Genomics of sorghum local adaptation to a parasitic plant

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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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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Transition from background selection to associative overdominance promotes diversity in regions of low recombination

10.1101/748004 ◽

2019 ◽

Cited By ~ 5

Author(s):

Kimberly J. Gilbert ◽

Fanny Pouyet ◽

Laurent Excoffier ◽

Stephan Peischl

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Purifying Selection ◽

Heterozygote Advantage ◽

Background Selection ◽

Deleterious Mutations ◽

Recombination Rates ◽

Locus Model ◽

Genome Wide ◽

Linked Selection

SummaryLinked selection is a major driver of genetic diversity. Selection against deleterious mutations removes linked neutral diversity (background selection, BGS, Charlesworth et al. 1993), creating a positive correlation between recombination rates and genetic diversity. Purifying selection against recessive variants, however, can also lead to associative overdominance (AOD, Ohta 1971, Zhao & Charlesworth, 2016), due to an apparent heterozygote advantage at linked neutral loci that opposes the loss of neutral diversity by BGS. Zhao & Charlesworth (2016) identified the conditions when AOD should dominate over BGS in a single-locus model and suggested that the effect of AOD could become stronger if multiple linked deleterious variants co-segregate. We present a model describing how and under which conditions multi-locus dynamics can amplify the effects of AOD. We derive the conditions for a transition from BGS to AOD due to pseudo-overdominance (Ohta & Kimura 1970), i.e. a form of balancing selection that maintains complementary deleterious haplotypes that mask the effect of recessive deleterious mutations. Simulations confirm these findings and show that multi-locus AOD can increase diversity in low recombination regions much more strongly than previously appreciated. While BGS is known to drive genome-wide diversity in humans (Pouyet et al. 2018), the observation of a resurgence of genetic diversity in regions of very low recombination is indicative of AOD. We identify 21 such regions in the human genome showing clear signals of multi-locus AOD. Our results demonstrate that AOD may play an important role in the evolution of low recombination regions of many species.

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Heterogeneity in effective size across the genome: effects on the Inverse Instantaneous Coalescence Rate (IICR) and implications for demographic inference under linked selection.

10.1101/2021.06.11.448122 ◽

2021 ◽

Author(s):

Simon Boitard ◽

Armando Arredondo ◽

Camille Noûs ◽

Lounes Chikhi ◽

Olivier Mazet

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Effective Population ◽

Recombination Rates ◽

Genome Wide ◽

Coalescence Rate ◽

Demographic Inference ◽

The Impact ◽

Linked Selection ◽

Coalescence Times

The relative contribution of selection and neutrality in shaping species genetic diversity is one of the most central and controversial questions in evolutionary theory. Genomic data provide growing evidence that linked selection, i.e. the modification of genetic diversity at neutral sites through linkage with selected sites, might be pervasive over the genome. Several studies proposed that linked selection could be modelled as first approximation by a local reduction (e.g. purifying selection, selective sweeps) or increase (e.g. balancing selection) of effective population size (Ne). At the genome-wide scale, this leads to a large variance of Ne from one region to another, reflecting the heterogeneity of selective constraints and recombination rates between regions. We investigate here the consequences of this variation of Ne on the genome-wide distribution of coalescence times. The underlying motivation concerns the impact of linked selection on demographic inference, because the distribution of coalescence times is at the heart of several important demographic inference approaches. Using the concept of Inverse Instantaneous Coalescence Rate, we demonstrate that in a panmictic population, linked selection always results in a spurious apparent decrease of Ne along time. Balancing selection has a particularly large effect, even when it concerns a very small part of the genome. We quantify the expected magnitude of the spurious decrease of Ne in humans and Drosophila melanogaster, based on Ne distributions inferred from real data in these species. We also find that the effect of linked selection can be significantly reduced by that of population structure.

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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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Supergene formation is associated with a major shift in genome-wide patterns of diversity in a butterfly

10.1101/2021.09.29.462348 ◽

2021 ◽

Author(s):

María Ángeles Rodríguez de Cara ◽

Paul Jay ◽

Mathieu Chouteau ◽

Annabel Whibley ◽

Barbara Huber ◽

...

