-QTL, we find that GxE genes showing a high AFD and LD, display a significant and much higher enrichment along GT-QTL than the genome-wide/E set of genes. Nonetheless, E genes show a higher enrichment than the genome-wide control. In summary, our results suggest, that these highly expressed and selectively constrained GxE genes, may have been part of a cold-responsive regulon of E genes that experienced recent selection when migrating to new environments. Candidate GxE genes underlying GT-QTL reveal interesting biological processes that may underlie local adaptation to temperature, including flowering time, light-dependent cold acclimation, freezing tolerance, and response to hypoxia. Finally, we find no evidence linking lower expression of the CBF-dependent freezing tolerance pathway to genetic-tradeoffs and adaptation to warmer climates.

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Genomics of sorghum local adaptation to a parasitic plant

10.1101/633529 ◽

2019 ◽

Cited By ~ 1

Author(s):

Emily S. Bellis ◽

Elizabeth A. Kelly ◽

Claire M. Lorts ◽

Huirong Gao ◽

Victoria L. DeLeo ◽

...

Keyword(s):

Genetic Diversity ◽

Local Adaptation ◽

Striga Hermonthica ◽

Wild Plant ◽

Parasitic Weed ◽

Genome Wide ◽

Staple Crop ◽

Term Maintenance ◽

Maintenance Of Diversity

ABSTRACTHost-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential tradeoffs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and belowground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with tradeoffs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9 edited sorghum further indicate the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.SIGNIFICANCE STATEMENTUnderstanding co-evolution in crop-parasite systems is critical to management of myriad pests and pathogens confronting modern agriculture. In contrast to wild plant communities, parasites in agricultural ecosystems are usually expected to gain the upper hand in co-evolutionary ‘arms races’ due to limited genetic diversity of host crops in cultivation. Here, we develop a framework to characterize associations between genome variants in global landraces (traditional varieties) of the staple crop sorghum with the distribution of the devastating parasitic weed Striga hermonthica. We find long-term maintenance of diversity in genes related to parasite resistance, highlighting an important role of host adaptation for co-evolutionary dynamics in smallholder agroecosystems.

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Low genome-wide divergence between two lizard populations with high adaptive phenotypic differentiation

10.22541/au.163250123.31170409/v1 ◽

2021 ◽

Author(s):

Alejandro Llanos-Garrido ◽

Javier Pérez-Tris ◽

José Díaz

Keyword(s):

Local Adaptation ◽

Genetic Divergence ◽

Elevational Gradient ◽

Phenotypic Differentiation ◽

Genome Wide ◽

Isolation By Environment ◽

Psammodromus Algirus ◽

Low Levels ◽

Two Populations ◽

Degree Of Isolation

Usually, adaptive phenotypic differentiation is paralleled by genetic divergence between locally adapted populations. However, adaptation can also happen in a scenario of non-significant genetic divergence due to intense gene flow and/or recent differentiation. While this phenomenon is rarely published, findings on incipient ecologically-driven divergence or isolation by adaptation are relatively common, which could confound our understanding about the frequency at which they actually occur in nature. Here, we explore genome-wide traces of divergence between two populations of the lacertid lizard Psammodromus algirus separated by a 600 m elevational gradient. These populations seem to be differentially adapted to their environments despite showing low levels of genetic differentiation (according to previously studies of mtDNA and microsatellite data). We performed a search for outliers (i.e. loci subject to selection) trying to identify specific loci with FST statistics significantly higher than those expected on the basis of overall, genome-wide estimates of genetic divergence. We find that local phenotypic adaptation (in terms of a wide diversity of characters) was not accompanied by genome-wide differentiation, even when we maximized the chances of unveiling such differentiation at particular loci with FST-based outlier detection tests. Instead, our analyses confirmed the lack of differentiation on the basis of more than 70,000 SNPs, which is concordant with a scenario of local adaptation without any degree of isolation by environment. Our results add evidence to previous studies in which local adaptation does not lead to any kind of isolation (or early stages of ecological speciation), but maintains phenotypic divergence despite the lack of a differentiated genomic background.

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Local adaptation does not lead to genome‐wide differentiation in lava flow lizards

Ecology and Evolution ◽

10.1002/ece3.5231 ◽

2019 ◽

Vol 9 (12) ◽

pp. 6810-6820 ◽

Cited By ~ 1

Author(s):

Alexander R. Krohn ◽

Eveline T. Diepeveen ◽

Ke Bi ◽

Erica Bree Rosenblum

Keyword(s):

Lava Flow ◽

Local Adaptation ◽

Genome Wide

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Pooled population resequencing of clam shrimp (Eulimnadia texana) from different vernal pools reveals signatures of local adaptation

10.1101/223602 ◽

2017 ◽

Author(s):

James G. Baldwin-Brown ◽

Anthony D. Long

Keyword(s):

