Limited Evidence for Parallel Evolution Among Desert-AdaptedPeromyscusDeer Mice

Abstract

Warming climate and increasing desertification urges the identification of genes involved in heat- and dehydration-tolerance to better inform and target biodiversity conservation efforts. Comparisons among extant desert adapted species can highlight parallel or convergent patterns of genome evolution through the identification of shared signatures of selection. We generate chromosome-level genome assembly for the canyon mouse (Peromyscus crinitus) and test for signature of parallel evolution by comparing signatures of selective sweeps across population-level genomic resequencing data from another desert specialist deer mouse (P. eremicus) and a widely-distributed habitat generalist (P. maniculatus), that may be locally adapted to arid conditions. We identify few shared candidate loci involved in desert adaptation and do not find support for a shared pattern of parallel evolution. Instead, we hypothesize divergent molecular mechanisms of desert adaptation among deer mice, potentially tied to species-specific historical demography, which may limit or enhance adaptation. We identify a number of candidate loci experiencing selective sweeps in the P. crinitus genome that are implicated in osmoregulation (Trypsin, Prostasin) and metabolic regulation (Kallikrein, eIF2-alpha kinase GCN2, APPL1/2), which may be important to accommodating hot and dry environmental conditions.

Chromosome size affects sequence divergence between species through the interplay of recombination and selection

“…Although rodents of the genus Peromyscus look similar to Mus mice in appearance and have similar genome sizes, they last shared a common ancestor with Mus ~25 million years ago (Steppan et al 2004) and have very karyotypically stable genomes (2n=48; Smalec et al 2019), even more so than great apes. As a rodent lineage with increasing genomic resources (Colella et al 2020;Tigano et al 2020;Colella et al 2021) and conserved genome structure, Peromyscus offers similarities and contrasts to both the Mus and the great apes lineages, thus representing an ideal third clade to understanding the role of genome structure stability and the relationships between chromosome size, recombination, diversity, and divergence in mammals. For example, similar to the great apes (Hellman et al 2003) but contrasting with M. musculus, the cactus mouse (Peromyscus eremicus) shows a strong inverse correlation between chromosome size and π (Tigano et al 2020); conserved synteny, recombination rates, and crossover patterning among Peromyscus species (Peterson et al 2019;Smalec et al 2019) together suggest that this relationship between chromosome size and π may be common among species in this genus.…”

Life in Deserts: The Genetic Basis of Mammalian Desert Adaptation

“…Similar methods on hot-desert fat-tail sheep breeds and goats (Capra hircus) identified many candidate regions spanning genes and/or pathways significantly enriched for fat metabolism, insulin signaling, kidney function, oxidative stress and DNA repair, response to heat and UV radiation, body size development, and melanogenesis [17,20]. Species of the genus Peromyscus have also been used in case studies in population genomics as examples of rapid environmental/ecological differentiation [18,21]. Different arid-dwelling species repeatedly evolved during the radiation of the genus in North America.…”

“…Several studies of different desert mammals have identified genes, and functional classes of genes and pathways, involved in fat metabolism [17,21,32,39,55], thyroid-induced metabolism [12], salt metabolism and prevention of high blood pressure [13,16,34], insulin signaling Box 1. Endurer-Evader-Evaporator Concept Aiming to summarize and categorize decades of classic literature on desert adaptations in species occupying distinct ecological niches, Willmer et al [2] proposed a classification system relative to extreme temperatures and body size.…”

“…However, some authors have criticized this categorization due to overlap between the categories and have proposed other frameworks to synthesize desert mammalian phenotypic adaptations (e.g., [6]). Water Increased vasopressin En (1,8), Ev (1,6,10) ; Increased aldosterone En (1,3,4), Ev (3,4) Increased urine osmolality/Increased water reabsorption from the kidney En (1,2), Ev, Evap (1,4) ; decreased urine production Ev (1,5,7) Reduced aldosterone En (1) Increased urine sodium excretion En (1) Low glomerular filtration rate En (1,3), Ev (2,5,7) Higher levels of plasma creatinine with no apparent kidney damage or renal impairment En (1,2), Ev (5,7) Higher urea En (1,2), Ev (5,7) , glucose En (1,7), potassium Ev (7) , sodium En (1) , and chloride Ev (5,7) Increased plasma osmolality En (1,2), Ev (1, 5,7,10), Evap (5) Food/water Increased fat storage in body tissues En (1,7,7 ,4) Energy reservation during food/water scarcity Fat metabolism En (1,2,4,7), Ev (13,14) Enhanced use of metabolic water En (1,2,7), Ev (1,2,8, 12,13,14), Evap (1,2) Higher plasma sodium En (1) Tolerance of high-salt diet En (1,6,7 ), Ev (1,4,8,9), Evap (5) Decreased insulin secretion without diabetes Ev (1) Adaptive tolerance to dehydration and starvation [ 17,21,32,…”

“…The major mechanisms shared across mammals relate to phenotypes that have been associated with adaptation to starvation and dehydration, as well as water retention at the kidney. For instance, the highest overlap is in functional classes of genes associated with fat storage and fat metabolism, including genes that affect energy expenditures, and/or cold-and diet-induced thermogenesis [17,21,32,39,55]. Changes in genes involved in fat metabolism may relate to diverse adaptive phenotypes that result in adaptive tolerance to heat/cold (through regulation of energy expenditures and thermogenesis), dehydration (through enhanced use of metabolic water from fat) and food scarcity (energy stored in localized fat) [5,6] (Figure 1D).…”