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Mate Preferences ◽

Heterozygote Advantage ◽

Effective Population ◽

Adaptive Introgression ◽

Continental Scale ◽

Geographic Structure ◽

Genome Wide ◽

Genetic Diversity And Structure

AbstractSelection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genome-wide patterns of diversity and demographic responses. Adaptive introgression provides a way to assess how adaptive evolution at one locus impacts whole-genome biology. Here we study the patterns of genetic variation and geographic structure in a neotropical butterfly, Heliconius numata, and its closely related allies in the so-called melpomene-silvaniform subclade. H. numata is known to have evolved a supergene via the introgression of an adaptive inversion about 2.2 million years ago, triggering a polymorphism maintained by balancing selection. This locus controls variation in wing patterns involved in mimicry associations with distinct groups of co-mimics, and butterflies show disassortative mate preferences and heterozygote advantage at this locus. We contrasted patterns of genetic diversity and structure 1) among extant polymorphic and monomorphic populations of H. numata, 2) between H. numata and its close relatives, and 3) between ancestral lineages in a phylogenetic framework. We show that H. numata populations which carry the introgressed inversions in a balanced polymorphism show markedly distinct patterns of diversity compared to all other taxa. They show the highest diversity and demographic estimates in the entire clade, as well as a remarkably low level of geographic structure and isolation by distance across the entire Amazon basin. By contrast, monomorphic populations of H. numata as well as its sister species and their ancestral lineages all show the lowest effective population sizes and genetic diversity in the clade, and higher levels of geographical structure across the continent. This suggests that the large effective population size of polymorphic populations could be a property associated with harbouring the supergene. Our results are consistent with the hypothesis that the adaptive introgression of the inversion triggered a shift from directional to balancing selection and a change in gene flow due to disassortative mating, causing a general increase in genetic diversity and the homogenisation of genomes at the continental scale.

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Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection?

Genetics ◽

10.1093/genetics/138.3.811 ◽

1994 ◽

Vol 138 (3) ◽

pp. 811-828 ◽

Cited By ~ 3

Author(s):

U Hanfstingl ◽

A Berry ◽

E A Kellogg ◽

J T Costa ◽

W Rüdiger ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Alcohol Dehydrogenase ◽

Balancing Selection ◽

Haplotype Diversity ◽

Hypervariable Region ◽

Amino Acid Replacement ◽

Loss Of Function ◽

Closely Related Species ◽

Genome Wide ◽

Chemically Induced

Abstract We designate a region of the alcohol dehydrogenase locus (Adh) of the weedy crucifer, Arabidopsis thaliana, as "hypervariable" on the basis of a comparison of sequences from ecotypes Columbia and Landsberg. We found eight synonymous and two replacement mutations in the first 262 nucleotides of exon 4, and an additional two mutations in the contiguous region of intron 3. The rest of the sequence (2611 bp) has just three mutations, all of them confined to noncoding regions. Our survey of the hypervariable region among 37 ecotypes of A. thaliana revealed two predominant haplotypes, corresponding to the Columbia and Landsberg sequences. We identified five additional haplotypes and 4 additional segregating sites. The lack of haplotype diversity is presumably in part a function of low rates of recombination between haplotypes conferred by A. thaliana's tendency to self-fertilize. However, an analysis in 32 ecotypes of 12 genome-wide polymorphic markers distinguishing Columbia and Landsberg ecotypes indicated levels of outcrossing sufficient at least to erode linkage disequilibrium between dispersed markers. We discuss possible evolutionary explanations for the coupled observation of marked divergence within the hypervariable region and a lack of haplotype diversity among ecotypes. The sequence of the region for closely related species argues against the possibility that one allele is the product of introgression. We note (1) that several loss of function mutations (both naturally and chemically induced) map to the hypervariable region, and (2) the presence of two amino acid replacement polymorphisms, one of which causes the mobility difference between the two major classes of A. thaliana Adh electrophoretic alleles. We argue that protein polymorphism in such a functionally significant part of the molecule may be subject to balancing selection. The observed pattern of extensive divergence between the alleles is consistent with this explanation because balancing selection on a particular site maintains linked neutral polymorphisms at intermediate frequencies.

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Local adaptation and spatiotemporal patterns of genetic diversity revealed by repeated sampling of Caenorhabditis elegans across the Hawaiian Islands

10.1101/2021.10.11.463952 ◽

2021 ◽

Author(s):

Timothy A. Crombie ◽

Paul Battlay ◽

Robyn E. Tanny ◽

Kathryn S. Evans ◽

Claire M. Buchanan ◽

...

Keyword(s):

