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Human-Mediated Introgression of Haplotypes in a Modern Dairy

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Human-Mediated Introgression of Haplotypes in a Modern Dairy Genetics: Early Online, published on May 30, 2018 as 10.1534/genetics.118.301143 1 Human-mediated introgression of haplotypes in a modern 2 dairy cattle breed 3 4 Qianqian Zhang1,2,#,*, Mario Calus2, Mirte Bosse2, Goutam Sahana1, Mogens Sandø Lund1, and 5 Bernt Guldbrandtsen1 6 7 1 Center for Quantitative Genetics and Genomics, Department of Molecular Biology and Genetics, 8 Aarhus University, Denmark 9 2 Animal Breeding and Genomics, Wageningen University & Research, the Netherlands 10 # Present address: Department of Veterinary and Animal Sciences, Faculty of Health and Medical 11 Sciences, University of Copenhagen, Denmark 12 * Corresponding author 13 14 Email addresses: 15 QZ: [email protected] 16 MC: [email protected] 17 MB: [email protected] 18 GS: [email protected] 19 MSL: [email protected] 20 BG: [email protected] Copyright 2018. 21 Abstract 22 23 Domestic animals can serve as model systems of adaptive introgression and their genomic 24 signatures. In part their usefulness as model systems is due to their well-known histories. Different 25 breeding strategies such as introgression and artificial selection have generated numerous desirable 26 phenotypes and superior performance in domestic animals. The Modern Danish Red Dairy Cattle is 27 studied as an example of an introgressed population. It originates from crossing the traditional 28 Danish Red Dairy Cattle with the Holstein and Brown Swiss breeds, both known for high milk 29 production. This crossing happened among other things due to changes in production system, to 30 raise milk production and overall performance. The genomes of Modern Danish Red Dairy Cattle 31 are heavily influenced by regions introgressed from the Holstein and Brown Swiss breeds and under 32 subsequent selection in the admixed population. The introgressed proportion of the genome was 33 found to be highly variable across the genome. Haplotypes introgressed from Holstein and Brown 34 Swiss contained or overlapped known genes affecting milk production, as well as protein and fat 35 content (CD14, ZNF215, BCL2L12 and THRSP for Holstein origin; ITPR2, BCAT1, LAP3 and 36 MED28 for Brown Swiss origin). Genomic regions with high introgression signals also contained 37 genes and enriched QTLs associated with calving traits, body confirmation, feed efficiency, carcass, 38 and fertility traits. These introgressed signals with relative identity by descent scores larger than the 39 median showing Holstein or Brown Swiss introgression are mostly significantly correlated with the 40 corresponding test statistics from signatures of selection analyses in Modern Danish Red Dairy 41 Cattle. Meanwhile, the putative significant introgressed signals have a significant dependency with 42 the putative significant signals from signatures of selection analyses. Artificial Selection has played 43 an important role in the genomic footprints of introgression in the genome of Modern Danish Red 44 Dairy Cattle. Our study on a modern cattle breed contributes to an understanding of genomic 45 consequences of selective introgression by demonstrating the extent to which adaptive effects 46 contribute to shaping the specific genomic consequences of introgression. 47 48 Keywords: selective introgression, signature of selection, high yielding cattle breeds, modern dairy 49 cattle breed 50 51 52 53 Introduction 54 55 Processes of adaptive introgression are complex and their genomic signatures in human and other 56 species have been studied extensively (Hasenkamp, Solomon et al. 2015, Deschamps, Laval et al. 57 2016, Figueiro, Li et al. 2017, Jagoda, Lawson et al. 2017). Genome analysis has enabled an in- 58 depth assessment of genomic consequences of different demographic processes including 59 introgression, selection, and their interplay in the modern species (Deschamps, Laval et al. 2016, 60 Figueiro, Li et al. 2017). Domestic animals can serve as model organisms for these processes. They 61 have several advantages in understanding the impact of introgression and selection on genomes: 62 first, introgression and selection is known to occur between breeds, and the processes are often well 63 documented by breeders; second, massive data are routine collected before and after introgression 64 and selection such as parentage, genotypes and phenotypes; third, under controlled appropriate 65 environmental conditions a large part of genomic consequence is caused by human-mediated 66 directional introgression and selection. 