scholarly journals Karyotype-environment associations support a role for a chromosomal inversion in local adaptation in the seaweed fly Coelopa frigida

2018 ◽  
Author(s):  
Claire Mérot ◽  
Emma Berdan ◽  
Charles Babin ◽  
Eric Normandeau ◽  
Maren Wellenreuther ◽  
...  
Keyword(s):  
North America ◽  
Local Adaptation ◽  
Environmental Gradients ◽  
Balancing Selection ◽  
Natural Populations ◽  
Inversion Polymorphism ◽  
Life History Strategies ◽  
Heterogeneous Environments ◽  
Adult Size ◽  
Coelopa Frigida

AbstractLarge chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialisation. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2,000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.

scholarly journals Intercontinental karyotype–environment parallelism supports a role for a chromosomal inversion in local adaptation in a seaweed fly

2018 ◽  
Vol 285 (1881) ◽  
pp. 20180519 ◽  
Author(s):  
Claire Mérot ◽  
Emma L. Berdan ◽  
Charles Babin ◽  
Eric Normandeau ◽  
Maren Wellenreuther ◽  
...  
Keyword(s):  
North America ◽  
Local Adaptation ◽  
Environmental Gradients ◽  
Balancing Selection ◽  
Chromosomal Rearrangements ◽  
Natural Populations ◽  
Inversion Polymorphism ◽  
Life History Strategies ◽  
Heterogeneous Environments ◽  
Adult Size

Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialization. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely to be maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.

scholarly journals Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

2019 ◽  
Author(s):  
Claire Mérot ◽  
Violaine Llaurens ◽  
Eric Normandeau ◽  
Louis Bernatchez ◽  
Maren Wellenreuther
Keyword(s):  
Life History ◽  
Balancing Selection ◽  
Natural Populations ◽  
Inversion Polymorphism ◽  
Antagonistic Pleiotropy ◽  
Trade Off ◽  
Trade Offs ◽  
Survival And Reproduction ◽  
Coelopa Frigida

AbstractHow genetic diversity is maintained in natural populations is an evolutionary puzzle. Over time, genetic variation within species can be eroded by drift and directional selection, leading to the fixation or elimination of alleles. However, some loci show persistent variants at intermediate frequencies for long evolutionary time-scales, implicating a role of balancing selection, but studies are seldom set up to uncover the underlying processes. Here, we identify and quantify the selective pressures involved in the widespread maintenance of an inversion polymorphism in the seaweed fly Coelopa frigida, using an experimental evolution approach to estimate fitness associated with different allelic combinations. By precisely evaluating reproductive success and survival rates separately, we show that the maintenance of the polymorphism is governed by a life-history trade-off, whereby each inverted haplotype has opposed pleiotropic effects on survival and reproduction. Using numerical simulations, we confirm that this uncovered antagonism between natural and sexual selection can maintain inversion variation in natural populations of C. frigida. Moreover, our experimental data highlights that inversion-associated fitness is affected differently by sex, dominance and environmental heterogeneity. The interaction between these factors promotes polymorphism maintenance through antagonistic pleiotropy. Taken together, our findings indicate that combinations of natural and sexual selective mechanisms enable the persistence of diverse trait in nature. The joint dynamics of life history trade-offs and antagonistic pleiotropy documented here is likely to apply to other species where large phenotypic variation is controlled by structural variants.Significance statementPersistence of chromosomal rearrangements is widespread in nature and often associated with divergent life-history traits. Understanding how contrasted life-history strategies are maintained in wild populations has implications for food production, health and biodiversity in a changing environment. Using the seaweed fly Coelopa frigida, we show that a polymorphic chromosomal inversion is maintained by a trade-off between survival and reproduction, and thus provide empirical support for a role of balancing selection via antagonistic pleiotropy. This mechanism has long been overlooked because it was thought to only apply to a narrow range of ecological scenarios. These findings empirically reinforce the recent theoretical predictions that co-interacting factors (dominance, environment and sex) can lead to polymorphism maintenance by antagonistic pleiotropy and favour life-history variation.

