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 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 ...

Population structure and local selection yield high genomic variation in Mimulus guttatus

“…; Lee et al . ) and also between IM and other populations (Lowry & Willis ; Holeski et al . ; Twyford & Friedman ).…”

What can genome‐wide association studies tell us about the evolutionary forces maintaining genetic variation for quantitative traits?

“…Second, the signature of long‐term balancing selection on linked neutral polymorphism can be difficult to detect, because recombination and gene conversion can weaken the association between neutral variants and the site under balancing selection (Andolfatto & Nordborg, ). The effects of recombination and gene conversion weakening the signature of balancing selection is one reason why the clearest cases of balanced polymorphisms arise when recombination is suppressed in a genomic region, such as at the self‐incompatability locus or on sex chromosomes (Charlesworth, ) or in inversions (Lee et al ., ). However, low rates of recombination in highly selfing plants mean that balancing selection may in fact play a significant role in structuring patterns of shared and unique variation across the genome of selfing species.…”

Severe inbreeding depression is predicted by the “rare allele load” inMimulus guttatus*

“…), and/or from loci with partially dominant alleles maintained at intermediate frequency by some form of balancing selection (Lee et al. ). Under the “overdominance hypothesis,” fitness may positively correlate with genome‐wide heterozygosity, although this prediction depends on how many loci exhibit heterozygote advantage.…”

“…ID may result from rare (partially) recessive deleterious alleles at low frequency in the population (the "dominance hypothesis," Charlesworth and Willis 2009), in which case fitness of inbred individuals should decline with the load of deleterious alleles. ID could also result from increased homozygosity at overdominant loci (Li et al 2001b;Luo et al 2001), and/or from loci with partially dominant alleles maintained at intermediate frequency by some form of balancing selection (Lee et al 2016). Under the "overdominance hypothesis," fitness may positively correlate with genome-wide heterozygosity, although this prediction depends on how many loci exhibit heterozygote advantage.…”