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

Abstract

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.

Why do Inbreeding Depression and Load Resist Both Purging and Fixation?

“…Genomic tools have exposed loci with large inbreeding effects (Kardos et al 2016) suggesting PODs. Brown and Kelly (2020) found these results hard to reconcile with current theoretical studies but noted they were compatible with associative overdominance generated by closely linked deleterious recessive alleles in linkage disequilibrium. In fact, recessive semi-lethal mutations linked in strong repulsion occur in wild populations of C. elegans (Seidel et al 2008).…”

Waiting for love but not forever: modelling the evolution of waiting time to selfing in hermaphrodites

“…A positive effect of the level of inbreeding depression on waiting times, where large inbreeding depression is correlated with long waiting times, has been shown in Physa acuta (Jarne et al 2000; Weeks et al 2001; Escobar et al 2009; Noël et al 2016; Noël et al 2018), and Eulimnadia texana (Weeks et al 1999; Weeks et al 2001). A recent study in plants (Brown and Kelly 2020) has shown that inbreeding depression caused by rare mutations can be severe enough to meet the criteria shown in Figure K in the supporting information. It should, however, be mentioned that other studies in the same systems did not find links between inbreeding depression and waiting time (Weeks et al 1999; Escobar et al 2007).…”

Review: evolutionary drivers of agricultural adaptation in Lolium spp.

“…has been inferred indirectly by means of linkage disequilibrium, because this estimate is dependent on the effective population size and the map distance between loci 15 . The gametophytic self‐incompatibility breeding system reduces the accumulation of deleterious alleles that may cause inbreeding depression, 16 and is a key trait in the recovery of populations (i.e. evolutionary rescue) following population bottlenecks.…”