scholarly journals A New Catalog of Structural Variants in 1,301 A. thaliana Lines from Africa, Eurasia, and North America Reveals a Signature of Balancing Selection at Defense Response Genes

2020 ◽  
Author(s):  
Mehmet Göktay ◽  
Andrea Fulgione ◽  
Angela M Hancock
Keyword(s):  
North America ◽  
Defense Response ◽  
Balancing Selection ◽  
Natural Populations ◽  
Housekeeping Genes ◽  
Intermediate Frequency ◽  
Genomic Variation ◽  
Nucleotide Polymorphisms ◽  
Structural Variants ◽  
Defense Response Genes

Abstract Genomic variation in the model plant Arabidopsis thaliana has been extensively used to understand evolutionary processes in natural populations, mainly focusing on single-nucleotide polymorphisms. Conversely, structural variation has been largely ignored in spite of its potential to dramatically affect phenotype. Here, we identify 155,440 indels and structural variants ranging in size from 1 bp to 10 kb, including presence/absence variants (PAVs), inversions, and tandem duplications in 1,301 A. thaliana natural accessions from Morocco, Madeira, Europe, Asia, and North America. We show evidence for strong purifying selection on PAVs in genes, in particular for housekeeping genes and homeobox genes, and we find that PAVs are concentrated in defense-related genes (R-genes, secondary metabolites) and F-box genes. This implies the presence of a “core” genome underlying basic cellular processes and a “flexible” genome that includes genes that may be important in spatially or temporally varying selection. Further, we find an excess of intermediate frequency PAVs in defense response genes in nearly all populations studied, consistent with a history of balancing selection on this class of genes. Finally, we find that PAVs in genes involved in the cold requirement for flowering (vernalization) and drought response are strongly associated with temperature at the sites of origin.

scholarly journals The WZA: A window-based method for characterizing genotype-environment association

2021 ◽  
Author(s):  
Tom Booker ◽  
Sam Yeaman ◽  
Michael Whitlock
Keyword(s):  
Population Structure ◽  
Local Adaptation ◽  
Selection Pressure ◽  
Genetic Basis ◽  
Natural Populations ◽  
Original Study ◽  
Published Data ◽  
Heterogeneous Environments ◽  
Candidate Loci ◽  
Number Of Individuals

Genotype environment association (GEA) studies have the potential to elucidate the genetic basis of local adaptation in natural populations. Specifically, GEA approaches look for a correlation between allele frequencies and putatively selective features of the environment. Genetic markers with extreme evidence of correlation with the environment are presumed to be tagging the location of alleles that contribute to local adaptation. In this study, we propose a new method for GEA studies called the weighted-Z analysis (WZA) that combines information from closely linked sites into analysis windows in a way that was inspired by methods for calculating FST. We analyze simulations modelling local adaptation to heterogeneous environments either using a GEA method that controls for population structure or an uncorrected approach. In the majority of cases we tested, the WZA either outperformed single-SNP based approaches or performed similarly. The WZA outperformed individual SNP approaches when the measured environment is not perfectly correlated with the true selection pressure or when a small number of individuals or demes was sampled. We apply the WZA to previously published data from lodgepole pine and identified candidate loci that were not found in the original study.

scholarly journals Community monopolization: local adaptation enhances priority effects in an evolving metacommunity

2009 ◽  
Vol 276 (1676) ◽  
pp. 4129-4138 ◽  
Author(s):  
Mark C. Urban ◽  
Luc De Meester
Keyword(s):  
Local Adaptation ◽  
Environmental Gradients ◽  
Natural Populations ◽  
Species Distributions ◽  
Priority Effects ◽  
Priority Effect ◽  
Colonization History ◽  
Biological Communities ◽  
Structure And Dynamics ◽  
Individual Based Simulation

