Partial Selfing Can Reduce Genetic Loads While Maintaining Diversity During Experimental Evolution

Abstract

Partial selfing, whereby self- and cross- fertilization occur in populations at intermediate frequencies, is generally thought to be evolutionarily unstable. Yet, it is found in natural populations. This could be explained if populations with partial selfing are able to reduce genetic loads and the possibility for inbreeding depression while keeping genetic diversity that may be important for future adaptation. To address this hypothesis, we compare the experimental evolution of Caenorhabditis elegans populations under partial selfing, exclusive selfing or predominant outcrossing, while they adapt to osmotically challenging conditions. We find that the ancestral genetic load, as measured by the risk of extinction upon inbreeding by selfing, is maintained as long as outcrossing is the main reproductive mode, but becomes reduced otherwise. Analysis of genome-wide single-nucleotide polymorphisms (SNPs) during experimental evolution and among the inbred lines that survived enforced inbreeding indicates that populations with predominant outcrossing or partial selfing maintained more genetic diversity than expected with neutrality or purifying selection. We discuss the conditions under which this could be explained by the presence of recessive deleterious alleles and/or overdominant loci. Taken together, our observations suggest that populations evolving under partial selfing can gain some of the benefits of eliminating unlinked deleterious recessive alleles and also the benefits of maintaining genetic diversity at partially dominant or overdominant loci that become associated due to variance of inbreeding levels.

Keywords: C. elegans; Disequilibrium; Evolve & Resequence; Overdominance; Self-fertilization.

Figure 1

Experimental design and origin of populations used in this work. The genetically diverse androdioecious population A6140 (containing males and hermaphrodites) was used as the ancestral population for experimental evolution under increasing NaCl concentrations for 50 generations, reported as the ”Gradual regime” in Theologidis et al. (2014). This ancestral population was subjected to introgression of sex determination mutant alleles to generate populations with different proportions of males, hermaphrodites and females, which evolved under different contributions of selfing and outcrossing (M00 - monoecious; A00 - androdioecious; and, T00 - trioecious populations). Population A00 was derived by sampling of A6140 without any genetic manipulation. Experimental evolution was done with several replicates and, at the end of it, inbred lines were derived by selfing from the resulting populations as had been for the ancestral A6140. Population nomenclature follows Theologidis et al. (2014) and Noble et al. (2017) and font colors are those used throughout this paper.

Figure 2

Genetic diversity comparison between the ancestral population and populations evolved under the three different reproductive modes. Legend colors apply equally to all panels. (a, b), Higher inbreeding coefficients ($F_{is}$) are seen in monoecious and androdioecious populations than in the ancestral or trioecious populations, while SNP allele diversity ($H_e$) is almost halved only in monoecious populations. (c), Linkage disequilibrium within chromosomes, shown as the expected decay in $r^2$ with genetic distance (cM). Data were fitted with $E\left[r^2\right]=1/\left(1+xc\right)$, with respect to x and lines represent fitted values for ancestral and derived populations with shaded areas showing 95% confidence intervals (see Materials and Methods). Lines from the ancestral and trioecious populations overlap. Y axis is shown in a logarithmic scale. (d), Expected identity disequilibrium ($g2$) is shown with exception of monoecious populations that have no heterozygotes. Means and one SD among replicate populations (dots) are shown (see Materials and Methods). Asterisks show significant differences between experimentally evolved populations and the ancestral population for p-values < 0.05 (*) or p-values < 0.005 (**).

Figure 3

(a), Kaplan-Meier estimates of survival rates (1 minus risk of lineage extinction) are shown for the laboratory adapted ancestral population (gray line) and the experimentally evolved populations, with shaded areas representing 95% confidence intervals. Hermaphrodites were selfed for 13-16 generations and the proportion of surviving lineages recorded. Simulations of the extent to which lineage extinction in the trioecious population is due to picking segregating females or fog-2(q71) heterozygous hermaphrodites is shown in Supplementary Figure S2. Significant differences in the risk of extinction to evolved monoecious populations, which represent the condition of no inbreeding depression, or ancestral population are shown as lines: * p-value < 0.05, ** p-value < 0.005. In (b), the tendency for populations with higher inbreeding after 50 generations of experimental evolution to have a lower risk of extinction is revealed by a negative correlation (p-value < 0.005) between inbreeding coefficients and hazard ratios, in which the monoecious populations were used as reference (shown in blue). Coefficient of determination is shown.

Figure 4

Reproductive output and line derivation. Mean fertility and one SEM among replicate populations are shown for populations from each reproductive mode, in 305 mM NaCl (a) and 25 mM NaCl (b). In each group, from left to right, results are shown for the experimental populations and the inbred lines derived from them. No significant differences between populations and inbred lines were found.

Figure 5

Diversity, shown as the average SNP allele diversity ($H_e$, panel a) or mean effective haplotype number ($h_e$, panel b) is plotted for each replicate population (A6140, GT150, GT250, GA150, GA250, GA450, GM150 and GM350 - dark-colored bars) and among the inbred lines derived from them (A6140L, GT150L, GT250L, GA150L, GA250L, GA450L, GM150L and GM350L - light-colored bars). Adjacent to the inbred lines (in white), the expected diversity with no selection during enforced inbreeding obtained with 1,000 numerical simulations is shown with error bars giving 95% credible intervals (see Materials and Methods).