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.

Polymorphic chromosomal rearrangements can bind hundreds of genes into single genetic loci with diverse effects. Rearrangements are often associated with local adaptation and speciation and may also be an important component of genetic variation within populations. We genetically and phenotypically characterize a segregating inversion (inv6) in the Iron Mountain (IM) population of Mimulus guttatus (yellow monkeyflower). We initially mapped inv6 as a region of recombination suppression in three F 2 populations resulting from crosses among IM plants. In each case, the F 1 parent was heterozygous for a derived haplotype, homogenous across markers spanning over 5 Mb of chromsome 6. In the three F 2 populations, inv6 reduced male and female fitness components. In addition, inv6 carriers suffered an 30% loss of pollen viability in the field. Despite these costs, inv6 exists at moderate frequency (8%) in the natural population, suggesting counterbalancing fitness benefits that maintain the polymorphism. Across 4 years of monitoring in the field, inv6 had an overall significant positive effect on seed production (lifetime female fitness) of carriers. This benefit was particularly strong in harsh years and may be mediated (in part) by strong positive effects on flower production. These data suggest that opposing fitness effects maintain an intermediate frequency, and as a consequence, inv6 generates inbreeding depression and high genetic variance. We discuss these findings in relation to the theory of inbreeding depression and the maintenance of fitness variation.KEYWORDS inbreeding depression; polymorphism; variation; chromosomal rearrangement; Mimulus guttatus P OLYMORPHIC chromosomal inversions are an important component of genetic variability (Sturtevant and Mather 1938;Hoffmann and Rieseberg 2008). They are associated with species differentiation in both plants (Rieseberg et al. 1999;Fishman et al. 2013;Hermann et al. 2013) and animals (Noor et al. 2001). Within species, inversions often exhibit clines suggestive of adaptation to latitudinal environmental variables (Balanyà et al. 2003;Hoffmann and Rieseberg 2008;Cheng et al. 2012;Fang et al. 2012). Similarly, putatively adaptive trait differences cosegregate with inversions within many species, including Drosophila (Krimbas and Powell 1992), Anopheles (Coluzzi et al. 2002), Rhagoletis (Feder et al. 2003), seaweed flies (Gilburn and Day 1999), monkeyflowers (Lowry and Willis 2010), and sticklebacks (Jones et al. 2012). These patterns support the idea that inversions contribute to local adaptation and speciation because they suppress recombination among multiple genetic variants with context-dependent effects on fitness (Kirkpatrick and Barton 2006).The same evolutionary processes that generate differences among geographical populations can also maintain chromosomal polymorphisms within populations. Environmental fluctuations or frequency dependence could allow the persistence of alternative arrangements containing sets of coadapted alleles, each set being ...

Summary Evolution of genetic (co)variances (the G-matrix) fundamentally influences multitrait divergence. Here, we isolated the contribution of two chromosomal quantitative trait loci (QTLs), a meiotic drive locus and a polymorphic inversion, to the overall G-matrix for a suite of floral, phenological and male fitness traits in a population of Mimulus guttatus. This allowed us to predict the evolution of trait means and genetic (co)variances as a function of allele frequencies, and to evaluate theories about the maintenance of genetic variation in fitness.Individuals generated using a replicated F2 breeding design were grown under common conditions, genotyped and measured for trait values.Significant additive genetic variance existed for all traits, and most genetic covariances were significantly nonzero. Both QTLs contribute to the additive genetic (co)variances of multiple traits. Pleiotropy was not generally consistent, either between QTLs or with the genetic background.Shifts in allele frequencies at either QTL are predicted to result in substantial changes in the G-matrix. Both QTLs contribute substantially to the genetic variation in pollen viability. The Drive QTL, and perhaps also the inversion, demonstrates the contribution of balancing selection to the maintenance of genetic variation in fitness.

These authors contributed equally to the study.Most natural populations display substantial genetic variation in behaviour, morphology, physiology, life history and the susceptibility to disease. A major challenge is to determine the contributions of individual loci to variation in complex traits. Quantitative trait locus (QTL) mapping has identified genomic regions affecting ecologically significant traits of many species. In nearly all cases, however, the importance of these QTLs to population variation remains unclear. In this paper, we apply a novel experimental method to parse the genetic variance of floral traits of the annual plant Mimulus guttatus into contributions of individual QTLs. We first use QTL-mapping to identify nine loci and then conduct a population-based breeding experiment to estimate V Q , the genetic variance attributable to each QTL. We find that three QTLs with moderate effects explain up to one-third of the genetic variance in the natural population. Variation at these loci is probably maintained by some form of balancing selection. Notably, the largest effect QTLs were relatively minor in their contribution to heritability.