A segregating inversion generates fitness variation in a yellow monkeyflower (Mimulus guttatus) population

Abstract

Polymorphic chromosomal rearrangements, which can bind together hundreds of genes into single genetic loci with diverse effects, are increasingly associated with local adaptation and speciation. They may also be an important component of genetic variation within populations. We genetically and phenotypically characterized a novel segregating inversion (inv6) in the Iron Mountain (IM) population of Mimulus guttatus (yellow monkeyflower). We first identified a region of recombination suppression in three F2 mapping populations resulting from crosses among IM plants; in each case, the F1 hybrid parent was heterozygous for a homogenous derived haplotype (inv6) across markers spanning over 4.2 Mb of Linkage Group 6. Genotype-phenotype associations in the three F2 populations demonstrated negative inv6 effects on male and female fitness components. In addition, inv6 carriers suffered a ~30% loss of pollen viability in the field. Despite these costs, inv6 exists at moderate and apparently stable frequency (~7%) in the natural population, suggesting counter-balancing fitness benefits that maintain the polymorphism. Across four years of monitoring in the field, inv6 had an overall significant positive effect on the seed production (lifetime female fitness) of carriers. This benefit was particularly strong in harsh years and may be mediated (in part) by strong positive inv6 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 the context of theory about the genetic basis of inbreeding depression and the role for chromosomal rearrangements in population divergence with gene flow.