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The History and Evolution of the Denisovan-EPAS1

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The History and Evolution of the Denisovan-EPAS1 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.01.323113; this version posted October 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The history and evolution of the Denisovan-EPAS1 haplotype in Tibetans 2 3 4 Xinjun Zhang1, Kelsey Witt2,3, Amy Ko4, Kai Yuan5,6,7, Shuhua Xu5,6,7, Rasmus Nielsen4, Emilia 5 Huerta-Sanchez2,3* 6 7 8 1. Department of Ecology and Evolutionary Biology, University of California Los Angeles 9 2. Department of Ecology and Evolutionary Biology, Brown University 10 3. Center for Computational Molecular Biology, Brown University 11 4. Department of Integrative Biology, University of California Berkeley 12 5. Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational 13 Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of 14 Sciences, Chinese Academy of Sciences, Shanghai, China; 15 6. School of Life Science and Technology, Shanghai Technology University, Shanghai, China; 16 7. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 17 Kunming, China; 18 *Corresponding author 19 20 21 22 Abstract 23 24 Recent studies suggest that admixture with archaic hominins played an important 25 role in facilitating biological adaptations to new environments. For example, interbreeding 26 with Denisovans facilitated the adaptation to high altitude environments on the Tibetan 27 Plateau. Specifically, the EPAS1 gene, a transcription factor that regulates the response to 28 hypoxia, exhibits strong signatures of both positive selection and introgression from 29 Denisovans in Tibetan individuals. Interestingly, despite being geographically closer to the 30 Denisova cave, East Asian populations do not harbor as much Denisovan ancestry as 31 populations from Melanesia. Recently, two studies have suggested two independent waves 32 of Denisovan admixture into East Asians, one of which is shared with South Asians and 33 Oceanians. Here we leverage data from EPAS1 in 78 Tibetan individuals to interrogate which 34 of these two introgression events introduced the EPAS1 beneficial sequence into the 35 ancestral population of Tibetans, and we use the distribution of introgressed segment 36 lengths at this locus to infer the timing of the introgression and selection event. We find that 37 the introgression event unique to East Asians most likely introduced the beneficial haplotype 38 into the ancestral population of Tibetans around 43,000 (15,700–60,000) years ago, and 39 selection started 12,000 (1,925-50,000) years ago. Our estimates suggest that one of the 40 most convincing examples of adaptive introgression is in fact selection acting on standing 41 archaic variation. 42 43 44 45 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.01.323113; this version posted October 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 46 Introduction 47 48 The identification of the Denisovan genome using DNA recovered from a phalanx 49 bone is one of the most stunning discoveries in human evolution in the past decade1,2. 50 However, many questions remain unanswered regarding the Denisovans. For example: What 51 did the they look like? What was their geographical range? What is their genetic legacy to 52 modern humans? Much of the ongoing research investigating the Denisovans focuses on 53 studying the morphological features from dental and cranial samples3, dating the age of 54 remains from the Denisova cave4, and learning about the admixture events that involved 55 Denisovans, Neanderthals, and other unknown archaic populations1,5–7. We now know that 56 Denisovans diverged from Neanderthals approximately 390 thousand years ago (ka)8,9, and 57 both groups inhabited Eurasia until up to 40 ka4,10 based on radiocarbon dating of materials 58 from Neanderthal or Denisovan archeological sites. 59 Although the fossil remains of Denisovans found so far are limited in number and 60 highly fragmented in nature1,11,12, certain aspects of this hominin group have been revealed 61 through studying a single high-coverage genome2. The occurrence of admixture between 62 archaic hominins and modern humans is undisputed, as it left varying amounts of archaic 63 DNA in our genomes at detectable levels1,8,13. Notably, Papuans and indigenous Australians 64 harbor the largest genome-wide amount of Denisovan introgression (~ 1% – 5%1,6,14,15), 65 followed by East and South Asians (~ 0.06 % – 0.5%1,6,14), and Indigenous Americans (~ 66 0.05% – 0.4%1,6,14). Thus, one approach to study the Denisovans is through the surviving 67 Denisovan DNA segments in modern humans. 