Inbreeding depression due to recent and ancient inbreeding in Dutch Holstein–Friesian dairy cattle

Abstract

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 ($$F_{PED}$$ F PED ) was computed and 75 k genotype data were used to compute genomic inbreeding, among others based on regions of homozygosity (ROH) in the genome ($$F_{ROH}$$ F ROH ). Results Inbreeding depression was observed, e.g. a 1% increase in $$F_{ROH}$$ F ROH 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 $$F_{PED}$$ F PED was split into generation-based components, inbreeding on recent generations was more harmful than inbreeding on more distant generations for yield traits. When $$F_{PED}$$ F PED 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.

Inbreeding depression across the genome of Dutch Holstein Friesian dairy cattle

“…In total, 38,792 first-parity cows (fraction Holstein Friesian > 87.5%, either red or black), which calved in the period 2012–2016 in 233 herds, were included. The same dataset was used as in Doekes et al [ 8 ]. Genotype and phenotype data were provided by the Dutch-Flemish cattle improvement co-operative (CRV; Arnhem, the Netherlands).…”

“…Genotypes were imputed to approximately 76 k, following Druet et al [ 18 ]. The 75,538 SNPs used by Doekes et al [ 8 ] were remapped to the ARS-UCD1.2 assembly, using the NAGRP Data Repository [ 19 ] and the NCBI Genome Remapping Service [ 20 ]. The final dataset comprised 75,377 successfully remapped SNPs.…”

“…Somatic cell scores were calculated as 1000 + 100*[log2 of cells/mL]. Descriptive statistics for the different traits are reported by Doekes et al [ 8 ].…”

“…Many important traits in dairy cattle show inbreeding depression [ 2 – 5 ]. For example, a 1% increase in pedigree-based inbreeding is associated with a decrease in 305-day milk yield of 20 to 38 kg and with an increase in calving interval of 0.2 to 0.7 days [ 6 – 8 ]. The reduction in mean performance is believed to be caused by the increase in homozygosity associated with inbreeding, reducing the expression of dominance effects [ 1 , 9 ].…”

“…[ 45 ]). Second, ROH capture more recent inbreeding, and recent inbreeding is expected to be more harmful than old inbreeding, although empirical results do not always support this hypothesis [ 2 , 8 ]. In a simulation study, Keller et al [ 17 ] found that, among the inbreeding measures that they investigated, ROH-based inbreeding performed best in capturing the homozygous inbreeding load.…”