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.
Highlights
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
Lobelia inflata 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; genomewide homozygosity precludes some mechanisms of balancing selection, and microsatellites are, in effect, genotypic lineage markers
Frequency-dependent selection is likely to be less important in maintaining genetic variation in selfing than outcrossing populations because no selection acts on mating system components such as through intraspecific competition for pollinators
Summary
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. Because of several ecological and genetical peculiarities revealed in the recent work on this system, Lobelia inflata provides an exceptional opportunity to isolate effects of a single mechanism, namely to perform a test of the hypothesis that temporally variable selection maintains genetic variation. With a mean of 2.50 alleles per microsatellite locus across 22 loci, the extent of polymorphism is higher than that observed in species with mixed mating systems [31], despite recombination being ineffectual at generating new haplotypes under complete selffertilization In this earlier work, genetic lineage was associated consistently with flower colour [30], and significant quantitative genetic variation was found in the timing of flowering [32]. Genetic variation within populations that occurs exclusively among genetic lineages is expected to erode through both amplified effects of genetic drift and selection [38,39] and requires explanation
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