Multi-locus genomic signatures of local adaptation to snow across the landscape in California populations of a willow leaf beetle

Abstract

Organisms living in mountains contend with extreme climatic conditions, including short growing seasons and long winters with extensive snow cover. Anthropogenic climate change is driving unprecedented, rapid warming of montane regions across the globe, resulting in reduced winter snowpack. Loss of snow as a thermal buffer may have serious consequences for animals overwintering in soil, yet little is known about how variability in snowpack acts as a selective agent in montane ecosystems. Here, we examine genomic variation in California populations of the leaf beetle Chrysomela aeneicollis, an emerging natural model system for understanding how organisms respond to climate change. We used a genotype-environment association approach to identify genomic signatures of local adaptation to microclimate in populations from three montane regions with variable snowpack and a coastal region with no snow. We found that both winter-associated environmental variation and geographical distance contribute to overall genomic variation across the landscape. We identified non-synonymous variation in novel candidate loci associated with cytoskeletal function, ion transport and membrane stability, cellular processes associated with cold tolerance in other insects. These findings provide intriguing evidence that variation in snowpack imposes selective gradients in montane ecosystems.

Keywords: climate change; cold tolerance; insect; landscape genomics; local adaptation; winter.

Figure 1.

Genetic differentiation and structure of Chrysomela aeneicollis populations across California. (a) Map of study populations. Abbreviation in parentheses refers to population ecoregion (SN, Sierra Nevada; CB, Central Basin; EC, Eastern Cascades; CR, Coast Range). Inset map features the sampled populations located in the Sierra Nevada and Central Basin ecoregions. Populations in the Sierra Nevada ecoregion are presented using a blue colour gradient and are ordered based by latitude, south to north representing increasing latitude. (b) PCA ordination highlighting genomic differentiation among populations based on the minor allele frequencies. (c) Stacked barplots for each individual (N = 175 total) indicate estimated ancestry coefficients, representing the posterior probability that an individual originates from K = 5 ancestral gene pools. Colours below the stacked barplot indicate each individual's a priori population designations, as shown in (a,b). Two-letter population designations are described in table 1.

Figure 2.

Genomic differentiation as a function of geographical distance and habitat type for California willow beetle populations. Data shown highlight the relationship between pairwise geographical distance (kilometres) and pairwise genetic distance (F_st). The black lines indicate the fitted values from the ANCOVA model, and points are colour coded by the categorical independent variable used in the ANCOVA model.

Figure 3.

Partial redundancy analysis (pRDA) identifies candidate loci associated with selective climatic gradients. (a) Ordination of populations and environmental variable loadings in multivariate space. Environmental variable loadings are multiplied by 10 to improve visualization. (b) Ordination of SNP loci and environmental variable loadings in multivariate space. Outlier loci are coloured based on correlation with an environmental variable (Pearson's r > |0.65|). Environmental variable loadings are multiplied by 0.4 to improve visualization. Two-letter population designations are described in table 1. Results of pRDA with only montane populations are provided in electronic supplementary material, figure S7.

Figure 4.

Latent factor mixed model (LFMM) identifies candidate loci associated with selective climatic gradients. Points indicate the FDR-adjusted p-value (q-value) of the association between a locus and an environmental gradient. The dotted black line represents a q-value of 0.05, and purple and red coloured loci are those detected by the pRDA. (a) Loci associations with annual air temperature range. (b) Loci associations with maximum daily snowfall. Results of LFMM with only montane populations are provided in electronic supplementary material, figure S8.