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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.

SUBMITTER: Berenos C

PROVIDER: S-EPMC4950049 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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

Bérénos Camillo C Ellis Philip A PA Pilkington Jill G JG Pemberton Josephine M JM

Molecular ecology 20160606 13

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 coefficient ...[more]

PMID: 27135155

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Project description:BACKGROUND:Inbreeding decreases animal performance (inbreeding depression), but not all inbreeding is expected to be equally harmful. Recent inbreeding is expected to be more harmful than ancient inbreeding, because selection decreases the frequency of deleterious alleles over time. Selection efficiency is increased by inbreeding, a process called purging. Our objective was to investigate effects of recent and ancient inbreeding on yield, fertility and udder health traits in Dutch Holstein-Friesian cows. METHODS:In total, 38,792 first-parity cows were included. Pedigree inbreeding ([Formula: see text]) was computed and 75 k genotype data were used to compute genomic inbreeding, among others based on regions of homozygosity (ROH) in the genome ([Formula: see text]). RESULTS:Inbreeding depression was observed, e.g. a 1% increase in [Formula: see text] was associated with a 36.3 kg (SE?=?2.4) decrease in 305-day milk yield, a 0.48 day (SE?=?0.15) increase in calving interval and a 0.86 unit (SE?=?0.28) increase in somatic cell score for day 150 through to 400. These effects equalled -?0.45, 0.12 and 0.05% of the trait means, respectively. When [Formula: see text] was split into generation-based components, inbreeding on recent generations was more harmful than inbreeding on more distant generations for yield traits. When [Formula: see text] was split into new and ancestral components, based on whether alleles were identical-by-descent for the first time or not, new inbreeding was more harmful than ancestral inbreeding, especially for yield traits. For example, a 1% increase in new inbreeding was associated with a 2.42 kg (SE?=?0.41) decrease in 305-day fat yield, compared to a 0.03 kg (SE?=?0.71) increase for ancestral inbreeding. There were no clear differences between effects of long ROH (recent inbreeding) and short ROH (ancient inbreeding). CONCLUSIONS:Inbreeding depression was observed for yield, fertility and udder health traits. For yield traits and based on pedigree, inbreeding on recent generations was more harmful than inbreeding on distant generations and there was evidence of purging. Across all traits, long and short ROH contributed to inbreeding depression. In future work, inbreeding depression and purging should be assessed in more detail at the genomic level, using higher density information and genomic time series.

Project description:Inbreeding coefficients can be estimated either from pedigree data or from genomic data, and with genomic data, they are either global or local (when the linkage map is used). Recently, we developed a new hidden Markov model (HMM) that estimates probabilities of homozygosity-by-descent (HBD) at each marker position and automatically partitions autozygosity in multiple age-related classes (based on the length of HBD segments). Our objectives were to: (1) characterize inbreeding with our model in an intensively selected population such as the Belgian Blue Beef (BBB) cattle breed; (2) compare the properties of the model at different marker densities; and (3) compare our model with other methods.When using 600 K single nucleotide polymorphisms (SNPs), the inbreeding coefficient (probability of sampling an HBD locus in an individual) was on average 0.303 (ranging from 0.258 to 0.375). HBD-classes associated to historical ancestors (with small segments ? 200 kb) accounted for 21.6% of the genome length (71.4% of the total length of the genome in HBD segments), whereas classes associated to more recent ancestors accounted for only 22.6% of the total length of the genome in HBD segments. However, these recent classes presented more individual variation than more ancient classes. Although inbreeding coefficients obtained with low SNP densities (7 and 32 K) were much lower (0.060 and 0.093), they were highly correlated with those obtained at higher density (r = 0.934 and 0.975, respectively), indicating that they captured most of the individual variation. At higher SNP density, smaller HBD segments are identified and, thus, more past generations can be explored. We observed very high correlations between our estimates and those based on homozygosity (r = 0.95) or on runs-of-homozygosity (r = 0.95). As expected, pedigree-based estimates were mainly correlated with recent HBD-classes (r = 0.56).Although we observed high levels of autozygosity associated with small HBD segments in BBB cattle, recent inbreeding accounted for most of the individual variation. Recent autozygosity can be captured efficiently with low-density SNP arrays and relatively simple models (e.g., two HBD classes). The HMM framework provides local HBD probabilities that are still useful at lower SNP densities.

Dataset Information

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

Publications

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

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