Genomic analyses suggest adaptive differentiation of northern European native cattle breeds

Abstract

Native domestic breeds represent important cultural heritage and genetic diversity relevant for production traits, environmental adaptation and food security. However, risks associated with low effective population size, such as inbreeding and genetic drift, have elevated concerns over whether unique within-breed lineages should be kept separate or managed as one population. As a conservation genomic case study of the genetic diversity represented by native breeds, we examined native and commercial cattle (Bos taurus) breeds including the threatened Danish Jutland cattle. We examined population structure and genetic diversity within breeds and lineages genotyped across 770K single nucleotide polymorphism loci to determine (a) the amount and distribution of genetic diversity in native breeds, and (b) the role of genetic drift versus selection. We further investigated the presence of outlier loci to detect (c) signatures of environmental selection in native versus commercial breeds, and (d) native breed adaptation to various landscapes. Moreover, we included older cryopreserved samples to determine (e) whether cryopreservation allows (re)introduction of original genetic diversity. We investigated a final set of 195 individuals and 677K autosomal loci for genetic diversity within and among breeds, examined population structure with principal component analyses and a maximum-likelihood approach and searched for outlier loci suggesting artificial or natural selection. Our findings demonstrate the potential of genomics for identifying the uniqueness of native domestic breeds, and for maintaining their genetic diversity and long-term evolutionary potential through conservation plans balancing inbreeding with carefully designed outcrossing. One promising opportunity is the use of cryopreserved samples, which can provide important genetic diversity for populations with few individuals, while helping to preserve their traditional genetic characteristics. Outlier tests for native versus commercial breeds identified genes associated with climate adaptation, immunity and metabolism, and native breeds may carry genetic variation important for animal health and robustness in a changing climate.

Keywords: Bos taurus; animal health; artificial selection; climate adaptation; conservation genomics; environmental selection; production traits; single nucleotide polymorphism.

Figure 1

Proposed timeline for founding of the four contemporary lineages of the Danish Jutland cattle breed. The Westergaard‐lineage is deemed to be the oldest, although the precise time of its origin is unknown

Figure 2

Principal component analyses (PCAs) with 195 individuals showing the first and second PC axes. Cattle breeds/lineages (denoted in figure legend as Pop) are as follows: FI: Faroe Island cattle; HOL: Holstein; JER: Jersey; JK: Jutland cattle Kortegaard‐lineage; JO: Jutland cattle Oregaard‐lineage; JV: Jutland cattle Vesterbølle‐lineage; JW: Jutland cattle Westergaard‐lineage; OB1: old bulls pre‐1980 (cryopreserved semen samples from SDM‐1965 cattle); OB2: old bulls post‐1980 (cryopreserved from n = 14 Jutland and n = 4 SDM‐1965 cattle); SDM: SDM‐1965 cattle; WNF: Western Norwegian Fjord cattle; WNR: Western Norwegian Red‐polled cattle

Figure 3

ADMIXTURE analyses of cattle with cross‐validation (CV) error plot for K‐values from 2 to 9 with 195 individuals and 88,190 single nucleotide polymorphism loci. The CV error is markedly reduced with each increase in K until K = 5. Hereafter it declines more slowly towards the minimal value at K = 9. Increases in K beyond this level are not supported

Figure 4

ADMIXTURE plots for K‐values from 2 to 9 clusters with 195 individuals and 88,190 single nucleotide polymorphism loci. Each vertical bar represents one individual, and the Y‐axis shows individual ancestry (range: 0–1). Cattle breeds/lineages are as follows: FI: Faroe Island cattle; HOL: Holstein; JER: Jersey; JK: Jutland cattle Kortegaard‐lineage; JO: Jutland cattle Oregaard‐lineage; JV: Jutland cattle Vesterbølle‐lineage; JW: Jutland cattle Westergaard‐lineage; OB1: old bulls pre‐1980 (cryopreserved semen samples from SDM‐1965 cattle); OB2: old bulls post‐1980 (cryopreserved from n = 14 Jutland and n = 4 SDM‐1965 cattle); SDM: SDM‐1965 cattle; WNF: Western Norwegian Fjord cattle; WNR: Western Norwegian Red‐polled cattle

Figure 5

Maximum‐likelihood tree for 12 cattle populations with 195 individuals and 595,025 SNPs pruned for minor allele frequency of 1% and genotyping success of 98%. The scale bar on the horizontal axis shows 10× the average standard error of the sample covariance matrix, and the length of horizontal branches is proportional to the amount of genetic drift the populations have experienced. Cattle breeds/lineages are as follows: FI: Faroe Island cattle; HOL: Holstein; JER: Jersey; JK: Jutland cattle Kortegaard‐lineage; JO: Jutland cattle Oregaard‐lineage; JV: Jutland cattle Vesterbølle‐lineage; JW: Jutland cattle Westergaard‐lineage; OB1: old bulls pre‐1980 (cryopreserved semen samples from SDM‐1965 cattle); OB2: old bulls post‐1980 (cryopreserved from n = 14 Jutland and n = 4 SDM‐1965 cattle); SDM: SDM‐1965 cattle; WNF: Western Norwegian Fjord cattle; WNR: Western Norwegian Red‐polled cattle. Migration arrows are coloured according to their weight and indicate admixture between old bulls post‐1980 and Kortegaard, as well as between old bulls post‐1980 and SDM‐1965

Figure 6

Plots displaying runs of homozygosity (ROH) per autosomal chromosome and outliers from pairwise comparisons of native and commercial breeds central to this study. Outliers and ROH could both be indicative of selection, and we mapped our findings to examine the degree of overlap. ROH shared by at least six individuals per breed are shown in vertical coloured lines. Outlier loci where focal genes were found within 3,000‐bp flanking regions are marked as dark grey horizontal lines. The plots show pairwise comparisons of (a) Jutland cattle versus Holstein cattle, and (b) Jutland cattle versus Western Norwegian Red‐polled cattle