Local Adaptation ◽

Environmental Variables ◽

Vernal Pool ◽

Vernal Pools ◽

Genomic Region ◽

Population Subdivision ◽

Restricted Gene Flow ◽

Clam Shrimp ◽

Genome Wide ◽

A Genome

AbstractVernal pool clam shrimp (Eulimnadia texana) are a promising model due to ease of culturing, short generation time, modest genome size, and obligate desiccated diapaused eggs. We collected Illumina data (Poolseq) from eleven pooled wild vernal pool clam shrimp populations. We hypothesized that restricted gene flow between vernal pools, separated by distances of 0.36 to 253 km, in concert with Poolseq data from each population, could be used to identify genes important in local adaptation. We adapted Bayenv2 to genome-wide Poolseq data and detected thirteen genomic regions showing a strong excess of population subdivision relative to a genome-wide background. We identified a set of regions that appear to be significantly diverged in allele frequency, above what is expected based on the relationships amongst the populations. Regions identified as significant were on average 9.5 kb in size and harbored 3.8 genes. We attempted to identify correlations between allele frequencies at each genomic region and environmental variables that may influence local adaptation in the sequences populations, but found that there were too many confounding environmental variables to draw strong conclusions. One such genomic region harbored an ortholog of Drosophila melanogaster CG10413, a gene predicted to have sodium/potassium/chloride activity. Finally, we demonstrate that the identified regions could not have been found with less powerful statistics, i.e. FST, or with a less contiguous genome assembly.

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DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation

eLife ◽

10.7554/elife.05255 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 244

Author(s):

Manu J Dubin ◽

Pei Zhang ◽

Dazhe Meng ◽

Marie-Stanislas Remigereau ◽

Edward J Osborne ◽

...

Keyword(s):

Dna Methylation ◽

Local Adaptation ◽

Dna Methyltransferase ◽

Association Studies ◽

Genome Wide Association Studies ◽

Gene Body Methylation ◽

Genome Wide ◽

Different Temperatures ◽

Cis And Trans ◽

Methylation Variation

Epigenome modulation potentially provides a mechanism for organisms to adapt, within and between generations. However, neither the extent to which this occurs, nor the mechanisms involved are known. Here we investigate DNA methylation variation in Swedish Arabidopsis thaliana accessions grown at two different temperatures. Environmental effects were limited to transposons, where CHH methylation was found to increase with temperature. Genome-wide association studies (GWAS) revealed that the extensive CHH methylation variation was strongly associated with genetic variants in both cis and trans, including a major trans-association close to the DNA methyltransferase CMT2. Unlike CHH methylation, CpG gene body methylation (GBM) was not affected by growth temperature, but was instead correlated with the latitude of origin. Accessions from colder regions had higher levels of GBM for a significant fraction of the genome, and this was associated with increased transcription for the genes affected. GWAS revealed that this effect was largely due to trans-acting loci, many of which showed evidence of local adaptation.

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Replicated Landscape Genomics Identifies Evidence of Local Adaptation to Urbanization in Wood Frogs

Journal of Heredity ◽

10.1093/jhered/esz041 ◽

2019 ◽

Vol 110 (6) ◽

pp. 707-719 ◽

Cited By ~ 1

Author(s):

Jared J Homola ◽

Cynthia S Loftin ◽

Kristina M Cammen ◽

Caren C Helbing ◽

Inanc Birol ◽

...

Keyword(s):

Genetic Diversity ◽

Local Adaptation ◽

Parallel Evolution ◽

Urban Environments ◽

Wood Frogs ◽

Urban Populations ◽

Genome Wide ◽

Outlier Loci ◽

Selection Factors ◽

Fst Outlier

Abstract Native species that persist in urban environments may benefit from local adaptation to novel selection factors. We used double-digest restriction-side associated DNA (RAD) sequencing to evaluate shifts in genome-wide genetic diversity and investigate the presence of parallel evolution associated with urban-specific selection factors in wood frogs (Lithobates sylvaticus). Our replicated paired study design involved 12 individuals from each of 4 rural and urban populations to improve our confidence that detected signals of selection are indeed associated with urbanization. Genetic diversity measures were less for urban populations; however, the effect size was small, suggesting little biological consequence. Using an FST outlier approach, we identified 37 of 8344 genotyped single nucleotide polymorphisms with consistent evidence of directional selection across replicates. A genome-wide association study analysis detected modest support for an association between environment type and 12 of the 37 FST outlier loci. Discriminant analysis of principal components using the 37 FST outlier loci produced correct reassignment for 87.5% of rural samples and 93.8% of urban samples. Eighteen of the 37 FST outlier loci mapped to the American bullfrog (Rana [Lithobates] catesbeiana) genome, although none were in coding regions. This evidence of parallel evolution to urban environments provides a powerful example of the ability of urban landscapes to direct evolutionary processes.

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