Keeping It Local: Evidence for Positive Selection in Swedish Arabidopsis thaliana

Huber, Christian D.; Nordborg, Magnus; Hermisson, Joachim; Hellmann, Ines

doi:10.1093/molbev/msu247

Cited by 75 publications

(85 citation statements)

References 48 publications

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“…Studies of A. thaliana in Sweden [47] suggest that selection was stronger in the north than the south. This conclusion was based on simulation results; in the absence of a defined statistical model, no actual inference regarding the strength of selection could be made.…”

Section: Detecting the Genetic Basis Of Adaptations In Selfersmentioning

confidence: 99%

The Evolutionary Interplay between Adaptation and Self-Fertilization

2017

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Genome-wide surveys of nucleotide polymorphisms, obtained from next-generation sequencing, have uncovered numerous examples of adaptation in self-fertilizing organisms, especially regarding changes to climate, geography, and reproductive systems. Yet existing models for inferring attributes of adaptive mutations often assume idealized outcrossing populations, which risks mischaracterizing properties of these variants. Recent theoretical work is emphasizing how various aspects of self-fertilization affects adaptation, yet empirical data on these properties are lacking. We review theoretical and empirical studies demonstrating how self-fertilization alters the process of adaptation, illustrated using examples from current sequencing projects. We propose ideas for how future research can more accurately quantify aspects of adaptation in self-fertilizers, including incorporating the effects of standing variation, demographic history, and polygenic adaptation.

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Section: Detecting the Genetic Basis Of Adaptations In Selfersmentioning

confidence: 99%

The Evolutionary Interplay between Adaptation and Self-Fertilization

2017

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“…However, widespread local adaptation to climate in Arabidopsis is observed (Fournier-Level et al 2011;Hancock et al 2011;Ågren et al 2013), which is expected to leave a weaker signature on the genome at the species scale (Slotte 2014). However, the power to detect local selection can increase once demography and population structure are accounted for (Huber et al 2014).Finally, both outcrossing and selfing domesticated plant and crop species can also be used to demonstrate recent adaptation. Ronfort and Glémin (2013) showed how adaptive traits obtained from quantitative trait loci tended to be dominant in outcrossers and recessive in selfers, in line with "Haldane's sieve" (where dominant mutants are more likely to fix than recessive types in outcrossers).…”

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Limits to Adaptation in Partially Selfing Species

Hartfield

Glémin

2016

Genetics

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In outcrossing populations, "Haldane's sieve" states that recessive beneficial alleles are less likely to fix than dominant ones, because they are less exposed to selection when rare. In contrast, selfing organisms are not subject to Haldane's sieve and are more likely to fix recessive types than outcrossers, as selfing rapidly creates homozygotes, increasing overall selection acting on mutations. However, longer homozygous tracts in selfers also reduce the ability of recombination to create new genotypes. It is unclear how these two effects influence overall adaptation rates in partially selfing organisms. Here, we calculate the fixation probability of beneficial alleles if there is an existing selective sweep in the population. We consider both the potential loss of the second beneficial mutation if it has a weaker advantage than the first one, and the possible replacement of the initial allele if the second mutant is fitter. Overall, loss of weaker adaptive alleles during a first selective sweep has a larger impact on preventing fixation of both mutations in highly selfing organisms. Furthermore, the presence of linked mutations has two opposing effects on Haldane's sieve. First, recessive mutants are disproportionally likely to be lost in outcrossers, so it is likelier that dominant mutations will fix. Second, with elevated rates of adaptive mutation, selective interference annuls the advantage in selfing organisms of not suffering from Haldane's sieve; outcrossing organisms are more able to fix weak beneficial mutations of any dominance value. Overall, weakened recombination effects can greatly limit adaptation in selfing organisms.KEYWORDS adaptation; selection interference; dominance; self-fertilization; recombination S ELF-FERTILIZATION-reproduction where both gametes arise from the same parent-frequently evolves from outcrossing species in nature. Self-fertilization is widespread in angiosperms (Igic and Kohn 2006), some groups of animals (Jarne and Auld 2006), and fungi (Billiard et al. 2011;Gioti et al. 2012). It confers an initial benefit to an individual's fecundity, including up to a 50% transmission advantage (Fisher 1941) and reproductive assurance under mate limitation (Baker 1955(Baker , 1967Pannell et al. 2015). Both factors should allow selfing organisms to rapidly spread upon invasion of new habitats, unless countered by high levels of inbreeding depression (Lande and Schemske 1985). However, empirical studies usually find that selfing lineages are a "dead end," since back transitions to outcrossing are rare, and high extinction rates have been inferred from comparative studies of related selfing-outcrossing taxa (Igic et al. 2008;Goldberg et al. 2010;Wright and Barrett 2010;Wright et al. 2013).Self-fertilization has therefore been posited to be detrimental in the long term. For an organism with selfing rate s, the population has an inbreeding rate F ¼ s=ð2 2 sÞ; equivalent to Wright's (1951) F IS statistic. The effective population size N e is reduced by a factor of at least 1=ð1 þ...