67 68 Artificial selection and different breeding strategies have enabled generating numerous desirable 69 phenotypes in domestic animals such as cattle (Hartwig, Wellmann et al. 2015, Buzanskas, Ventura 70 et al. 2017, Davis, Spelman et al. 2017), pigs (Bosse, Megens et al. 2014, Bosse, Megens et al. 2014, 71 Ai, Fang et al. 2015) and dogs (Galov, Fabbri et al. 2015, vonHoldt, Kays et al. 2016). Strategies 72 including crossbreeding and introgression have been very successful in improving productivity and 73 performance in domestic animals. For example, Chinese pig breeds have been imported to Europe 74 to improve the productivity of European pigs in the late eighteenth and early nineteenth centuries 75 (White 2011). The fertility related traits have been largely improved by the crossbreeding and 76 introgression from Asian pigs (Merks, Mathur et al. 2012, Bosse, Megens et al. 2014, Bosse, Lopes 77 et al. 2015). Similarly, in dairy cattle, crossbreeding and following introgression between local 78 breeds with other breeds has been applied in order to achieve better productivity and performance 79 (Davis, Spelman et al. 2017). The genetic architecture of modern domestic animals including dairy 80 cattle is shaped by the interplay between different forces including the intentional introduction of 81 favorable alleles from other breeds, subsequent selection for favorable introgressed alleles and 82 demographic processes. 83 84 Since the introduction of scientific breeding, the main breeding goal in cattle has been to improve 85 milk yield, fat, and protein content, even for dual-purpose breeds in intensive farming systems 86 especially in Europe (Hartwig, Wellmann et al. 2015). By the crossing of high yielding breeds with 87 local breeds, the productivity of local breeds could rapidly be increased at the expense of the 88 genetic distinctiveness of the local breeds. The high productivity of these admixed breeds was 89 further improved by intense selection, resulting in increased frequencies or even fixation of 90 favorable alleles. Many of the variants thus spreading in the population will have been of 91 introgressed origin. With the great success of cattle breeding including crossbreeding, and because 92 of the availability of large scale genomic data sets, analysis of admixed local cattle breeds 93 represents an appealing model to identify the genomic consequences of admixture with the intention 94 of improving traits of interest in local breeds. We expect that the introgressed genomic regions play 95 an important role in improving productivity and performance in the crossbreeds. We hypothesize 96 that: 1) the genome-wide introgressed regions are non-randomly distributed across the genome with 97 respect to their genomic locations, and that: 2) the majority of highly introgressed regions affects 98 production and performance traits, and that: 3) these introduced haplotypes are or have been under 99 selection in the admixed breed. 100 101 To test these hypotheses and identify specific genomic regions and genes of interest involved in the 102 important traits from high-yields breeds such as Holstein (HOL) and Brown Swiss (BSW), we use 103 the hybrid Modern Danish Red Dairy Cattle (mRDC) breed as an example. Our analyses illustrate 104 the patterns of introgressed and selected haplotypes in an admixed local breed. The hybrid mRDC 105 originates from traditional Danish Red Dairy Cattle (tRDC). In recent decades Holstein and Brown 106 Swiss have been used extensively to improve the milk yield of mRDC (Kantanen, Olsaker et al. 107 2000). Years of crossbreeding and selection have led to the differentiation between mRDC and 108 tRDC. The introgression of and selection for haplotypes from HOL and BSW has probably made a 109 significant contribution to the increased milk production level of mRDC. The objective of this study 110 was to examine genomic patterns of introgression from two high-yielding breeds (HOL and BSW) 111 in a modern dairy breed (i.e. the hybrid mRDC), and unravel the consequences of introgression and 112 selection at the genome level using the whole genome sequence data. 113 114 Methods 115 116 1. SNP genotyping, sequencing, variant calling, and quality control 117 118 Whole genome sequence data were available for 97 animals from 4 breeds (32 Holstein: HOL; 20 119 Brown Swiss: BSW; 15 traditional Red Danish Dairy Cattle: tRDC; 30 modern Danish Red Dairy 120 cattle: mRDC). All individuals’ genomes were sequenced to ~10× of depth or deeper using Illumina 121 paired-end sequencing. Reads were aligned to the cattle genome assembly UMD3.1 (Zimin, 122 Delcher et al. 2009) using bwa (Li and Durbin 2009). Aligned sequences were converted to raw 123 BAM files using samtools (Li, Handsaker et al. 2009). Duplicate reads were marked using the 124 samtools rmdup option (Li, Handsaker et al. 2009). The Genome Analysis Toolkit (McKenna, Hanna 125 et al. 2010) was used for local realignment around insertion/deletion (indels) regions, and 126 recalibration following the 1000 Bull Genome
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