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

ABSTRACT: BACKGROUND:The initiation of growth cessation and dormancy represent critical life-history trade-offs 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. RESULTS:We 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). A single genomic region containing the PtFT2 gene mediates local adaptation in the timing of bud set and 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 affects the phenotypic variation in bud set that we observe in wild natural populations. CONCLUSIONS:Our results reveal a major effect locus that determines the timing of bud set and that has 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.

SUBMITTER: Wang J

PROVIDER: S-EPMC5985590 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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

Wang Jing J Ding Jihua J Tan Biyue B Robinson Kathryn M KM Michelson Ingrid H IH Johansson Anna A Nystedt Björn B Scofield Douglas G DG Nilsson Ove O Jansson Stefan S Street Nathaniel R NR Ingvarsson Pär K PK

Genome biology 20180604 1

<h4>Background</h4>The initiation of growth cessation and dormancy represent critical life-history trade-offs 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.<h4>Results</h4>We integrate whole genome re-sequencing with environmental and phenotypic data from common ga ...[more]

PMID: 29866176

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Project description:Background and aimsThe ability of plants to track shifting fitness optima is crucial within the context of global change, where increasing environmental extremes may have dramatic consequences for life history, fitness, and ultimately population persistence. However, tracking changing conditions relies on the relationship between genetic and environmental variance, where selection may favour plasticity, the evolution of genetic differences, or both depending on the spatial and temporal scale of environmental heterogeneity.MethodsOver three years, we compared the genetic and environmental components of phenological and life-history variation in a common environment for the spring perennial Geum triflorum. Populations were sourced from alvar habitats that exhibit extreme but predictable annual flood-desiccation cycles and prairie habitats that exhibit similar but less predictable variation in water availability.Key resultsHeritability was generally higher for early life-history (emergence probability) relative to later life-history traits (total seed mass), indicating that traits associated with establishment are under stronger genetic control relative to later life-history fitness expressions, where plasticity may play a larger role. This pattern was particularly notable in seeds sourced from environmentally extreme but predictable alvar habitats relative to less predictable prairie environments. Fitness landscapes based on seed source origin, largely characterized by varying water availability and flower production, described selection as the degree of maladaptation of seed source environment relative to the prairie common garden environment. Plants from alvar populations were consistently closer to the fitness optimum across all years. Annually, the breadth of the fitness optimum expanded primarily along a moisture gradient, with inclusion of more populations onto the expanding optimum.ConclusionsThese results highlight the importance of temporally and spatially varying selection in life-history evolution, indicating plasticity may become a primary mechanism needed to track fitness for later life-history events within perennial systems.

Project description:The role of chromosomal inversions in adaptation and speciation is controversial. Historically, inversions were thought to contribute to these processes either by directly causing hybrid sterility or by facilitating the maintenance of co-adapted gene complexes. Because inversions suppress recombination when heterozygous, a recently proposed local adaptation mechanism predicts that they will spread if they capture alleles at multiple loci involved in divergent adaptation to contrasting environments. Many empirical studies have found inversion polymorphisms linked to putatively adaptive phenotypes or distributed along environmental clines. However, direct involvement of an inversion in local adaptation and consequent ecological reproductive isolation has not to our knowledge been demonstrated in nature. In this study, we discovered that a chromosomal inversion polymorphism is geographically widespread, and we test the extent to which it contributes to adaptation and reproductive isolation under natural field conditions. Replicated crosses between the prezygotically reproductively isolated annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus, revealed that alternative chromosomal inversion arrangements are associated with life-history divergence over thousands of kilometers across North America. The inversion polymorphism affected adaptive flowering time divergence and other morphological traits in all replicated crosses between four pairs of annual and perennial populations. To determine if the inversion contributes to adaptation and reproductive isolation in natural populations, we conducted a novel reciprocal transplant experiment involving outbred lines, where alternative arrangements of the inversion were reciprocally introgressed into the genetic backgrounds of each ecotype. Our results demonstrate for the first time in nature the contribution of an inversion to adaptation, an annual/perennial life-history shift, and multiple reproductive isolating barriers. These results are consistent with the local adaptation mechanism being responsible for the distribution of the two inversion arrangements across the geographic range of M. guttatus and that locally adaptive inversion effects contribute directly to reproductive isolation. Such a mechanism may be partially responsible for the observation that closely related species often differ by multiple chromosomal rearrangements.

Dataset Information

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

Publications

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

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