Deciphering the patterns of genetic admixture and diversity in southern European cattle using genome-wide SNPs

Abstract

The divergence between indicine cattle (Bos indicus) and taurine cattle (Bos taurus) is estimated to have occurred approximately 250,000 years ago, but a small number of European cattle breeds still display shared ancestry with indicine cattle. Additionally, following the divergence of African and European taurine, the gene flow between African taurine and southern European cattle has also been proposed. However, the extent to which non-European cattle ancestry is diffused across southern European cattle has not been investigated thoroughly. Also, in recent times, many local breeds have suffered severe reductions in effective population size. Therefore, in the present study, we investigated the pattern of genetic diversity in various European cattle based on single nucleotide polymorphisms (SNP) identified from whole-genome sequencing data. Additionally, we also employed unlinked and phased SNP-based approaches on high-density SNP array data to characterize non-European cattle ancestry in several southern European cattle breeds. Using heterozygosity-based parameters, we concluded that, on average, nucleotide diversity is greater in southern European cattle than western European (British and commercial) cattle. However, an abundance of long runs of homozygosity (ROH) and the pattern of Linkage disequilibrium decay suggested recent bottlenecks in Maltese and Romagnola. High nucleotide diversity outside ROH indicated a highly diverse founder population for southern European and African taurine. We also show that Iberian cattle display shared ancestry with African cattle. Furthermore, we show that Podolica is an ancient cross-bred between Indicine zebu and European taurine. Additionally, we also inferred similar ancestry profile of non-European cattle ancestry in different Balkan and Italian cattle breeds which might be an indication of the common origin of indicine ancestry in these breeds. Finally, we discuss several plausible demographic scenarios which might account for the presence of non-European cattle ancestry in these cattle breeds.

Keywords: African taurine; SNPs; admixture; cattle; genetic diversity; haplotype; indicine ancestry; southern European.

Figure 1

Boxplots showing average population scaled mutation rate (a) and average heterozygosity calculated in 10‐kbp window using whole‐genome sequencing data. AFRTAU: African Taurine; AFRZEB: African Zebu; BAITAU: Balkan and Italian Taurine; IBRTAU: Iberian Taurine; INDZEB: Indian Zebu; WESTAU: western European Taurine. Refer to Supporting Information Table S1 for the breed abbreviations

Figure 2

Boxplots showing average heterozygosity calculated in 10‐kbp window outside ROH (a) and distribution of ROH (b) using whole‐genome sequencing data. AFRTAU: African Taurine; AFRZEB: African Zebu; BAITAU: Balkan and Italian Taurine; IBRTAU: Iberian Taurine; INDZEB: Indian Zebu; WESTAU: western European Taurine. Refer to Supporting Information Table S1 for the breed abbreviations

Figure 3

Unsupervised hierarchical clustering (a) showing results for an inferred number of clusters, K varying from 2 to 6. Linkage disequilibrium decay analysis (b) comparing central Italian cattle breeds against commercial cattle breeds. Refer to Supporting Information Table S2 for the breed abbreviations

Figure 4

Three‐population tests with Busha (a), Pajuna (b), Marchigiana (c) and Podolica (d) as target populations. In the case of Podolica, f3 tests were performed on whole‐genome sequencing data, while for the remaining population, f3 tests were performed on SNP array data. The dot shows f3 statistics value, while the horizontal bar shows a plus or minus standard error. Refer to Supporting Information Table S2 for the breed abbreviations

Figure 5

Maximum‐likelihood‐based phylogenetic tree. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix. Refer to Supporting Information Table S2 for the breed abbreviations

Figure 6

Clustering of individuals based on fineStructure algorithm. Note that breeds are coloured according to their geographic origin. The intensity of colour indicates shared haplotypic segments (values in terms of centiMorgan) based on chunklength coancestry matrix generated by ChromoPainter algorithm. The number beside the clusters indicates (1) Zebu cattle, (2) African cattle (N'Dama and EAZ), (3) southern European cattle (Iberian and Italian) and (4) west European cattle (commercial and British cattle). Note that African cattle clusters with European when performed the same analysis but with a smaller number of zebu and taurine samples (Supporting Information Figure S3). Refer to Supporting Information Table S2 for the breed abbreviations

Figure 7

Ancestry proportion of different donor populations in the genome of Italian and Balkan cattle breeds. INDZEB: Indian Zebu; AFRTAU: African taurine; SOUTAU: southern European taurine (without Italian cattle breeds); WESTAU: western European taurine. Note that Busha individuals come from two different subpopulations and hence treated separately in this analysis. Refer to Supporting Information Table S2 for the breed abbreviations