bioRxiv preprint doi: https://doi.org/10.1101/2020.06.29.178392; this version posted January 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. Original article Running title: desert adaptation Peromyscus Limited evidence for parallel evolution among desert adapted Peromyscus deer mice Authors: Jocelyn P. Colella1,2,†*, Anna Tigano1,2, Olga Dudchenko3,4, Arina D. Omer4, Ruqayya Khan4,5, Ivan D. Bochkov4,5, Erez L. Aiden3,4,6,7, Matthew D. MacManes1,2 1University of New Hampshire, Molecular, Cellular, and Biomedical Sciences Department, Durham, NH 03824, USA; [email protected] (JPC), [email protected] (AT) [email protected] (MDM) 2Hubbard Genome Center, University of New Hampshire, Durham, NH 03824, USA 3Department of Computer Science, Department of Computational and Applied Mathematics; Center for Theoretical and Biological Physics, Rice University, Houston, TX 77030, USA; [email protected] (OD), [email protected] (ELA) 4The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; [email protected] (ADO), [email protected] (RK), [email protected] (IDB) 5Department of Computer Science, Department of Computational and Applied Mathematics, Rice University, Houston, TX 77030, USA; 6Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai 201210, China 7School of Agriculture and Environment, University of Western Australia, Perth, WA 6009, Australia †Biodiversity Institute, University of Kansas, Lawrence, KS 66045, USA * Corresponding Author: [email protected] bioRxiv preprint doi: https://doi.org/10.1101/2020.06.29.178392; this version posted January 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 1 ABSTRACT 2 Phenotypic plasticity enables an immediate response to changing conditions, but for most 3 species, evolutionary change through adaptation will be more important for long-term survival. 4 Warming climate and increasing desertification urges the identification of genes involved in 5 heat- and dehydration-tolerance to better inform and target biodiversity conservation efforts. 6 Comparisons among extant desert adapted species can highlight parallel or convergent patterns 7 of genome evolution through the identification of shared signatures of selection. We generate 8 chromosome-level genome assembly for the canyon mouse (Peromyscus crinitus) and test for 9 signature of parallel evolution by comparing signatures of selective sweeps across population- 10 level genomic resequencing data from another desert specialist deer mouse (P. eremicus) and 11 a widely-distributed habitat generalist (P. maniculatus), that may locally adapted to arid 12 conditions. We identify few shared candidate loci involved in desert adaptation and do not find 13 support for a shared pattern of parallel evolution. Instead, we hypothesize divergent molecular 14 mechanisms of desert adaptation among deer mice, potentially tied to species-specific historical 15 demography, which may limit or enhance adaptation. We identify a number of candidate loci 16 experiencing selective sweeps in the P. crinitus genome that are implicated in osmoregulation 17 (Trypsin, Prostasin) and metabolic regulation (Kallikrein, eIF2-alpha kinase GCN2, APPL1/2), 18 which may be important to accommodating hot and dry environmental conditions. 19 20 Key words: dehydration, desert, parallel evolution, Peromyscus, thermoregulation bioRxiv preprint doi: https://doi.org/10.1101/2020.06.29.178392; this version posted January 6, 2021. 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 4.0 International license. 21 INTRODUCTION 22 Increasing global temperatures and altered patterns of precipitation threaten biodiversity 23 worldwide (Moritz et al. 2008; Cahill et al. 2013; Urban 2015). Phenotypic plasticity enables an 24 immediate response to changing conditions but adaptation through evolutionary change will be 25 critical for the long-term survival of most species (Hoffman and Sgrò 2011; Cahill et al. 2013). 26 Range shifts upward in elevation and latitude have been documented in a number of terrestrial 27 species and interpreted as a response to warming (Chen et al. 2011; Tingley and Beissinger 28 2013; Freeman et al. 2018); however, responses vary even among closely-related species or 29 populations (Hoffman and Willi 2008; Moritz et al. 2008). Geographic range shifts are often 30 governed by the physiological limits of species, which are in part controlled by genetics and 31 have been shaped by neutral and selective evolutionary forces across many generations. 