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Introgression in Hares 1 Title bioRxiv preprint doi: https://doi.org/10.1101/2020.06.19.160283; this version posted June 20, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 1 Running head: Introgression in hares 2 Title: The legacy of recurrent introgression during the radiation of hares 3 4 Mafalda S. Ferreira1,2,3, Matthew R. Jones3, Colin M. Callahan3, Liliana Farelo1, 5 Zelalem Tolesa4, Franz Suchentrunk5, Pierre Boursot6, L. Scott Mills7,8,9, Paulo C. 6 Alves1,2,7, Jeffrey M. Good3,7,*, José Melo-Ferreira1,2,* 7 8 1CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO 9 Laboratório Associado, Universidade do Porto, Vairão, Portugal. 10 2Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto, 11 Portugal. 12 3Division of Biological Sciences, University of Montana, Missoula, Montana, USA. 13 4Department of Biology, Hawassa University, Hawassa, Ethiopia. 14 5Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, 15 Vienna, Austria. 16 6Institut des Sciences de l’Évolution Montpellier (ISEM), Université Montpellier, CNRS, 17 IRD, EPHE, France. 18 7Wildlife Biology Program, College of Forestry and Conservation, University of 19 Montana, Missoula, Montana, USA. 20 8Office of Research and Creative Scholarship, University of Montana, Missoula, 21 Montana, USA. 22 9Fisheries, Wildlife, and Conservation Biology Program, Department of Forestry and 23 Environmental Resources, North Carolina State University, Raleigh, North Carolina, 24 USA. 25 *Shared senior authorship. bioRxiv preprint doi: https://doi.org/10.1101/2020.06.19.160283; this version posted June 20, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. Ferreira et al. 26 27 Correspondence: Mafalda S. Ferreira, [email protected]; Jeffrey M. Good, 28 [email protected]; José Melo-Ferreira, [email protected] 29 30 ABSTRACT 31 Hybridization may often be an important source of adaptive variation, but the extent and 32 long-term impacts of introgression have seldom been evaluated in the phylogenetic 33 context of a radiation. Hares (Lepus) represent a widespread mammalian radiation of 32 34 extant species characterized by striking ecological adaptations and recurrent admixture. 35 To understand the relevance of introgressive hybridization during the diversification of 36 Lepus, we analyzed whole exome sequences (61.7 Mb) from 15 species of hares (1- 4 37 individuals per species), spanning the global distribution of the genus, and two 38 outgroups. We used a coalescent framework to infer species relationships and 39 divergence times, despite extensive genealogical discordance. We found high levels of 40 allele sharing among species and show that this reflects extensive incomplete lineage 41 sorting and temporally layered hybridization. Our results revealed recurrent 42 introgression at all stages along the Lepus radiation, including recent gene flow between 43 extant species since the last glacial maximum, but also pervasive ancient introgression 44 occurring since near the origin of the hare lineages. We show that ancient hybridization 45 between northern hemisphere species has resulted in shared variation of potential 46 adaptive relevance to highly seasonal environments, including genes involved in 47 circadian rhythm regulation, pigmentation, and thermoregulation. Our results illustrate 48 how the genetic legacy of ancestral hybridization may persist across a radiation, leaving 49 a long-lasting signature of shared genetic variation that may contribute to adaptation 50 within and among species. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.19.160283; this version posted June 20, 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-ND 4.0 International license. Introgression in hares 51 52 KEYWORDS 53 Ancient introgression; Adaptation; Hybridization; Phylogenomics; Lepus 54 55 Species radiations are often accompanied by extensive gene flow between nascent 56 lineages (e.g., Lamichhaney et al. 2015; Árnason et al. 2018; Malinsky et al. 2018; Li et 57 al. 2019; Barth et al. 2020). Genetic signatures of hybridization between several closely 58 related species could either represent recent or ongoing introgressive hybridization 59 (Eaton et al. 2015), or the remnants of hybridization among ancestral populations that 60 remain shared among contemporary species (Malinsky et al. 2018; Li et al. 2019). 