Genetic Diversity ◽

Caenorhabditis Elegans ◽

Local Adaptation ◽

Balancing Selection ◽

Sampling Site ◽

Hawaiian Islands ◽

Pathogen Resistance ◽

Pacific Rim ◽

High Genetic Diversity ◽

C Elegans

AbstractThe nematode Caenorhabditis elegans is among the most widely studied organisms, but relatively little is known about its natural ecology. Wild C. elegans have been isolated from both temperate and tropical climates, where they feed on bacteria associated with decomposing plant material. Genetic diversity is low across much of the globe but high in the Hawaiian Islands and across the Pacific Rim. The high genetic diversity found there suggests that: (1) the origin of the species lies in Hawaii or the surrounding Pacific Rim; and (2) the ancestral niche of the species is likely similar to the Hawaiian niche. A recent study of the Hawaiian niche found that genetically distinct groups appeared to correlate with elevation and temperature, but the study had a limited sample size. To better characterize the niche and genetic diversity of C. elegans on the Hawaiian Islands and to explore how genetic diversity might be influenced by local adaptation, we repeatedly sampled nematodes over a three-year period, measured various environmental parameters at each sampling site, and whole-genome sequenced the C. elegans isolates that we identified. We found that the typical Hawaiian C. elegans niche is moderately moist native forests at high elevations (500 to 1500 meters) where temperatures are cool (15 to 20°C). We measured levels of genetic diversity and differentiation among Hawaiian strains and found evidence of seven genetically distinct groups distributed across the islands. Then, we scanned these genomes for signatures of local adaptation and identified 18 distinct regions that overlap with hyperdivergent regions, which are likely maintained by balancing selection and enriched for genes related to environmental sensing, xenobiotic detoxification, and pathogen resistance. These results provide strong evidence of local adaptation among Hawaiian C. elegans and a possible genetic basis for this adaptation.

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Genome-wide SNP analysis of three moose subspecies at the southern range limit in the contiguous United States

Conservation Genetics ◽

10.1007/s10592-021-01402-w ◽

2021 ◽

Author(s):

Jason A. Ferrante ◽

Chase H. Smith ◽

Laura M. Thompson ◽

Margaret E. Hunter

Keyword(s):

United States ◽

Genetic Diversity ◽

Species Interactions ◽

The United States ◽

Conservation Priorities ◽

Putative Hybrid ◽

Snp Analysis ◽

Range Limit ◽

Genome Wide ◽

Management And Conservation

AbstractGenome-wide evaluations of genetic diversity and population structure are important for informing management and conservation of trailing-edge populations. North American moose (Alces alces) are declining along portions of the southern edge of their range due to disease, species interactions, and marginal habitat, all of which may be exacerbated by climate change. We employed a genotyping by sequencing (GBS) approach in an effort to collect baseline information on the genetic variation of moose inhabiting the species’ southern range periphery in the contiguous United States. We identified 1920 single nucleotide polymorphisms (SNPs) from 155 moose representing three subspecies from five states: A. a. americana (New Hampshire), A. a. andersoni (Minnesota), and A. a. shirasi (Idaho, Montana, and Wyoming). Molecular analyses supported three geographically isolated clusters, congruent with currently recognized subspecies. Additionally, while moderately low genetic diversity was observed, there was little evidence of inbreeding. Results also indicated > 20% shared ancestry proportions between A. a. shirasi samples from northern Montana and A. a. andersoni samples from Minnesota, indicating a putative hybrid zone warranting further investigation. GBS has proven to be a simple and effective method for genome-wide SNP discovery in moose and provides robust data for informing herd management and conservation priorities. With increasing disease, predation, and climate related pressure on range edge moose populations in the United States, the use of SNP data to identify gene flow between subspecies may prove a powerful tool for moose management and recovery, particularly if hybrid moose are more able to adapt.

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Influence of environmental factors on the genetic variation of the aquatic macrophyte Ranunculus subrigidus on the Qinghai-Tibetan Plateau

BMC Evolutionary Biology ◽

10.1186/s12862-019-1559-0 ◽

2019 ◽

Vol 19 (1) ◽

Cited By ~ 2

Author(s):

Zhigang Wu ◽

Xinwei Xu ◽

Juan Zhang ◽

Gerhard Wiegleb ◽

Hongwei Hou

Keyword(s):

Genetic Diversity ◽

Tibetan Plateau ◽

Environmental Factors ◽

Local Adaptation ◽

Aquatic Macrophyte ◽

Spatial Genetic Structure ◽

Long Distance ◽

Elevation Gradients ◽

Mantel Tests ◽

Genetic Patterns

Abstract Background Due to the environmental heterogeneity along elevation gradients, alpine ecosystems are ideal study objects for investigating how ecological variables shape the genetic patterns of natural species. The highest region in the world, the Qinghai-Tibetan Plateau, is a hotspot for the studies of evolutionary processes in plants. Many large rivers spring from the plateau, providing abundant habitats for aquatic and amphibious organisms. In the present study, we examined the genetic diversity of 13 Ranunculus subrigidus populations distributed throughout the plateau in order to elucidate the relative contribution of geographic distance and environmental dissimilarity to the spatial genetic pattern. Results A relatively low level of genetic diversity within populations was found. No spatial genetic structure was suggested by the analyses of molecular variance, Bayesian clustering analysis and Mantel tests. Partial Mantel tests and multiple matrix regression analysis showed a significant influence of the environment on the genetic divergence of the species. Both climatic and water quality variables contribute to the habitat heterogeneity of R. subrigidus populations. Conclusions Our results suggest that historical processes involving long-distance dispersal and local adaptation may account for the genetic patterns of R. subrigidus and current environmental factors play an important role in the genetic differentiation and local adaptation of aquatic plants in alpine landscapes.

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