In absence of local adaptation, plasticity and spatially varying selection rule: a view from genomic reaction norms in a panmictic species (Anguilla rostrata)

ABSTRACTSignatures of spatially varying selection have been investigated both at the genomic and transcriptomic level in several organisms. In Drosophila melanogaster, the majority of these studies have analyzed North American and Australian populations, leading to the identification of several loci and traits under selection. However, populations in these two continents showed evidence of admixture that likely contributed to the observed population differentiation patterns. Thus, disentangling demography from selection is challenging when analyzing these populations. European populations could be a suitable system to identify loci under spatially varying selection provided that no recent admixture from African populations would have occurred. In this work, we individually sequence the genome of 42 European strains collected in populations from contrasting environments: Stockholm (Sweden), and Castellana Grotte, (Southern Italy). We found low levels of population structure and no evidence of recent African admixture in these two populations. We thus look for patterns of spatially varying selection affecting individual genes and gene sets. Besides single nucleotide polymorphisms, we also investigate the role of transposable elements in local adaptation. We concluded that European populations are a good dataset to identify loci under spatially varying selection. The analysis of the two populations sequenced in this work in the context of all the available D. melanogaster data allowed us to pinpoint genes and biological processes relevant for local adaptation. Identifying and analyzing populations with low levels of population structure and admixture should help to disentangle selective from non-selective forces underlying patterns of population differentiation in other species as well.

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Local adaptation and the evolution of inversions on sex chromosomes and autosomes

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2017.0423 ◽

2018 ◽

Vol 373 (1757) ◽

pp. 20170423 ◽

Cited By ~ 12

Author(s):

Tim Connallon ◽

Colin Olito ◽

Ludovic Dutoit ◽

Homa Papoli ◽

Filip Ruzicka ◽

...

Keyword(s):

Gene Flow ◽

Local Adaptation ◽

Evolutionary Dynamics ◽

Deleterious Mutation ◽

Local Selection ◽

Theoretical Predictions ◽

Elevated Rate ◽

Genomic Regions ◽

Spatially Varying ◽

Spatially Varying Selection

Spatially varying selection with gene flow can favour the evolution of inversions that bind locally adapted alleles together, facilitate local adaptation and ultimately drive genomic divergence between species. Several studies have shown that the rates of spread and establishment of new inversions capturing locally adaptive alleles depend on a suite of evolutionary factors, including the strength of selection for local adaptation, rates of gene flow and recombination, and the deleterious mutation load carried by inversions. Because the balance of these factors is expected to differ between X (or Z) chromosomes and autosomes, opportunities for inversion evolution are likely to systematically differ between these genomic regions, though such scenarios have not been formally modelled. Here, we consider the evolutionary dynamics of X-linked and autosomal inversions in populations evolving at a balance between migration and local selection. We identify three factors that lead to asymmetric rates of X-linked and autosome inversion establishment: (1) sex-biased migration, (2) dominance of locally adapted alleles and (3) chromosome-specific deleterious mutation loads. This theory predicts an elevated rate of fixation, and depressed opportunities for polymorphism, for X-linked inversions. Our survey of data on the genomic distribution of polymorphic and fixed inversions supports both theoretical predictions. This article is part of the theme issue ‘Linking local adaptation with the evolution of sex differences'.

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Global adaptation confounds the search for local adaptation

10.1101/742247 ◽

2019 ◽

Cited By ~ 1

Author(s):

Tom R. Booker ◽

Sam Yeaman ◽

Michael C. Whitlock

Keyword(s):

Genetic Differentiation ◽

Local Adaptation ◽

Natural Populations ◽

Wide Distribution ◽

Structured Populations ◽

Substantial Contribution ◽

Beneficial Mutations ◽

Genome Wide ◽

Spatially Varying ◽

Spatially Varying Selection

AbstractSpatially varying selection promotes variance in allele frequencies, increasing genetic differentiation between the demes of a metapopulation. For that reason, outliers in the genome wide distribution of summary statistics measuring genetic differentiation, such as FST, are often interpreted as evidence for alleles which contribute to local adaptation. However, in spatially structured populations, the spread of beneficial mutations with spatially uniform effects can also induce transient genetic differentiation and numerous theoretical studies have suggested that species-wide, or global, adaptation makes a substantial contribution to molecular evolution. In this study, we ask whether such global adaptation affects the genome-wide distribution of FST and generates statistical outliers which could be mistaken for local adaptation. Using forward-in-time population genetic simulations assuming parameters for the rate and strength of beneficial mutations similar to those that have been estimated for natural populations, we show the spread of globally beneficial in parapatric populations can readily generate FST outliers, which may be misinterpreted as evidence for local adaptation. The spread of beneficial mutations causes selective sweeps at flanking sites, so the effects of global versus local adaptation may be distinguished by examining patterns of nucleotide diversity along with FST. Our study suggests that global adaptation should be considered in the interpretation of genome-scan results and the design of future studies aimed at understanding the genetic basis of local adaptation.

