Adaptive evolution in a conifer hybrid zone is driven by a mosaic of recently introgressed and background genetic variants

Abstract

Extant conifer species may be susceptible to rapid environmental change owing to their long generation times, but could also be resilient due to high levels of standing genetic diversity. Hybridisation between closely related species can increase genetic diversity and generate novel allelic combinations capable of fuelling adaptive evolution. Our study unravelled the genetic architecture of adaptive evolution in a conifer hybrid zone formed between Pinus strobiformis and P. flexilis. Using a multifaceted approach emphasising the spatial and environmental patterns of linkage disequilibrium and ancestry enrichment, we identified recently introgressed and background genetic variants to be driving adaptive evolution along different environmental gradients. Specifically, recently introgressed variants from P. flexilis were favoured along freeze-related environmental gradients, while background variants were favoured along water availability-related gradients. We posit that such mosaics of allelic variants within conifer hybrid zones will confer upon them greater resilience to ongoing and future environmental change and can be a key resource for conservation efforts.

Variation in gene expression patterns across a conifer hybrid zone highlights the architecture of adaptive evolution under novel selective pressures

“…These hybrid populations experience severe drought, aseasonal frost and diurnal fluctuations in temperature (Adams & Kolb, 2004; Williams et al 2010). In agreement with theoretical models (Fisher, 1930), previous genotype-environment association studies in this system have demonstrated a dominance of many small effect loci driving adaptive evolution (Menon et al 2021). However, an understanding of how adaptive evolution proceeds under novel selective pressures is only beginning to be gathered in trees and across other systems.…”

“…However, drawing from our previous work(Menon et al 2021) and a likely wider environmental tolerance of P. flexilis than P. strobiformis (Windmuller-Campione & Long, 2016) we speculate that significant association between ancestry and survival only in BS is indicative of P. flexilis like variants enhancing survival in cooler environments. Overall, by using a space-for-time substitution study design and measuring several quantitative traits through transcriptomics, we…”

“…Following the ddRADseq library preparation detailed in Parchman et al (2013), we size selected 300-400 bp regions and performed single-end sequencing (1 × 150 bp) on Illumina HiSeq 4000 (Novogene Corporation). The resulting fastq files were processed using dDocent v.1.0 (Puritz et al 2014) to obtain genotype calls, as in Menon et al (2018, 2021). Following post-filtering steps implemented in VCFTOOLS v.0.1.153 (Danecek et al 2011) and custom functions implemented through python v.3 (Methods S2), we obtained 23,261 SNPs.…”

“…Population-level estimates of climate variables were obtained by averaging values across the three maternal trees selected per population. Following Menon et al (2021), we classified the environmental variables into drought- and freeze-associated variables, as these two axes are likely the primary selective agents across the hybrid zone populations. To reduce the dimensionality of the environmental dataset and avoid multicollinearity, we performed principal component analysis (PCA) separately for the drought and freeze associated variables and retained the PC axes that explained at least 90% of the variance as predictors in RDA.…”

Quantitative Disease Resistance to White Pine Blister Rust at Southwestern White Pine’s (Pinus strobiformis) Northern Range

“…The species thrives in mixed-conifer stands at mid to high elevations (Looney and Waring, 2012;Shirk et al, 2018) where it is moderately shadetolerant (Goodrich and Waring, 2017) and drought-tolerant (Bucholz et al, 2020), often occurring in sky islands. Within the northern extent of its range, P. strobiformis is part of a moving hybrid zone with Pinus flexilis (Menon et al, 2020) with some evidence of increased fitness due to introgressed alleles from P. flexilis (Menon et al, 2021).…”