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Introgression and the Fate of Domesticated Genes in a Wild Mammal

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Introgression and the Fate of Domesticated Genes in a Wild Mammal Adaptive Admixture in Soay Sheep 1 1 Introgression and the Fate of Domesticated Genes in a Wild Mammal This is the peer reviewed version of the following article: Feulner PGD, Gratten J, Kijas JW, Visscher 2 Population PM, Pemberton JM & Slate J (2013) Introgression and the fate of domesticated genes in a wild mammal population. Molecular Ecology 22: 4210–4221, which has been published in final form at 10.1111/mec.12378. This article may be used for non-commercial purposes in accordance with 3 Wiley Terms and Conditions for self-archiving. 4 Philine G.D. Feulner*1,2, Jacob Gratten*1,3, James W. Kijas4, Peter M. Visscher1,5, Josephine 5 M. Pemberton6, Jon Slate1 6 *joint first authors 7 8 1 Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK 9 2 Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, 24306 Ploen, 10 Germany 11 3 The University of Queensland, Queensland Brain Institute, Brisbane, Queensland, Australia 12 4 Livestock Industries, CSIRO, Brisbane, Australia 13 5 The University of Queensland Diamantina Institute, Brisbane, Queensland, Australia 14 6 Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, 15 Edinburgh, EH9 3JT, UK 16 17 Keywords: admixture; adaptive introgression; Soay sheep; domesticated alleles; natural 18 selection 19 20 Corresponding author: 21 Philine Feulner 22 Max Planck Institute for Evolutionary Biology 23 August-Thienemann-Str. 2 24 24306 Plön 1 Adaptive Admixture in Soay Sheep 2 25 Germany 26 Tel: +49 (0) 4522 763-228 27 Fax: +49 (0) 4522 763-310 28 [email protected] 29 2 Adaptive Admixture in Soay Sheep 3 30 Abstract 31 When domesticated species are not reproductively isolated from their wild relatives, the opportunity 32 arises for artificially selected variants to be re-introduced into the wild. However, the evolutionary 33 consequences of introgression of domesticated genes back into the wild are poorly understood. By 34 combining high-throughput genotyping with 25 years of long-term ecological field data we describe 35 the occurrence and consequences of admixture between a primitive sheep breed, the free-living Soay 36 sheep of St Kilda, and more modern breeds. Utilising data from a 50K ovine SNP chip, together with 37 forward simulations of demographic scenarios, we show that admixture occurred between Soay sheep 38 and a more modern breed, consistent with historical accounts, approximately 150 years ago. 39 Haplotype sharing analyses with other breeds revealed that polymorphisms in coat colour and pattern 40 in Soay sheep arose as a result of introgression of genetic variants favoured by artificial selection. 41 Because the haplotypes carrying the causative mutations are known to be under natural selection in 42 free-living Soay sheep, the admixture event created an opportunity to observe the outcome of a 43 ‘natural laboratory’ experiment where ancestral and domesticated genes competed with each other. 44 The haplotype carrying the domesticated light coat colour allele was favoured by natural selection 45 while the haplotype associated with the domesticated self coat pattern allele was associated with 46 decreased survival. Therefore, we demonstrate that introgression of domesticated alleles into wild 47 populations can provide a novel source of variation capable of generating rapid evolutionary changes. 48 49 3 Adaptive Admixture in Soay Sheep 4 50 Introduction 51 Admixture brings together the genomes of divergent populations. The resulting introgression 52 of alleles from one population into another can either hinder local adaptation by slowing 53 down the rate of adaptive evolution, or promote adaptation by providing a substantial source 54 of genetic variation upon which selection can act. Admixture is an important evolutionary 55 force both in the context of hybrid speciation (Baack & Rieseberg 2007) and adaptation to 56 new environments (Mallet 2005; Nolte & Tautz 2010; Rieseberg 2009; Staubach et al. 2012), 57 and is also hypothesised to facilitate invasions to new environments (Ellstrand & 58 Schierenbeck 2000; Keller & Taylor 2010). Admixture between wild species and their 59 domesticated relatives is a well-documented phenomenon e.g. in sunflowers (Kane et al. 60 2009), radish (Snow et al. 2010), bees (Zayed & Whitfield 2008), dogs/gray wolves 61 (Anderson et al. 2009), cats (Lecis et al. 2006), cattle/bison (Halbert & Derr 2007). However, 62 demonstrating the adaptive impact of admixture is challenging because it requires that 63 introgressed genomic loci can be identified and that their frequency and fitness consequences 64 can be quantified and traced over many generations; to date such studies have largely been 65 restricted to experimental populations (Burke & Rieseberg 2003). 