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Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster

10.1101/009084 ◽

2014 ◽

Cited By ~ 2

Author(s):

Alan O. Bergland ◽

Ray Tobler ◽

Josefa Gonzalez ◽

Paul Schmidt ◽

Dmitri Petrov

Keyword(s):

Drosophila Melanogaster ◽

North America ◽

Local Adaptation ◽

Latitudinal Gradients ◽

Secondary Contact ◽

Clinal Variation ◽

Evolutionary Forces ◽

Genome Wide ◽

Spatially Varying ◽

Spatially Varying Selection

Populations arrayed along broad latitudinal gradients often show patterns of clinal variation in phenotype and genotype. Such population differentiation can be generated and maintained by historical demographic events and local adaptation. These evolutionary forces are not mutually exclusive and, moreover, can in some cases produce nearly identical patterns of genetic differentiation among populations. Here, we investigate the evolutionary forces that generated and maintain clinal variation genome-wide among populations ofDrosophila melanogastersampled in North America and Australia. We contrast patterns of clinal variation in these continents with patterns of differentiation among ancestral European and African populations. Using established and novel methods we derive here, we show that recently derived North America and Australia populations were likely founded by both European and African lineages and that this admixture event contributed to genome-wide patterns of parallel clinal variation. The pervasive effects of admixture meant that only a handful of loci could be attributed to the operation of spatially varying selection using an FST outlier approach. Our results provide novel insight into the well-studied system of clinal differentiation inD. melanogasterand provide a context for future studies seeking to identify loci contributing to local adaptation in a wide variety of organisms, including other invasive species as well as some temperate endemics.

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Do Differences in Latitudinal Distributions of Species and Organelle Haplotypes Reflect Thermal Reaction Norms Within the Emiliania/Gephyrocapsa Complex?

Frontiers in Marine Science ◽

10.3389/fmars.2021.785763 ◽

2021 ◽

Vol 8 ◽

Author(s):

Peter von Dassow ◽

Paula Valentina Muñoz Farías ◽

Sarah Pinon ◽

Esther Velasco-Senovilla ◽

Simon Anguita-Salinas

Keyword(s):

Local Adaptation ◽

Coastal Upwelling ◽

Environmental Gradients ◽

Reaction Norm ◽

Emiliania Huxleyi ◽

Thermal Reaction ◽

Reaction Norms ◽

Thermal Niche ◽

Significant Difference ◽

The Difference

The cosmopolitan phytoplankter Emiliania huxleyi contrasts with its closest relatives that are restricted to narrower latitudinal bands, making it interesting for exploring how alternative outcomes in phytoplankton range distributions arise. Mitochondrial and chloroplast haplogroups within E. huxleyi are shared with their closest relatives: Some E. huxleyi share organelle haplogroups with Gephyrocapsa parvula and G. ericsonii which inhabit lower latitudes, while other E. huxleyi share organelle haplogroups with G. muellerae, which inhabit high latitudes. We investigated whether the phylogeny of E. huxleyi organelles reflects environmental gradients, focusing on the Southeast Pacific where the different haplogroups and species co-occur. There was a high congruence between mitochondrial and chloroplast haplogroups within E. huxleyi. Haplogroup II of E. huxleyi is negatively associated with cooler less saline waters, compared to haplogroup I, both when analyzed globally and across temporal variability at the small special scale of a center of coastal upwelling at 30° S. A new mitochondrial haplogroup Ib detected in coastal Chile was associated with warmer waters. In an experiment focused on inter-species comparisons, laboratory-determined thermal reaction norms were consistent with latitudinal/thermal distributions of species, with G. oceanica exhibiting warm thermal optima and tolerance and G. muellerae exhibiting cooler thermal optima and tolerances. Emiliania huxleyi haplogroups I and II tended to exhibit a wider thermal niche compared to the other Gephyrocapsa, but no differences among haplogroups within E. huxleyi were found. A second experiment, controlling for local adaptation and time in culture, found a significant difference between E. huxleyi haplogroups. The difference between I and II was of the expected sign, but not the difference between I and Ib. The differences were small (≤1°C) compared to differences reported previously within E. huxleyi by local adaptation and even in-culture evolution. Haplogroup Ib showed a narrower thermal niche. The cosmopolitanism of E. huxleyi might result from both wide-spread generalist phenotypes and specialist phenotypes, as well as a capacity for local adaptation. Thermal reaction norm differences can well explain the species distributions but poorly explain distributions among mitochondrial haplogroups within E. huxleyi. Perhaps organelle haplogroup distributions reflect historical rather than selective processes.

