Comparative and population genomics approaches reveal the basis of adaptation to deserts in a small rodent

Abstract

Organisms that live in deserts offer the opportunity to investigate how species adapt to environmental conditions that are lethal to most plants and animals. In the hot deserts of North America, high temperatures and lack of water are conspicuous challenges for organisms living there. The cactus mouse (Peromyscus eremicus) displays several adaptations to these conditions, including low metabolic rate, heat tolerance, and the ability to maintain homeostasis under extreme dehydration. To investigate the genomic basis of desert adaptation in cactus mice, we built a chromosome-level genome assembly and resequenced 26 additional cactus mouse genomes from two locations in southern California (USA). Using these data, we integrated comparative, population, and functional genomic approaches. We identified 16 gene families exhibiting significant contractions or expansions in the cactus mouse compared to 17 other Myodontine rodent genomes, and found 232 sites across the genome associated with selective sweeps. Functional annotations of candidate gene families and selective sweeps revealed a pervasive signature of selection at genes involved in the synthesis and degradation of proteins, consistent with the evolution of cellular mechanisms to cope with protein denaturation caused by thermal and hyperosmotic stress. Other strong candidate genes included receptors for bitter taste, suggesting a dietary shift towards chemically defended desert plants and insects, and a growth factor involved in lipid metabolism, potentially involved in prevention of dehydration.Understanding how species adapted to deserts will provide an important foundation for predicting future evolutionary responses to increasing temperatures, droughts and desertification in the cactus mouse and other species. K E Y W O R D Sbitter taste receptor, hyperosmotic stress, Peromyscus eremicus, ribosomal protein, selective sweeps, thermal stress | 1301 TIGANO eT Al.

Comparative genomic analysis of sifakas ( Propithecus ) reveals selection for folivory and high heterozygosity despite endangered status

“…The rapid evolution of ribosomal proteins, as well as other gene families involved in translation and proteome maintenance, is of potential interest as these families have been found to show rapid evolution in desert- and/or heat-adapted animal species ( 104 , 105 ). High temperatures can disrupt transcription and translation and cause the denaturation and degradation of proteins ( 106 ).…”

A linked‐read approach to museomics: Higher quality de novo genome assemblies from degraded tissues

“…Following broad application of single-and multilocus investigations (Hickerson et al, 2010), high-throughput sequencing methods have further increased our ability to interrogate historical archives molecularly and to address a variety of evolutionary questions at increased resolution. The growing field of museomics (Bi et al, 2013;Schmitt, Cook, Zamudio, & Edwards, 2018) continues to explore the tree of life (Guschanski et al, 2013;Teeling & Hedges, 2013), elucidate early human histories (Green et al, 2010;Meyer et al, 2012) and identify evolutionary adaptations of nonmodel species (Cheviron & Brumfeld, 2012;Jones, Mills, Jensen, & Good, 2019;Tigano, Colella, & MacManes, 2020 Although the contiguity and completeness of linked-read assemblies depend on DNA integrity, linked-read methods may be especially useful to build genome assemblies for rare or extinct species, or when the collection of new material is difficult or impossible (Payne & Sorenson, 2002) due to the conservation status or geographical location (e.g., international) of the target species. As new or higher-quality tissue samples will never again be available for extinct species, linked-reads may be the best currently available option F I G U R E 1 Maximum-likelihood phylogeny of the four new linked-read Peromyscus genome assemblies, three publicly available Peromyscus assemblies and five outgroup assemblies within Rodentia.…”

Limited Evidence for Parallel Evolution Among Desert-AdaptedPeromyscusDeer Mice

“…As a model taxon inhabiting varied environments throughout North America ( Dewey and Dawson 2001 ; Bedford and Hoekstra 2015 ), deer mice (genus Peromyscus ) are a frequent and productive subject of adaptation studies (e.g., physiological, Storz 2007 ; behavioral, Hu and Hoekstra 2017 ; genetic, Cheviron et al 2012 ; Storz and Cheviron 2016 ; Tigano et al 2020 ). The physiological similarity of deer mice to house mice ( Mus musculus ), a well-studied biomedical model, further broadens the implications of evolutionary and ecological investigations of Peromyscus by linking results to biomedical sciences.…”

“…The genus Peromyscus ( N = 67 species; mammaldiversity.org ) is hypothesized to be the product of rapid ecological radiation across North America (origin ~8 Mya, radiation ~5.71 Mya; Platt et al 2015 ), evident in their varied ecological niches and rich species diversity ( Glazier 1980 ; Riddle et al 2000 ; Bradley et al 2007 ; Platt et al 2015 ; Lindsey 2020 ). Peromyscus display tremendous thermoregulatory plasticity and can be found in extreme thermal environments, ranging from cold, high elevations ( Pierce and Vogt 1993 ; Cheviron et al 2012 , 2014 ; Kaseloo et al 2014 ; Garcia-Elfring et al 2019 ) to arid, hot deserts ( Riddle et al 2000 ; MacManes 2017 ; Tigano et al 2020 ). Thermoregulation and dehydration tolerance are complex physiological traits, suggesting that several potential evolutionary routes could lead to the same phenotypic outcome.…”

“…Locally adapted desert populations of P. maniculatus (subspecies P. m. sonoriensis ) in the American Southwest, however, may exhibit patterns of selection similar to that of desert specialists, either through the parallel selective retention of functional ancestral polymorphisms or convergent selection on new mutations. Whole-genome assemblies are publicly available for both P. eremicus (PRJEB33593, ERZ119825; Tigano et al 2020 ) and P. maniculatus (GCA_003704035.1), which positions these species as ideal comparatives against P. crinitus to identify genes and regulatory regions associated with desert adaptation, including those unique to desert specialists P. eremicus and P. crinitus.…”