Association of transcriptome-wide sequence variation with climate gradients in valley oak (Quercus lobata)

Abstract

A fundamental goal of evolutionary biology is to understand how environment shapes genetic variation through its effect on demographic processes and through natural selection. In non-model species, transcriptome sequencing generates large single nucleotide polymorphism (SNP) panels to disentangle these influences. Quercus lobata (valley oak) offers an excellent system for such analyses because it has stably occupied a climatically heterogeneous landscape throughout California. We used 220,427 diallelic SNPs from 22 individuals identified against a recently assembled reference transcriptome to (1) quantify transcriptome-wide associations of SNPs with climate indicative of demographic responses to climate, (2) identify SNPs especially associated with climate and thus potential targets of natural selection, and (3) test the hypothesis that genetic diversity is high in climate-adaptive candidate genes. Constrained ordinations (redundancy analysis) and variance partitioning showed that genetic structure in Q. lobata was explained by spatial location (49 %) and climate (24 %), especially minimum temperature and summer/spring precipitation balance, suggesting that climate influences neutral demographic processes and gene flow. After accounting for underlying structure, individual-based environmental association analyses identified 79 SNPs from 49 transcripts as candidates under natural selection by climate. These candidate genes had significantly higher SNP rates per base pair per locus (θ W), nucleotide diversity (π), and gene diversity (G) than non-candidate genes. These results provide preliminary support for the hypothesis that balancing selection maintains diversity in climate-adaptive genes. Climate has likely shaped both population demography and local adaptation in valley oak.