Not just mutations: Inbreeding depression persists without genetic variation

Inbreeding depression (ID), the decline in fitness upon inbreeding, is thought to result from a decrease in genetic heterozygosity enhancing phenotypic effects of recessive deleterious mutations. However, emerging evidence suggests that mutations may not explain ID completely. In this study, we test whether ID can emerge even in contexts where genetic heterozygosity does not vary. To that end, highly inbred lines (F=0.99999997) of the freshwater snail Physa acuta were used to produce individuals with varying levels of parental relatedness (self-fertilization, sibling crosses, and cousin crosses), though with identical genomic heterozygosity. Several fitness traits declined significantly with increasing parental relatedness, a pattern characteristic of ID, and quantitatively representing a non-negligible fraction of the ID usually observed in natural, genetically diverse populations of Physa acuta. Individual-based simulations showed that mutation rates compatible with values of ID found in natural populations are way too low to generate as much ID as observed in our experiment. These findings are consistent with the hypothesis that epigenetic changes, in addition to mutations, could contribute to a rapid regeneration of ID and explain the persistence of detectable ID in sets of genetically identical individuals.