The diversity and composition of biological communities might often depend on colonization history because early colonists can exclude future colonists through a priority effect. These priority effects, which have been observed across a wide variety of ecosystems, often arise because early colonists have sufficient time to use available resources efficiently and subsequently withhold them from invaders. Here, we explore the extent to which rapid local adaptive evolution contributes to the pervasiveness of these priority effects. Using an individual-based simulation, we show that early colonization allows the descendants of colonists to adapt to novel conditions and reduce the establishment success of an initially ecologically equivalent competing species. Our model predicts that slight differences in colonization timing and adaptive capacity between species can substantially alter the dynamics and diversity of communities. We also show that priority effects and gene flow can generate a novel mechanism for the expansion and retraction of species distributions in a metacommunity. Our results suggest that local adaptation combined with stochastic colonization events can obscure direct relationships between species distributions and environmental gradients. Given the increasing recognition of rapid, microgeographic evolution in natural populations, we expect that evolutionary priority effects could affect the structure and dynamics of many natural metacommunities.

scholarly journals The WZA: A window-based method for characterizing genotype-environment association

2021 ◽  
Author(s):  
Tom R Booker ◽  
Sam Yeaman ◽  
Michael Whitlock
Keyword(s):  
Population Structure ◽  
Local Adaptation ◽  
Selection Pressure ◽  
Genetic Basis ◽  
Natural Populations ◽  
Original Study ◽  
Published Data ◽  
Heterogeneous Environments ◽  
Candidate Loci ◽  
Number Of Individuals

Genotype environment association (GEA) studies have the potential to elucidate the genetic basis of local adaptation in natural populations. Specifically, GEA approaches look for a correlation between allele frequencies and putatively selective features of the environment. Genetic markers with extreme evidence of correlation with the environment are presumed to be tagging the location of alleles that contribute to local adaptation. In this study, we propose a new method for GEA studies called the weighted-Z analysis (WZA) that combines information from closely linked sites into analysis windows in a way that was inspired by methods for calculating FST. We analyze simulations modelling local adaptation to heterogeneous environments either using a GEA method that controls for population structure or an uncorrected approach. In the majority of cases we tested, the WZA either outperformed single-SNP based approaches or performed similarly. The WZA outperformed individual SNP approaches when the measured environment is not perfectly correlated with the true selection pressure or when a small number of individuals or demes was sampled. We apply the WZA to previously published data from lodgepole pine identified candidate loci that were not found in the original study.

scholarly journals Phenotypic and Genomic Local Adaptation across Latitude and Altitude in Populus trichocarpa

2019 ◽  
Vol 11 (8) ◽  
pp. 2256-2272 ◽  
Author(s):  
Man Zhang ◽  
Haktan Suren ◽  
Jason A Holliday
Keyword(s):  
Local Adaptation ◽  
Environmental Gradients ◽  
Populus Trichocarpa ◽  
Latitudinal Gradients ◽  
Exome Capture ◽  
Phenotypic Traits ◽  
Clinal Variation ◽  
Heterogeneous Environments ◽  
Climatic Adaptation ◽  
Adaptive Architectures

Abstract Local adaptation to climate allows plants to cope with temporally and spatially heterogeneous environments, and parallel phenotypic clines provide a natural experiment to uncover the genomic architecture of adaptation. Though extensive effort has been made to investigate the genomic basis of local adaptation to climate across the latitudinal range of tree species, less is known for altitudinal clines. We used exome capture to genotype 451 Populus trichocarpa genotypes across altitudinal and latitudinal gradients spanning the natural species range, and phenotyped these trees for a variety of adaptive traits in two common gardens. We observed clinal variation in phenotypic traits across the two transects, which indicates climate-driven selection, and coupled gene-based genotype–phenotype and genotype–environment association scans to identify imprints of climatic adaptation on the genome. Although many of the phenotype- and climate-associated genes were unique to one transect, we found evidence of parallelism between latitude and altitude, as well as significant convergence when we compared our outlier genes with those putatively involved in climatic adaptation in two gymnosperm species. These results suggest that not only genomic constraint during adaptation to similar environmental gradients in poplar but also different environmental contexts, spatial scale, and perhaps redundant function among potentially adaptive genes and polymorphisms lead to divergent adaptive architectures.

scholarly journals ddRAD-seq Reveals Cryptic Phylogeographic Structure and Adaptive Population Differentiation of Hyporhamphus Intermedius in Heterogeneous Environments from China Mainland

