What constrains directional selection on complex traits in the wild?

The fact that abundant genetic variation persists within populations despite strong directional selection on complex traits is one of the unresolved conundrums in evolutionary biology. In this dissertation, I employed a multi-faceted approach combining classical and modern genomic methods with field studies to identify the factors that may reduce total selection on a complex trait. I investigated the causes and consequences of phenotypic and genotypic variation in flower size using the wild flower Mimulus guttatus (yellow monkeyflower) as the model system. Flower size in Mimulus guttatus exhibits abundant genetic variation amidst strong directional selection in the wild. To understand directional selection, we must consider the "invisible fraction" (the proportion of individuals that die before expressing the trait), which is typically unmeasured in correlative studies. Chapter 1 demonstrates that viability selection prior to trait expression can change the direction and magnitude of selection. In Chapter 2, I identified fitness trade-offs (viability and fecundity) and varying selection at the spatial and temporal scale as factors that can reduce the effect of directional selection in the wild. Using NILs (Nearly Isogenic Lines), I demonstrate that alleles increasing flower size also increase fecundity but they reduce survivorship. Furthermore, I also detected fluctuating selection by year and on a spatial scale of meters. Finally, correlated selection on corolla width may limit the evolutionary response to directional selection for flower size. I demonstrated in Chapter 3 using a multi-year phenotypic manipulation experiment that corolla width is under indirect selection due to its genetic correlation with other traits that influence fitness in the field (e.g. rate of development, reproductive capacity, vegetative size)

The Genomic Signal of Partial Sweeps in Mimulus guttatus

The molecular signature of selection depends strongly on whether new mutations are immediately favorable and sweep to fixation (hard sweeps) as opposed to when selection acts on segregating variation (soft sweeps). The prediction of reduced sequence variation around selected polymorphisms is much stronger for hard than soft sweeps, particularly when considering quantitative traits where sweeps are likely to be incomplete. Here, we directly investigate the genomic signal of soft sweeps within an artificial selection experiment on Mimulus guttatus. We first develop a statistical method based on Fisher’s angular transformation of allele frequencies to identify selected loci. Application of this method identifies about 400 significant windows, but no fixed differences between phenotypically divergent populations. With two notable exceptions, we find a modest average effect of partial sweeps on the amount of molecular variation. The first exception is a polymorphic inversion on chromosome 6. The increase of the derived haplotype has a broad genomic effect due to recombination suppression coupled with substantial initial haplotype structure within the population. Second, we found significant increases in nucleotide variation around selected loci in the population evolving larger flowers. This suggests that “high” alleles for flower size were initially less frequent than “low” alleles. This result is consistent with prior studies of M. guttatus and illustrates how molecular evolution can depend on the allele frequency spectrum at quantitative trait loci

Spatially and temporally varying selection on intra-population QTL for a life history tradeoff in Mimulus guttatus

This is the peer reviewed version of the following article: MOJICA, J. P., LEE, Y. W., WILLIS, J. H. and KELLY, J. K. (2012), Spatially and temporally varying selection on intrapopulation quantitative trait loci for a life history trade-off in Mimulus guttatus. Molecular Ecology, 21: 3718–3728. doi:10.1111/j.1365-294X.2012.05662.x, which has been published in final form at http://doi.org/10.1111/j.1365-294X.2012.05662.x. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.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