66 67 Recent technological advances have provided new opportunities to study admixture on a 68 genome-wide scale, because many thousands of genomic regions can now be genotyped 69 simultaneously; examples include the datasets generated by the Human HapMap Consortium 70 (Gibbs et al. 2003) and similar efforts for other species (Gibbs et al. 2009; Kijas et al. 2012; 71 Rubin et al. 2013). Combining high-throughput genomics methods with long-term ecological 72 data from wild populations promises to improve our understanding of the genome-wide 73 impact of admixture and the evolutionary fate of introgressed alleles in nature. 4 Adaptive Admixture in Soay Sheep 5 74 75 The Soay sheep of the St Kilda archipelago, Scotland are a free-living population that has 76 been the focus of an intensive long-term (almost three decades) field study on the island of 77 Hirta (Clutton-Brock & Pemberton 2004; Coulson et al. 2001). Soay sheep originated during 78 early domestication of sheep and are amongst the most primitive of all surviving breeds 79 (Chessa et al. 2009). They closely resemble the wild ancestors of modern sheep (Figure 1), 80 and have survived on the remote island with which they share their name for up to 4000 years 81 (Figure 2). In the past several hundred years, other breeds are known to have existed on the St 82 Kilda archipelago. The history of sheep on the St Kilda islands is closely tied to that of the 83 human settlers who inhabited the largest island in the group, Hirta, until they and their 84 livestock were evacuated in 1930 (see Figure 2). It is known that the St Kildans kept the Old 85 Scottish Shortwool breed (also known as Dunface) until the late 1800s, and there are 86 anecdotal reports suggesting that Dunface sheep were placed on Soay by the St Kildans 87 (Elwes 1912; see Methods). The Dunface breed was later replaced by Scottish Blackface 88 sheep from ~1870, and has now gone extinct (Elwes 1912). However, the Boreray breed, 89 which survives on the neighbouring island of Boreray, was founded by crossing Dunface 90 sheep with Scottish Blackface Sheep (Morton Boyd 1981). Therefore, Boreray sheep can be 91 regarded as a ‘living museum’ containing Dunface genes. 92 93 In 1932, one hundred and seven Soay sheep were moved from Soay to Hirta (i.e. after the 94 human population and their Scottish Blackface sheep were evacuated). Since then Soay sheep 95 have existed as unmanaged free-living populations on Soay and Hirta and are regarded as a 96 feral breed. While Soays are believed to be more or less unchanged since the bronze age, 97 Dunface were typical of Northern European short-tailed breeds that were improved during the 5 Adaptive Admixture in Soay Sheep 6 98 middle ages (Ryder 1981). Scottish Blackface sheep are a modern breed that gradually 99 replaced the Dunface breed throughout Scotland in the 1800s (Ryder 1981) and is now the 100 most numerous breed in the UK. 101 102 Surprisingly for a small island population, Soay sheep show a high degree of molecular and 103 phenotypic polymorphism. Two of the most striking polymorphisms (Figure 1 top panel) are 104 for coat colour (dark-light) and coat pattern (wild-self type). Gene mapping studies have 105 identified the molecular basis of these polymorphisms in the TYRP1 (Gratten et al. 2007) and 106 ASIP (Gratten et al. 2010) genes, respectively. The two genes are on different chromosomes, 107 segregate independently, and do not have epistatic effects (Gratten et al. 2012); i.e. the 108 polymorphisms and their effects are independent of each other. Subsequent investigation of 109 the relative fitness of TYRP1 revealed positive selection and a microevolutionary increase of 110 the frequency of the TYRP1 T allele, which is associated with light coat colour (Gratten et al. 111 2008). This microevolutionary trend is explained by genetic linkage between the causal 112 mutation underlying the colour polymorphism and quantitative trait loci with antagonistic 113 effects on size and fitness (Gratten et al. 2008). Similarly at ASIP, there was negative viability 114 selection on the self-pattern associated haplotype (Gratten et al. 2012). By employing gene- 115 dropping simulations, it has been shown that microevolutionary trends in the frequency and 116 excess of ASIP heterozygotes cannot be explained by genetic drift alone (Gratten et al. 2012). 117 When the coat colour mutation was identified, an exceptionally high degree of linkage 118 disequilibrium in the genomic region around TYRP1 was noted, and it was suggested that this 119 could be a signature of admixture between Soay sheep and another breed; for further details 120 see (Gratten et al. 2010). 121 6 Adaptive Admixture in Soay Sheep 7 122 In this study we tested whether genetic variation segregating within the contemporary Soay 123 sheep population on Hirta has been enhanced by the introgression of genes from more modern 124 breeds. Having demonstrated evidence of admixture, we then used genomic data and 125 simulations of different historical scenarios to investigate the origins of introduced genetic 126 variation. Admixture with Dunface sheep in the latter half of the 1800s appears to be the most 127 plausible explanation.
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