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Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub-Saharan Africa

Journal of Evolutionary Biology ◽

10.1111/jeb.12607 ◽

2015 ◽

Vol 28 (4) ◽

pp. 826-840 ◽

Cited By ~ 30

Author(s):

D. K. Fabian ◽

J. B. Lack ◽

V. Mathur ◽

C. Schlötterer ◽

P. S. Schmidt ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Life History ◽

Sub Saharan Africa ◽

Sub Saharan ◽

Spatially Varying ◽

Spatially Varying Selection

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Major QTL controls adaptation to serpentine soils in Mimulus guttatus

10.1101/328617 ◽

2018 ◽

Author(s):

Jessica P. Selby ◽

John H. Willis

Keyword(s):

Genetic Basis ◽

Common Garden ◽

Serpentine Soils ◽

Mimulus Guttatus ◽

Fitness Effects ◽

Spatially Varying ◽

Spatially Varying Selection ◽

Physical Challenges ◽

Two Populations ◽

Major Qtl

ABSTRACTSpatially varying selection is a critical driver of adaptive differentiation. Yet, there are few examples where the fitness effects of naturally segregating variants that contribute to local adaptation have been measured in the field. This project investigates the genetic basis of adaption to serpentine soils in Mimulus guttatus. Reciprocal transplant studies show that serpentine and non-serpentine populations of M. guttatus are genetically differentiated in their ability to survive on serpentine soils. We mapped serpentine tolerance by performing a bulk segregant analysis on F2 survivors from a field transplant study and identify a single QTL where individuals that are homozygous for the non-serpentine allele do not survive on serpentine soils. This same QTL controls serpentine tolerance in a second, geographically distant population. A common garden study where the two serpentine populations were grown on each other′s soil finds that one of the populations has significantly lower survival on this “foreign” serpentine soil compared to its home soil. So, while these two populations share a major QTL they either differ at other loci involved in serpentine adaptation or have different causal alleles at this QTL. This raises the possibility that serpentine populations may not be broadly tolerant to serpentine soils but may instead be locally adapted to their particular patch. Nevertheless, despite the myriad chemical and physical challenges that plants face in serpentine habitats, adaptation to these soils in M. guttatus has a simple genetic basis.

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Chromosomal rearrangements represent modular cassettes for local adaptation across different geographic scales

10.1101/2020.12.28.424584 ◽

2020 ◽

Author(s):

Claire Mérot ◽

Emma Berdan ◽

Hugo Cayuela ◽

Haig Djambazian ◽

Anne-Laure Ferchaud ◽

...

Keyword(s):

Gene Flow ◽

Local Adaptation ◽

Environmental Heterogeneity ◽

Salinity Gradient ◽

Chromosomal Rearrangements ◽

Fine Grained ◽

Varying Environments ◽

Genomic Regions ◽

Spatially Varying ◽

Low Coverage

AbstractAcross a species range, spatially-varying environments can drive the evolution of local adaptation. Multiples sources of environmental heterogeneity, at small and large scales, draw complex landscapes of selection which may challenge adaptation, particularly when gene flow is high. Because linkage opposes gene flow but also limits the efficiency of natural selection by contrasting pressures, the key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants like chromosomal inversions are important recombination modifiers that form massive co-segregating genomic blocks linking together alleles at numerous genes. In this study, we investigate the influence of chromosomal rearrangements on genetic variation to ask how their contribution to adaptation with gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient of 10° of latitude, a salinity gradient and across a range of heterogeneous, patchy habitats. We assembled a high-quality genome to analyse 1,446 low-coverage whole-genome sequences, and we found large non-recombining genomic regions, including putative inversions. In contrast to the collinear regions depicting extensive gene flow, inversions and low-recombining regions differentiated populations more strongly, either along an ecogeographic cline or at a fine-grained scale. Those genomic regions were disproportionately involved in associations with environmental factors and adaptive phenotypes, albeit with contrasting patterns between the different recombination modifiers. Altogether, our results highlight the importance of recombination in shaping the selection-migration balance and show that a set of several inversions behave as modular cassettes facilitating adaptation to environmental heterogeneity at local and large scales.

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