Abstract
Temperature is a master environmental factor that limits the geographical distribution of species, especially in ectotherms. To address challenges in biodiversity conservation under ongoing climate change, it is essential to characterize relevant functional limitations and adaptive genomic content at population and species levels. Here, we present evidence for adaptive divergence in cardiac function and genomic regions in redband trout (Oncorhynchus mykiss gairdneri) populations from desert and montane streams. Cardiac phenotypes of individual fish were measured in the field with a custom‐built electrocardiogram apparatus. Maximum heart rate and its rate limiting temperature during acute warming were significantly higher in fish that have evolved in the extreme of a desert climate compared to a montane climate. Association mapping with 526,301 single nucleotide polymorphisms (SNPs) across the genome revealed signatures of thermal selection both within and among ecotypes. Among desert and montane populations, 435 SNPs were identified as putative outliers under natural selection and 20 of these loci showed significant association with average summer water temperatures among populations. Phenotypes for cardiac performance were variable within each ecotype, and 207 genomic regions were strongly associated with either maximum heart rate or rate limiting temperatures among individuals. Annotation of significant loci provided candidate genes that underlie thermal adaptation, including pathways associated with cardiac function (IRX5, CASQ1, CAC1D, and TITIN), neuroendocrine system (GPR17 and NOS), and stress response (SERPH). By integrating comparative physiology and population genomics, results here advance our knowledge on evolutionary processes of thermal adaptation in aquatic ectotherms.
Highlights
| INTRODUCTIONTemperature is a master environmental factor that influences the distribution and diversity of species
We sampled six populations of redband trout across diverse environmental conditions that ranged from hot desert, through cool montane to cold montane streams and measured cardiac function of individual fish during acute warming with a custom-built electrocardiogram (ECG) apparatus in the field
We identified candidate genomic regions for thermal adaptation among populations and those that were associated with phenotypic variation in fh,max within ecotypes
Summary
Temperature is a master environmental factor that influences the distribution and diversity of species. Studies that integrate both physiology (Farrell, 2016; Pörtner, Bock, & Mark, 2017; Somero, 2011) and population genomics (Allendorf, Hohenlohe, & Luikart, 2010; Franks & Hoffmann, 2012; Narum, Buerkle, Davey, Miller, & Hohenlohe, 2013) to elucidate mechanisms of thermal adaptation in natural ecosystems remain scarce. Thermal performance has been examined from animals acclimated in both laboratory (Chen, Farrell, Matala, & Narum, 2018; Narum, Campbell, Meyer, Miller, & Hardy, 2013) and field environments (Gamperl et al, 2002; Rodnick et al, 2004), but with limitations in the number of populations and physiological measurements. We sampled six populations of redband trout across diverse environmental conditions that ranged from hot desert, through cool montane to cold montane streams and measured cardiac function of individual fish during acute warming with a custom-built electrocardiogram (ECG) apparatus in the field. Adaptation in aquatic ectotherms by integrating comparative physiology and population genomic approaches
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