Environmental stress increases selection against and dominance of deleterious mutations in inbred families of the Pacific oyster Crassostrea gigas

Abstract

The deleterious effects of inbreeding are well documented and of major concern in conservation biology. Stressful environments have generally been shown to increase inbreeding depression; however, little is known about the underlying genetic mechanisms of the inbreeding-by-stress interaction and to what extent the fitness of individual deleterious mutations is altered under stress. Using microsatellite marker segregation data and quantitative trait locus (QTL) mapping methods, I performed a genome scan for deleterious mutations affecting viability (viability or vQTL) in two inbred families of the Pacific oyster Crassostrea gigas, reared in a stressful, nutrient-poor diet and a favourable, nutrient-rich diet, which had significant effects on growth and survival. Twice as many vQTL were detected in the stressful diet compared with the favourable diet, resulting primarily from substantially greater mortality of homozygous genotypes. At vQTL, estimates of selection (s) and dominance (h) were greater in the stressful environment (= 0.86 vs. 0.54 and = 0.35 vs. 0.18, in stressful and nonstressful diets, respectively). There was no evidence of interaction between vQTL. Individual vQTL differed across diets in selection only, or in both selection and dominance, and some vQTL were not affected by diet. These results suggest that stress-associated increases in selection against individual deleterious alleles underlie greater inbreeding depression with stress. Furthermore, the finding that inbreeding-by-environment interaction appears, to some extent, to be locus specific, helps to explain previous observations of lineage-specific expression of inbreeding depression and environment-specific purging, which have important implications for conservation and evolutionary biology.

Genetic inviability is a major driver of type III survivorship in experimental families of a highly fecund marine bivalve

“…Mortality great enough to accommodate 99% genetic inviability must, therefore, have occurred during early life stages in the hatchery, where high mortality is typical (Helm & Bourne ). This timing would be consistent with the developmental patterns of selective and actual mortality previously observed in hatchery‐reared inbred families (Launey & Hedgecock ; Plough & Hedgecock ; Plough ) and with type III survivorship in general.…”

“…This 99% genetic inviability in random‐bred families is higher but probably not significantly higher than what we previously reported for inbred crosses, 90–96% (Plough & Hedgecock ; Plough ). Intuitively, one expects inbred crosses to suffer greater mortality from inbreeding depression, but evidence is mixed in the literature.…”

The roles of demography and genetics in the early stages of colonization

“…Inbreeding depression can manifest to varying degrees according to the environment [37,38], often being more severe in stressful environments [39,40]. Inbreeding depression may increase in stressful environments because the expression of genetic load (deleterious alleles) can change under stress [41,42]. For example, the dominance of deleterious alleles as well as selection against deleterious recessive alleles was shown to increase with stress, resulting in higher mortality of genotypes homozygous at deleterious loci [41].…”

“…Inbreeding depression may increase in stressful environments because the expression of genetic load (deleterious alleles) can change under stress [41,42]. For example, the dominance of deleterious alleles as well as selection against deleterious recessive alleles was shown to increase with stress, resulting in higher mortality of genotypes homozygous at deleterious loci [41]. The differential expression of deleterious alleles can also lower fitness of individuals by increasing their overall susceptibility to environmental stress and by hindering evolutionary responses, such as adaptive phenotypic plasticity, which could provide means for short-term survival in the face of sudden environmental change [42,43].…”

Reduction in the cumulative effect of stress-induced inbreeding depression due to intragenerational purging in Drosophila melanogaster

“…Purging is a reduction in the frequency of deleterious recessive alleles owing to their increased exposure to selection under inbreeding (Hedrick, 1994;Wang, 2000) and has been proposed as a potential tool for managing ID in endangered and captive populations (Swindell and Bouzat, 2006;de Cara et al, 2013). The effectiveness of purging in a population is predicted to increase during exposure to stress, given that stress can magnify the strength of selection against deleterious alleles (Bijlsma et al, 1999;Plough, 2012;Reed et al, 2012).…”