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“…A number of genes have been identified as candidates for local adaptation in Arabidopsis, including, for example, variants that affect flowering (Lempe et al, 2005;Stinchcombe et al, 2005;Balasubramanian et al, 2006;Shindo et al, 2006;Hopkins et al, 2008;Li et al, 2014), seed dormancy (Kronholm et al, 2012), drought-induced Pro accumulation (Kesari et al, 2012), sodium accumulation associated with distance to the coast (Baxter et al, 2010), and molybdenum accumulation associated with soil molybdenum (Poormohammad Kiana et al, 2012). Studies in silico and common garden field experiments have also found potential evidence for local adaptation on a genome-wide scale in Arabidopsis (Fournier-Level et al, 2011;Hancock et al, 2011;Huber et al, 2014;Lasky et al, 2014). Final proof of the adaptive role of a given allelic variant will require testing the fitness effects of alternative alleles of the gene in the same genetic background in the field over multiple growing seasons in the contrasting environments in which the alleles are hypothesized to be adaptive.…”

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Salinity Is an Agent of Divergent Selection Driving Local Adaptation of Arabidopsis to Coastal Habitats

et al. 2015

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Understanding the molecular mechanism of adaptive evolution in plants provides insights into the selective forces driving adaptation and the genetic basis of adaptive traits with agricultural value. The genomic resources available for Arabidopsis (Arabidopsis thaliana) make it well suited to the rapid molecular dissection of adaptive processes. Although numerous potentially adaptive loci have been identified in Arabidopsis, the consequences of divergent selection and migration (both important aspects of the process of local adaptation) for Arabidopsis are not well understood. Here, we use a multiyear field-based reciprocal transplant experiment to detect local populations of Arabidopsis composed of multiple small stands of plants (demes) that are locally adapted to the coast and adjacent inland habitats in northeastern Spain. We identify fitness tradeoffs between plants from these different habitats when grown together in inland and coastal common gardens and also, under controlled conditions in soil excavated from coastal and inland sites. Plants from the coastal habitat also outperform those from inland when grown under high salinity, indicating local adaptation to soil salinity. Sodium can be toxic to plants, and we find its concentration to be elevated in soil and plants sampled at the coast. We conclude that the local adaptation that we observe between adjacent coastal and inland populations is caused by ongoing divergent selection driven by the differential salinity between coastal and inland soils.

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Keeping It Local: Evidence for Positive Selection in Swedish Arabidopsis thaliana

Cited by 75 publications

References 48 publications

The Evolutionary Interplay between Adaptation and Self-Fertilization

The Evolutionary Interplay between Adaptation and Self-Fertilization

Limits to Adaptation in Partially Selfing Species

Salinity Is an Agent of Divergent Selection Driving Local Adaptation of Arabidopsis to Coastal Habitats

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