Epistasis in natural populations of a predominantly selfing plant

Abstract

Populations of predominantly selfing plant species often show spatial genetic structure but little is known whether epistatic gene interactions are spatially structured. To detect a possible epistatic effect and a spatial scale at which it operates, we created artificial crosses between plants spanning a range of fixed distances from 1 to 400 m in three populations of wild barley. The self-pollinated and crossed progeny (F 1 ) and two generations of segregated progeny (F 2 and F 3 ) were tested in experimentally simulated population environments for relative performance (RP). The measured fitness traits included number of seeds, total seed weight and seed germination. For any of these traits, there was no association between RP of F 1 , F 2 and F 3 plants and either pairwise kinship coefficients or crossing distance. In contrast, in all three populations, we found lower seed viability of outcrossed as compared with self-pollinated genotypes in the first generation of segregation. However, in the F 3 generation this outbreeding effect disappeared in the two populations and greatly decreased in the third population. For seed production, heterosis in F 1 and outbreeding depression in F 2 were observed only in the population with unusually high number of heterozygotes. Our findings support the view that in selfing species a spatial mosaic of various locally abundant genotypes represents not randomly fixed combinations of alleles but the co-adapted gene complexes that were sieved by selection, while heterozygotes are characteristic for the transient phase of this process, when segregation and purging of maladaptive genotypes have not yet occurred.

Adaptive genetic differentiation in a predominantly self‐pollinating species analyzed by transplanting into natural environment, crossbreeding and QST–FST test

“…6). Similar effects of pollen flow were detected in wild barley at the fine within‐population scale (Volis et al. , 2011).…”

Effects of partial selfing on the equilibrium genetic variance, mutation load, and inbreeding depression under stabilizing selection

“…This explains why outbreeding depression is not observed under complete (or nearly complete) selfing in Figure 9, as all outcrossed individuals are F1 hybrids between selfing lineages. Outbreeding depression between lineages collected from the same geographical location has been observed in highly selfing plants (Parker 1992;Volis et al 2011) and Caenorhabditis nematodes (Dolgin et al 2007;Gimond et al 2013). In all cases, estimated selfing rates are higher than those leading to δ < 0 in our simulations, however, and outbreeding depression was observed in F1 offspring of crosses between inbred lines of nematodes.…”

Population Structure Has Limited Fitness Consequences in the Highly Selfing PlantLeavenworthia uniflora(Brassicaceae)

“…Locally high levels of linkage disequilibrium may arise between genes whenever they are in close physical linkage or when natural selection favors certain multilocus gene combinations (Bonnin et al 1996;Volis et al 2011). In this study, we observed significant linkage disequilibrium between more than half of the polymorphic genes in the TN-C population.…”

“…The null model is additive inheritance, where the midparent (MP) mean predicts the F 1 mean (Mather and Jinks 1982;Fenster and Galloway 2000;Rhode and Cruzan 2005;Busch 2006). When F 1 fitness exceeds the MP value, heterosis caused by the masking of different deleterious recessive mutations in each population is likely, although additive-by-additive epistasis is also possible (Fenster and Galloway 2000;Johansen-Morris and Latta 2006;Volis et al 2011). In crosses between deeply divergent selfing populations, underdominance may be expected, because a dearth of heterozygosity will permit these mutations to contribute to genetic divergence as they fix by genetic drift within plant populations (Skrede et al 2008).…”

“…Selfing should be a powerful mechanism facilitating the selection of epistatic interactions, as it restricts the scale of gene flow to a small geographic scale and simultaneously reduces the breakup of epistatic interactions by recombination (Wade and Goodnight 2006;Volis et al 2011). In highly inbred or selfing populations, negative epistatic interactions have been revealed by a reduction in fitness in outcrossed, as opposed to selfed, lineages based on crosses between plants over very small spatial scales (Quilichini et al 2001;Volis et al 2011), between ecotypes (Johansen-Morris and Latta 2006), and also between populations at distant spatial scales (Skrede et al 2008). These results imply that local adaptation effectively generates coadapted gene complexes in highly selfing plant populations and may contribute to their eventual reproductive isolation.…”