Spatially and temporally varying selection on intrapopulation quantitative trait loci for a life history trade‐off in Mimulus guttatus

Abstract

Why do populations remain genetically variable despite strong continuous natural selection? Mutation reconstitutes variation eliminated by selection and genetic drift, but theoretical and experimental studies each suggest that mutation-selection balance insufficient to explain extant genetic variation in most complex traits. The alternative hypothesis of balancing selection, wherein selection maintains genetic variation, is an aggregate of multiple mechanisms (spatial and temporal heterogeneity in selection, frequency-dependent selection, antagonistic pleiotropy, etc.). Most of these mechanisms have been demonstrated for Mendelian traits, but there is little comparable data for loci affecting quantitative characters. Here, we report a three-year field study of selection on intra-population Quantitative Trait Loci (QTL) of flower size, a highly polygenic trait of Mimulus guttatus. The QTL exhibit antagonistic pleiotropy: alleles that increase flower size reduce viability but increase fecundity. The magnitude and direction of selection fluctuates yearly and on a spatial scale of meters. This study provides direct evidence of balancing selection mechanisms on QTL of an ecologically relevant trait.

Naturally segregating loci exhibit epistasis for fitness

“…Genetic interactions with the environment are important because even if selection acts consistently on a trait across time and space, change in allele frequency may not be consistent if marginal and/or epistatic genetic effects depend on environment. Although the genetic effects on viability did not differ significantly across years in this study, spatial and temporal variations in selection have been documented for other polymorphisms in this species and locale [3].…”

“…Additionally, the effect of a locus (gene) often depends on the environment experienced by the organism [2]. Field studies, using genetic lines containing known alleles, have shed light on the evolutionary significance of loci identified in controlled settings [3,4]. However, the common observation in mapping studies that genes interact with one another (i.e.…”

Resource allocation and post-reproductive degeneration in the freshwater cnidarian Hydra oligactis (Pallas, 1766)

“…These differences could represent alternative life history tactics within the population (e.g., local adaptations to differences in microhabitat) or a consequence of temporally varying selection on life history traits (e.g., Mojica et al, 2012). They could also be the consequence of a high rate of influx of genetically distinct individuals into the lake from which our founder polyps were derived.…”

Transatlantic invasion routes and adaptive potential in North American populations of the invasive glossy buckthorn,Frangula alnus

“…The preservation of diversity and allelic richness for ecologically relevant genes, even in the presence of limited neutral genetic diversity (e.g. Dlugosch and Parker, 2008), may result from an interplay between the rich genetic architecture underlying complex adaptive traits and balancing selection for adaptive diversity (Mojica et al, 2012;Des Marais et al, 2013). More specifically, a rich genetic architecture can involve multiple alternative genetic and phenotypic effects, including dominance, epistasis, pleiotropy and genotype  environment interactions.…”

“…More specifically, a rich genetic architecture can involve multiple alternative genetic and phenotypic effects, including dominance, epistasis, pleiotropy and genotype  environment interactions. These processes can in turn balance genetic diversity underlying quantitative fitness traits, thereby counteracting loss of the genetic diversity of genes governing adaptive phenotypic diversity during invasions of natural areas (Mojica et al, 2012;Alonso-Blanco and Méndez-Vigo, 2014;El-Soda et al, 2014).…”