61 Although these alternatives can be difficult to differentiate in large radiations (Eaton et 62 al. 2015; Malinsky et al. 2018; Vanderpool et al. 2020), both ancient and contemporary 63 introgression has been linked to local adaptation in several systems (e.g., Liu et al. 64 2015; Gittelman et al. 2016; Meier et al. 2017; Barlow et al. 2018; Giska et al. 2019; 65 Svardal et al. 2020). Thus, unraveling the tempo and contribution of introgression to 66 standing genetic variation within and among species remains a critical step in 67 understanding the overall importance of introgression to evolution. 68 Reconstructing the history of hybridization between several closely related 69 species requires inferring evolutionary relationships among species while considering 70 the two primary processes – incomplete lineage sorting and gene flow – that may cause 71 sharing of genetic variation among populations (Malinsky et al. 2018). The network 72 multispecies coalescent (NMSC) model (Than et al. 2011; Solís-Lemus et al. 2017; 73 Degnan 2018) offers one promising framework that appears to resolve species 74 relationships in the face of multiple reticulation events and rapid speciation (Kozak et 75 al. 2018; Edelman et al. 2019). However, the NMSC is still prohibitive for large 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.19.160283; this version posted June 20, 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-ND 4.0 International license. Ferreira et al. 76 datasets and choosing the exact number of migration events is not straightforward (Yu 77 and Nakhleh 2015). Alternatively, site-based summary statistics based on tree 78 asymmetries (e.g., Green et al. 2010; Pease and Hahn 2015), or admixture proportions 79 (e.g., Reich et al. 2009; Martin et al. 2015; Malinsky et al. 2018) are simpler to 80 implement, but offer less power for localizing the timing and number of introgression 81 events when recurrent hybridization is layered across a phylogeny (Malinsky et al. 82 2018). A combination of methods is thus most appropriate to infer a species tree that 83 may have layered events of hybridization throughout time (e.g., Kozak et al. 2018; 84 Malinsky et al. 2018; Edelman et al. 2019; Li et al. 2019). 85 Hares and jackrabbits comprise a group of 32 species (genus Lepus; Smith et al. 86 2018) whose common ancestor likely originated in North America and spread 87 throughout most of the Northern Hemisphere and Africa presumably in the last 4-6 88 million years (Yamada et al. 2002; Matthee et al. 2004; Melo-Ferreira et al. 2012). 89 Hares are primarily associated with open grasslands, but can be found across a broad 90 range of biomes (e.g., desert, forest, or arctic) and elevations (e.g., from sea level to the 91 Himalayan or Ethiopian plateau; Smith et al., 2018). The Lepus radiation also provides 92 case studies of hybridization and introgression, since admixture has been detected 93 among several modern species pairs (e.g., Liu et al. 2011; Melo-Ferreira et al. 2012; 94 Tolesa et al. 2017; Jones et al. 2018; Seixas et al. 2018; Lado et al. 2019; Kinoshita et 95 al. 2019). Selection on introgressed variation has been hypothesized to have aided the 96 range expansion of the Iberian hare (Seixas et al. 2018), and has been directly linked to 97 convergent adaptive evolution of non-white winter coats in populations of two species 98 that change the color of their pelage seasonally (Jones et al. 2018; Giska et al. 2019; 99 Jones et al. 2020a). These studies suggest that the relatively recent exchange of genetic 100 variation among extant Lepus species has provided an important source of adaptive 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.19.160283; this version posted June 20, 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-ND 4.0 International license. Introgression in hares 101 variation. However, the phylogenetic relationships among Lepus species remain poorly 102 resolved (Halanych et al. 1999; Matthee et al. 2004; Melo-Ferreira et al. 2012; Melo- 103 Ferreira and Alves 2018), and the contribution of ancient gene flow to the Lepus 104 evolutionary history in a deeper phylogenetic context remains unknown. 105 Here, we use exome-wide data to infer the evolutionary history of 15 Lepus 106 species and show that hybridization between lineages has likely occurred since the 107 origin of the radiation. The combination of incomplete lineage sorting and these 108 temporally layered events of hybridization have resulted in extremely high levels of 109 shared genetic variation among extant species, including species that currently occur on 110 different continents. We then use the case of ancient admixture among northern latitude 111 species that occupy highly seasonal environments to investigate the gene content and 112 possible functional relevance of introgressed genomic regions.
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