Naturally segregating loci exhibit epistasis for fitness

Monnahan, Patrick J.; Kelly, John K.

doi:10.1098/rsbl.2015.0498

Cited by 16 publications

(31 citation statements)

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“…Seed counts are within the range reported in previous field experiments using IM genotypes (Mojica and Kelly ; Mojica et al. ; Monnahan and Kelly ). These estimates are from the full model including both maternal line and line by cross‐interaction as random effects (See Table for all model fits).…”

Section: Resultssupporting

confidence: 85%

“…This high level of ID is caused by an almost threefold decrease in survival to flowering (28.5% vs. 9.85%, δ = 0.65, z = −6.044, P = 1.5 × 10 -9 ), and among survivors, the mean outcrossed seed set was 26.8 seeds versus only 11 seeds for inbred plants. Seed counts are within the range reported in previous field experiments using IM genotypes (Mojica and Kelly 2010;Mojica et al 2012;Monnahan and Kelly 2015). These estimates are from the full model including both maternal line and line by cross-interaction as random effects (See Table S2 for all model fits).…”

Section: Resultssupporting

confidence: 53%

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

Brown

Kelly

2019

Evolution

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Most flowering plants are hermaphroditic and experience strong pressures to evolve self‐pollination (automatic selection and reproductive assurance). Inbreeding depression (ID) can oppose selection for selfing, but it remains unclear if ID is typically strong enough to maintain outcrossing. To measure the full cost of sustained inbreeding on fitness, and its genomic basis, we planted highly homozygous, fully genome‐sequenced inbred lines of yellow monkeyflower (Mimulus guttatus) in the field next to outbred plants from crosses between the same lines. The cost of full homozygosity is severe: 65% for survival and 86% for lifetime seed production. Accounting for the unmeasured effect of lethal and sterile mutations, we estimate that the average fitness of fully inbred genotypes is only 3–4% that of outbred competitors. The genome sequence data provide no indication of simple overdominance, but the number of rare alleles carried by a line, especially within rare allele clusters nonrandomly distributed across the genome, is a significant negative predictor of fitness measurements. These findings are consistent with a deleterious allele model for ID. High variance in rare allele load among lines and the genomic distribution of rare alleles both suggest that migration might be an important source of deleterious alleles to local populations.

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Section: Resultssupporting

confidence: 85%

Section: Resultssupporting

confidence: 53%

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

Brown

Kelly

2019

Evolution

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“…Selection for larger flowers favours alleles that increase allocation towards vegetative growth (size of first few leaf pairs) at the expense of delayed progression to flowering; these plants have much higher reproductive capacity (table 2 of Kelly, ). While these responses reflect the pleiotropic effects of many loci, the trade‐off between developmental speed and size at flowering has also been demonstrated at the scale of individual loci in both laboratory (Scoville et al ., ) and field experiments (Mojica et al ., ; Monnahan & Kelly, ).…”

Section: Discussionmentioning

confidence: 99%

Antagonistic pleiotropy can maintain fitness variation in annual plants

Brown

Kelly

2017

J of Evolutionary Biology

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Antagonistic pleiotropy (AP) is a genetic trade-off between different fitness components. In annual plants, a trade-off between days to flower (DTF) and reproductive capacity often determines how many individuals survive to flower in a short growing season, and also influences the seed set of survivors. We develop a model of viability and fecundity selection informed by many experiments on the yellow monkeyflower, Mimulus guttatus, but applicable to many annual species. A viability/fecundity trade-off maintains stable polymorphism under surprisingly general conditions. We also introduce both spatial heterogeneity and temporal stochasticity in environmental parameters. Neither is necessary for polymorphism, but spatial heterogeneity allows polymorphism while also generating the often observed non-negative correlations in fitness components.

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“…Linked with deleterious recessive alleles, inv6 could represent a "supergene with baggage." Epistasis for fitness-related traits is common in M. guttatus (Kelly 2005;Monnahan and Kelly 2015); if positively interacting alleles are located on the same chromosome, inversions may often be favored because they suppress recombination among them. The environmental dependence of inv6 fitness effects, evident from differences between greenhouse and field and between years at the field site, is also likely important.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2016

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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 ...

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Naturally segregating loci exhibit epistasis for fitness

Cited by 16 publications

References 20 publications

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

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

Antagonistic pleiotropy can maintain fitness variation in annual plants

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

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