2020 ◽  
Author(s):  
Gongpei Wang ◽  
Han Lai ◽  
Sheng Bi ◽  
Dingli Guo ◽  
Xiaopin Zhao ◽  
...  
Keyword(s):  
Local Adaptation ◽  
Population Differentiation ◽  
Balancing Selection ◽  
Abiotic Factors ◽  
Demographic History ◽  
Ancestral Population ◽  
Phylogeographic Structure ◽  
Species Differentiation ◽  
Heterogeneous Environments ◽  
The Impact

Abstract BackgroundSpecies differentiation and local adaptation in heterogeneous environments have been getting a large focus but poor knowledge of the mechanism. With widespread in coastal areas and the hyperdiverse freshwater systems in China, Hyporhamphus intermedius is an excellent material for phylogeography and local adaptation research. Here, 156 individuals were sampled in 8 sites from heterogeneous aquatic habitats to comprehend environmental and genetic contributions to phenotypic divergence. Results32,744 SNPs among populations and obvious population differentiation was found by ddRAD-seq among groups from the different watersheds. Population genetic structure was partly geographic, successfully classifying all individuals into three genetic subgroups corresponding to the North, the South and the Plateau Lakes with more migrations within region. Due to the transplant event, the strikingly increasing divergence in a short time indicated the tendency of local differentiation for introduced populations in the Plateau Lakes. Dorsal and anal traits varied widely between the Southern and others, which highlighted previously unrecognized lineages. Furthermore, we inferred the whole population is in response to balancing selection from neutrality test with positive value (Tajima's D=2.773), and demographic history underlay two main split events from the northern ancestral population. Subgroup ranges appear to counterparts to geographic regions with heterogeneous hydrological factors, indicating these features are likely important drivers of diversification.ConclusionsAccordingly, our results revealed that genetic polymorphism and divergence of Hyporhamphus intermedius in heterogeneous environments might be ascribed to a consequence of balancing selection, gene flow at microscales, and the impact of abiotic factors, verifying potentially that genetic differences among populations are the result of both genetic canalization and plastic responses to environmental heterogeneity.

scholarly journals A major locus controls local adaptation and adaptive life history variation in a perennial plant

2017 ◽  
Author(s):  
Jing Wang ◽  
Jihua Ding ◽  
Biyue Tan ◽  
Kathryn M. Robinson ◽  
Ingrid H. Michelson ◽  
...  
Keyword(s):  
Life History ◽  
Local Adaptation ◽  
Environmental Gradients ◽  
Natural Populations ◽  
Major Effect ◽  
Life History Trait ◽  
Life History Variation ◽  
Phenotypic Data ◽  
Bud Set ◽  
European Aspen

AbstractBackgroundThe initiation of growth cessation and dormancy represent critical life-history tradeoffs between survival and growth, and have important fitness effects in perennial plants. Such adaptive life history traits often show strong local adaptation along environmental gradients but despite their importance, the genetic architecture of these traits remains poorly understood.ResultsWe integrate whole genome re-sequencing with environmental and phenotypic data from common garden experiments to investigate the genomic basis of local adaptation across a latitudinal gradient in European aspen (Populus tremula). We discover a single genomic region containing the PtFT2 gene that mediates local adaptation in the timing of bud set and that explains 65% of the observed genetic variation in bud set. This locus is the likely target of a recent selective sweep that originated right before or during colonization of northern Scandinavia following the last glaciation. Field and greenhouse experiments confirm that variation in PtFT2 gene expression affect the phenotypic variation in bud set that we observe in wild natural populations.ConclusionsOur results reveal a major effect locus that determine the timing of bud set and that have facilitated rapid adaptation to shorter growing seasons and colder climates in European aspen. The discovery of a single locus explaining a substantial fraction of the variation in a key life history trait is remarkable given that such traits are generally considered to be highly polygenic. These findings provide a dramatic illustration of how loci of large-effect for adaptive traits can arise and be maintained over large geographical scales in natural populations.

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