32 Population genomics methods enable genome-wide scans for selection to identify genes and 33 molecular pathways that may be involved in local adaptation (Bassham et al. 2018; Garcia- 34 Elfring et al. 2019). For species adapted to similar environments, parallel or convergent 35 evolution can be inferred if a greater number of genes or phenotypes share signatures of 36 selection than would be expected under a purely stochastic model of evolution (e.g., drift). The 37 same gene or suite of genes consistently tied to a specific adaptive phenotype across distantly 38 related taxa is consistent with a signal of convergent evolution. In contrast, for taxa that share a 39 recent common ancestor, signatures of selection at the same loci may reflect parallel selection 40 on either new mutations or shared ancestral variation or similar demographic histories, resulting 41 in the same phenotypic effect. Evidence of convergent or parallel evolution can highlight 42 common loci involved in shared adaptive phenotypes (Rundle et al. 2000; McDonald et al. 43 2009), while a lack of concerted evolution may identify idiosyncratic evolutionary strategies to 44 achieve the same phenotypic result. 45 As a model taxon (Dewey and Dawson 2001; Bedford and Hoekstra 2015) inhabiting 46 varied environments throughout North America, deer mice (genus Peromyscus) are a frequent bioRxiv preprint doi: https://doi.org/10.1101/2020.06.29.178392; this version posted January 6, 2021. 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 4.0 International license. 47 and productive subject of adaptation studies (e.g., physiological, Storz 2007; behavioral, Hu and 48 Hoekstra 2017; genetic, Cheviron et al. 2012; Storz and Cheviron 2016; Tigano et al. 2020). 49 Physiological similarity of deer mice to lab mice (Mus musculus) further broadens the 50 implications of evolutionary and ecological investigations of Peromyscus by linking to biomedical 51 sciences. The genus Peromyscus (N = 67 species; mammaldiversity.org) is hypothesized to be 52 the product of a rapid ecological radiation across North America (origin ~8 Mya, radiation ~5.71 53 Mya; Platt et al. 2015), evident in their varied ecological niches and rich species diversity 54 (Glazier 1980; Riddle et al. 2000; Bradley et al. 2007; Platt et al. 2015; Lindsey 2020). 55 Peromyscus display tremendous thermoregulatory plasticity and can be found in extreme 56 thermal environments, ranging from cold, high elevations (Pierce and Vogt 1993; Cheviron et al. 57 2012, 2014; Kaseloo et al. 2014; Garcia-Elfring et al. 2019) to arid, hot deserts (Riddle et al. 58 2000; MacManes 2017; Tigano et al. 2020). Thermoregulation and dehydration tolerance are 59 complex physiological traits, suggesting that several potential evolutionary routes could lead to 60 the same phenotypic outcome. Within this framework, comparisons among divergent 61 Peromyscus species adapted to similar environments may highlight shared adaptive 62 polymorphisms or disparate evolutionary paths central to achieving the same phenotype 63 (Cheviron et al. 2012; Ivy and Scott 2017; Hu and Hoekstra 2017; Storz et al. 2019). In cold 64 environments, endotherms rely on aerobic thermogenesis to maintain constant internal body 65 temperatures. Changes in both gene expression and the functional properties of proteins in deer 66 mice (P. maniculatus) adapted to high-altitude suggest that changes in multiple hierarchical 67 molecular pathways may be common in the evolution of complex physiological traits, such as 68 thermoregulation (Wichman and Lynch 1991; Storz 2007; Cheviron et al. 2012; Storz and 69 Cheviron 2016; Garcia-Elfring et al. 2019). Nonetheless, research focused on thermoregulatory 70 adaptations in high-elevation species may be confounded by concurrent selection on other traits 71 conferring fitness benefits, such as high hemoglobin oxygen-binding affinity (Storz and Kelly 72 2008; Storz et al. 2010; Natarajan et al. 2015), which is critically important given the low partial bioRxiv preprint doi: https://doi.org/10.1101/2020.06.29.178392; this version posted January 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license