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Genotype-environment interaction and the maintenance of genetic variation: an empirical study of Lobelia inflata (Campanulaceae).

ABSTRACT: High levels of genetic variation are often observed in natural populations, suggesting the action of processes such as frequency-dependent selection, heterozygote advantage and variable selection. However, the maintenance of genetic variation in fitness-related traits remains incompletely explained. The extent of genetic variation in obligately self-fertilizing populations of Lobelia inflata (Campanulaceae L.) strongly implies balancing selection. Lobelia inflata thus offers an exceptional opportunity for an empirical test of genotype-environment interaction (G × E) as a variance-maintaining mechanism under fluctuating selection: L. inflata is monocarpic and reproduces only by seed, facilitating assessment of lifetime fitness; genome-wide homozygosity precludes some mechanisms of balancing selection, and microsatellites are, in effect, genotypic lineage markers. Here, we find support for the temporal G × E hypothesis using a manipulated space-for-time approach across four environments: a field environment, an outdoor experimental plot and two differing growth-chamber environments. High genetic variance was confirmed: 83 field-collected individuals consisted of 45 distinct microsatellite lineages with, on average, 4.5 alleles per locus. Rank-order fitness, measured as lifetime fruit production in 16 replicated multilocus genotypes, changed significantly across environments. Phenotypic differences among microsatellite lineages were detected. Results thus support the G × E hypothesis in principle. However, the evaluation of the effect size of this mechanism and fitness effects of life-history traits will require a long-term study of fluctuating selection on labelled genotypes in the field.

SUBMITTER: Cote K

PROVIDER: S-EPMC7137973 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Genotype-environment interaction and the maintenance of genetic variation: an empirical study of Lobelia inflata (Campanulaceae).

Côté Kristen K Simons Andrew M AM

Royal Society open science 20200318 3

High levels of genetic variation are often observed in natural populations, suggesting the action of processes such as frequency-dependent selection, heterozygote advantage and variable selection. However, the maintenance of genetic variation in fitness-related traits remains incompletely explained. The extent of genetic variation in obligately self-fertilizing populations of Lobelia inflata (Campanulaceae L.) strongly implies balancing selection. Lobelia inflata thus offers an exc ...[more]

PMID: 32269800

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Project description:Abstract Allopatric gene pools can evolve in different directions through adaptive and nonadaptive processes and are therefore a source of intraspecific diversity. The connection of these previously isolated gene pools through human intervention can lead to intraspecific diversity loss, through extirpation of native populations or hybridization. However, the mechanisms leading to these situations are not always explicitly documented and are thus rarely used to manage intraspecific diversity. In particular, genotype‐by‐environment (GxE) interactions can drive postzygotic reproductive isolation mechanisms that may result in a mosaic of diversity patterns, depending on the local environment. We test this hypothesis using a salmonid species (Salmo trutta) in the Mediterranean (MED) area, where intensive stocking from non‐native Atlantic (ATL) origins has led to various outcomes of hybridization with the native MED lineage, going from MED resilience to total extirpation via full hybridization. We investigate patterns of offspring survival at egg stage in natural environments, based on parental genotypes in interaction with river temperature, to detect potential GxE interactions. Our results show a strong influence of maternal GxE interaction on embryonic survival, mediated by maternal effect through egg size, and a weak influence of paternal GxE interaction. In particular, when egg size is large and temperature is cold, the survival rate of offspring originating from MED females is three times higher than that of ATL females’ offspring. Because river temperatures show contrast at small scale, this cold adaptation for MED females’ offspring constitutes a potent postzygotic mechanism to explain small‐scale spatial heterogeneity in diversity observed in MED areas where ATL fish have been stocked. It also indicates that management efforts could be specifically targeted at the environments that actively favor native intraspecific diversity through eco‐evolutionary processes such as postzygotic selection.

Project description:Natural populations exhibit substantial variation in quantitative traits. A quantitative trait is typically defined by its mean and variance, and to date most genetic mapping studies focus on loci altering trait means but not (co)variances. For single traits, the control of trait variance across genetic backgrounds is referred to as genetic canalization. With multiple traits, the genetic covariance among different traits in the same environment indicates the magnitude of potential genetic constraint, while genotype-by-environment interaction (GxE) concerns the same trait across different environments. While some have suggested that these three attributes of quantitative traits are different views of similar concepts, it is not yet clear, however, whether they have the same underlying genetic mechanism. Here, we detect quantitative trait loci (QTL) influencing the (co)variance of phenological traits in six distinct environments in Boechera stricta, a close relative of Arabidopsis. We identified nFT as the QTL altering the magnitude of phenological trait canalization, genetic constraint, and GxE. Both the magnitude and direction of nFT's canalization effects depend on the environment, and to our knowledge, this reversibility of canalization across environments has not been reported previously. nFT's effects on trait covariance structure (genetic constraint and GxE) likely result from the variable and reversible canalization effects across different traits and environments, which can be explained by the interaction among nFT, genomic backgrounds, and environmental stimuli. This view is supported by experiments demonstrating significant nFT by genomic background epistatic interactions affecting phenological traits and expression of the candidate gene, FT. In contrast to the well-known canalization gene Hsp90, the case of nFT may exemplify an alternative mechanism: Our results suggest that (at least in traits with major signal integrators such as flowering time) genetic canalization, genetic constraint, and GxE may have related genetic mechanisms resulting from interactions among major QTL, genomic backgrounds, and environments.

Dataset Information

Genotype-environment interaction and the maintenance of genetic variation: an empirical study of Lobelia inflata (Campanulaceae).

Publications

Genotype-environment interaction and the maintenance of genetic variation: an empirical study of <i>Lobelia inflata</i> (Campanulaceae).

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