Genomic analysis reveals depression due to both individual and maternal inbreeding in a free‐living mammal population

Abstract

There is ample evidence for inbreeding depression manifested as a reduction in fitness or fitness‐related traits in the focal individual. In many organisms, fitness is not only affected by genes carried by the individual, but also by genes carried by their parents, for example if receiving parental care. While maternal effects have been described in many systems, the extent to which inbreeding affects fitness directly through the focal individual, or indirectly through the inbreeding coefficients of its parents, has rarely been examined jointly. The Soay sheep study population is an excellent system in which to test for both effects, as lambs receive extended maternal care. Here, we tested for both maternal and individual inbreeding depression in three fitness‐related traits (birthweight and weight and hindleg length at 4 months of age) and three fitness components (first‐year survival, adult annual survival and annual breeding success), using either pedigree‐derived inbreeding or genomic estimators calculated using ~37 000 SNP markers. We found evidence for inbreeding depression in 4‐month hindleg and weight, first‐year survival in males, and annual survival and breeding success in adults. Maternal inbreeding was found to depress both birthweight and 4‐month weight. We detected more instances of significant inbreeding depression using genomic estimators than the pedigree, which is partly explained through the increased sample sizes available. In conclusion, our results highlight that cross‐generational inbreeding effects warrant further exploration in species with parental care and that modern genomic tools can be used successfully instead of, or alongside, pedigrees in natural populations.

Inbreeding depression by environment interactions in a free-living mammal population

“…We have previously shown that this estimator is more strongly associated with a range of fitness components and aspects of juvenile body size than either pedigree inbreeding or several other genomic estimators (Bérénos et al , 2016). F GRM is a genome-wide estimate of inbreeding that is a weighted average across all loci (Fhat3 in Yang et al , 2011) and was calculated in the GCTA software (Yang et al , 2011).…”

“…To estimate the effects of population density ( E ) and inbreeding depression ( ID ) and the interaction between them, two parallel models were run. Note that in this population, both maternal and offspring inbreeding have a potential effect on juvenile body size, and therefore both effects were fitted, following Bérénos et al (2016). First, a model was run that included E (population density) and F GRM (both maternal and individual) as main effects only (model 1).…”

“…Molecular markers offer an alternative route to estimating the inbreeding status of an individual, but until recently, the number of markers available in natural population studies (typically panels of 10–20 microsatellites) had only low power to detect inbreeding depression via heterozygosity–fitness correlations (Balloux et al , 2004; Slate et al , 2004; Chapman et al , 2009). More recently, however, it has been shown that large panels of single-nucleotide polymorphism (SNP) markers generate estimates of individual inbreeding that offer three advantages in natural populations (Hoffman et al , 2014; Bérénos et al , 2016; Huisman et al , 2016). A big advantage is that the inbreeding status of an individual is judged from its own DNA sample and is not contingent on samples from and known ancestry of other individuals in the way that a pedigree estimate is.…”

“…The rate of inbreeding in this population is generally low, for example, just 0.5% of individuals are inbred at F =0.25 (Figure 1; more details in the Discussion). Nevertheless, we have previously found inbreeding depression in three juvenile body size traits and four of six fitness components using a genomic estimator of inbreeding ( F GRM ) based on 37 037 SNP loci genotyped in a large sample of sheep (Bérénos et al , 2016). Specifically, we found statistically significant depression associated with an individual's own F GRM in 4-month weight and hindleg length, and we found inbreeding depression associated with the mother's F GRM in offspring birth weight and 4-month weight.…”

“…Natural selection on phenotypic traits is also consistently stronger during high density winters (Milner et al , 1999; Morrissey et al , 2012). In the analysis of inbreeding depression described above (Bérénos et al , 2016), year of birth and/or year of measurement was included as a random effect in the models to account for variation in conditions between years. Here, we extend these models by fitting population density as a fixed effect and then investigate ID × E by fitting an interaction term for F GRM × population density.…”