A Segregating Inversion Generates Fitness Variation in Yellow Monkeyflower (Mimulus guttatus)

Abstract

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 F2 populations resulting from crosses among IM plants. In each case, the F1 parent was heterozygous for a derived haplotype, homogenous across markers spanning over 5 Mb of chromsome 6. In the three F2 populations, inv6 reduced male and female fitness components. In addition,i nv6 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: Mimulus guttatus; chromosomal rearrangement; inbreeding depression; polymorphism; variation.

Figure 1

Comparative linkage mapping of the upper end of chromosome 6 in Iron Mountain M. guttatus hybrids. In a freely recombining cross (left: IM179 × IM767 F₂; n = 86), this region spans ∼40 cM, whereas recombination is highly suppressed in all three F₂ mapping populations segregating for the inv6 haplotype (right; c3 map shown). Marker names are to the right, and centimorgans are to the left of bar. Shared markers are highlighted in italic red type.

Figure 2

Effect of inv6 genotype on pollen viability (mean ± 1 SE) and supplemented seedset within each of the F₂ mapping populations.

Figure 3

Delineation of inv6 haplotype block in M. guttatus individuals derived from wild IM plants by one generation of outbreeding (n = 96). Each cell represents the genotype of an individual genotyped at 17 markers across chromosome 6. Genotypes carrying at least one inv6-associated allele are shown in blue (for the 13 inv6-spanning markers) and non-inv6 genotypes are shown in white. Black indicates missing data, and three non-inv6 genotypes (likely genotyping errors or double crossovers) within the inv6 block are shown in green.

Figure 4

The average pairwise sequence divergence (π / bp) is reported across chromosome 6 for three distinct contrasts: blue indicates inv6/inv6, orange indicates inv6/standard, and gray indicates standard/standard. Points are based on a 1-Mb moving average (each is calculated by averaging π/bp estimates from contiguous 50-kb windows). The absence of data from 9 to 11 Mb corresponds to the putative centromere.

Figure 5

Effect of inv6 genotype on pollen viability (mean ± 1 SE) of wild Iron Mountain M. guttatus plants (2007; n = 177). Individuals were assigned to genotypic categories (inv6, no inv6) based on their alleles at the diagnostic markers e423 and e723. An inv6 assignment indicates a heterozygous individual, as the two inv6 homozygotes in the dataset were excluded.

Figure 6

Effects of inv6 genotype on female fitness components (mean ± 1 SE) of wild Iron Mountain M. guttatus plants (n = 1248). Individuals were assigned to genotypic categories (inv6, no inv6) based on their alleles at the diagnostic marker e423. There were only a few inv6 homozygotes in the entire 4-year dataset (not enough to include in the statistical analyses), so an inv6 assignment indicates a heterozygous individual. We show raw means and standard errors here, but the statistical tests in the text were done in a GLM framework (Poisson, log link for fruits and flowers) or with log-transformed values (normal, identity link for seeds).