Combined genotype and phenotype analyses reveal patterns of genomic adaptation to local environments in the subtropical oak Quercus acutissima

Jie Gao,Zhi‐Long Liu,Qing‐Yin Zeng,Wei Zhao,Kyle W Tomlinson,Shang‐Wen Xia,Jin Chen,Xiao‐Ru Wang

doi:10.1111/jse.12568

Abstract

AbstractUnderstanding the effects of the demographic dynamics and environmental heterogeneity on the genomic variation of forest species is important, not only for uncovering the evolutionary history of the species, but also for predicting their ability to adapt to climate change. In this study, we combined a common garden experiment with range‐wide population genomics analyses to infer the demographic history and characterize patterns of local adaptation in a subtropical oak species, Quercus acutissima (Carruthers). We scanned approximately 8% of the oak genome using a balanced representation of both genic and non‐genic regions and identified a total of 55 361 single nucleotide polymorphisms (SNPs) in 167 trees. Genomic diversity analyses revealed an east–west split in the species distribution range. Coalescent‐based model simulations inferred a late Pleistocene divergence in Q. acutissima between the east and west groups as well as subsequent preglaciation population expansion events. Consistent with observed genetic differentiation, morphological traits also showed east–west differentiation and the biomass allocation in seedlings was significantly associated with precipitation. Environment was found to have a significant and stronger impact on the non‐neutral than the neutral SNPs, and also significantly associated with the phenotypic differentiation, suggesting that, apart from the geography, environment had played a role in determining non‐neutral and phenotypic variation. Our approach, which combined a common garden experiment with landscape genomics data, validated the hypothesis of local adaptation of this long‐lived oak tree of subtropical China. Our study joins the small number of studies that have combined genotypic and phenotypic data to detect patterns of local adaptation.

Highlights

Detecting signatures of adaptation across conspecific populations is important for understanding both the genetic basis of adaptation to the local environment and the potential effects of climate change on species (Savolainen et al, 2013; Prunier et al, 2016; Yeaman et al, 2016)
Adaptive phenotypic traits are usually controlled by multiple genes, each with small effects spread across the genome (Le Corre & Kremer, 2012; Hendry, 2013)
We sampled approximately 8% of the oak genome, a higher degree of coverage than other genetic studies on oak species undertaken to date (e.g., Eation et al, 2015; Deng et al, 2018; Ortego et al, 2018; Pina‐Martins et al, 2019)

Summary

Introduction

Detecting signatures of adaptation across conspecific populations is important for understanding both the genetic basis of adaptation to the local environment and the potential effects of climate change on species (Savolainen et al, 2013; Prunier et al, 2016; Yeaman et al, 2016). Natural selection acts initially on phenotypic traits, over time resulting in changes of allele frequencies at the specific genetic loci underlying those traits and leading to locally adapted populations (Orsini et al, 2013). Tree species are of particular interest for research on local.

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