68 Examination of Denisovan-like DNA in modern humans revealed a number of 69 candidate genes with robust signatures of adaptive introgression16–21, among which the most 70 well-known example is found in the Endothelial Pas Domain Protein1 gene (EPAS1) in 71 modern Tibetans22–24 that facilitated local adaptation to their high altitude and hypoxic 72 environment. The discovery of adaptive introgression in Tibetans is particularly striking, as 73 they do not carry high amounts of Denisovan ancestry genome-wide, compared to other 74 South Asian and Oceanian populations6. Conversely, the Oceanian populations - including the 75 Papuans - do not carry the Denisovan EPAS1-haplotype, most likely due to the absence of 76 selective pressure outside of the high-altitude environment. The Tibetan plateau, with an 77 average altitude above 3,500 meters and oxygen concentration considerably lower than at 78 sea level, creates a strong physiological stress for most humans. One common 79 acclimatization to the hypoxic environment is an increase in hemoglobin concentration25, 80 which increases blood viscosity and is associated with increased risk of pregnancy 81 complications and cardiovascular disease26,27. Remarkably, Tibetans have a severely blunted 82 acclimatization response compared to lowlanders at high altitudes and tend not to suffer 83 from clinically elevated hemoglobin concentration28. This presumed adaptive response is 84 directly associated with variants in the EPAS1 gene, which encodes a transcription factor in 85 the hypoxia response pathway. 86 The remarkable Denisovan connection to Tibetans’ high-altitude adaptation has led 87 to more questions regarding this already mysterious hominin group. For example, why are 88 populations with Denisovan ancestry, including the Tibetans and Oceanians, located far 89 away from the Denisova cave in Siberia? One explanation for these seemingly puzzling 90 findings is a large Denisovan geographical range. Multiple introgression events may explain 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.01.323113; this version posted October 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 91 why some human populations exhibit higher levels of Denisovan introgression despite being 92 located far away from the Altai mountains in Siberia. Indeed, Browning et al.7 proposed two 93 Denisovan introgressions into modern East Asians, one of which is shared with Papuans and 94 South Asians. More recently, jacobs et al.29 proposed an additional introgression event into 95 the ancestral population of Papuans, making a total of three Denisovan introgression pulses 96 in Asia. Their estimates of divergence between the three Denisovan groups that admixed 97 with modern humans are large enough (~280 ka-360 ka) to suggest that there were multiple 98 Denisovan-like hominin groups inhabiting diverse locations in Asia. 99 In this study, we investigate the surviving Denisovan introgressed segments in 100 Tibetans to address the following questions: Do Tibetans exhibit signatures of more than one 101 Denisovan introgression? If so, which introgression event introduced the beneficial EPAS1 102 haplotype, and when? Did selection act immediately after introgression, or plausibly later 103 when modern humans began inhabiting the Tibetan Plateau? To address these questions, we 104 examined the EPAS1 gene sequences from a combined dataset of 78 Tibetan individuals from 105 two previously published studies23,30, among which 38 are high-coverage whole genome 106 sequences30. We leveraged information from the introgressed tracts in Tibetans to infer the 107 key time points related to the Denisovan introgression, as well as the onset of selection. We 108 also employed the whole genomes in the combined dataset to demonstrate that the 109 ancestors of modern Tibetans, similar to other East Asian populations7, experienced two 110 Denisovan introgression events. Our results provide resolution to the East Asian-specific 111 Denisovan admixture event that led to one of the most fascinating stories of human 112 adaptation, and shed light on the effects of different evolutionary processes that shape 113 patterns of adaptive introgression in humans. 114 115 116 Results 117 118 Evidence of three distinct archaic introgression episodes with ancestral Tibetans: one 119 from Neanderthals and two from Denisovans 120 121 To characterize the genomic landscape of archaic introgression in Tibetans and to 122 determine the number introgression pulses, we applied the method developed in Browning 123 et al.7, SPrime. This is a reference-free method that detects sets of diagnostic SNPs that tag 124 putatively archaic-introgressed segments in different regions of the genome. Applying 125 SPrime to the autosomes of 38 Tibetan genomes30 we inferred 1,426 regions, each containing 126 a set of diagnostic, putatively archaic-introgressed SNPs using Africans (YRI)31 as an 127 outgroup.
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