Genome-wide shifts in climate-related variation underpin responses to selective breeding in a widespread conifer

AbstractLocally adapted temperate tree populations exhibit genetic trade-offs among climate-related traits that can be exacerbated by selective breeding, and are challenging to manage under climate change. To inform climatically adaptive forest management, we investigated the genetic architecture and impacts of selective breeding on four climate-related traits in 105 natural and 20 selectively bred lodgepole pine populations from western Canada. Growth, cold injury and growth initiation and growth cessation phenotypes were tested for associations with 18,600 SNPs in natural populations to identify ‘positive effect alleles’ (PEAs). The effects of artificial selection for faster growth on PEA frequencies for each trait were quantified in breeding populations from different climates. Substantial shifts in PEA proportions and frequencies were observed across many loci after two generations of selective breeding for height, and responses of phenology-associated PEAs differed strongly among climatic regions. Extensive genetic overlap was evident among traits. Alleles most strongly associated with greater height were often also associated with greater cold injury and delayed phenology, although it is unclear whether potential trade-offs arose directly from pleiotropy or indirectly via genetic linkage. Modest variation among populations in PEA frequencies across many loci was associated with large phenotypic differences and strong climatic gradients, providing support for assisted gene flow polices. Relationships among genotypes, phenotypes and climate in natural populations were maintained or strengthened by selective breeding. However, future adaptive phenotypes and assisted gene flow may be compromised if selective breeding further increases the PEA frequencies of SNPs involved in adaptive trade-offs among climate-related traits., Usage notesAll usage notes are contained within the accompanying README.txt file, and comments within the analyses scripts supplied.摘要 本地适应性温带树木种群在气候相关性状间存在遗传权衡，这种权衡可因选择性育种而加剧，在气候变化背景下其管理颇具挑战。为支撑气候适应性森林管理，我们对加拿大西部105个天然种群和20个选择性育种种群的扭叶松（lodgepole pine）开展研究，解析了4个气候相关性状的遗传结构以及选择性育种对其的影响。针对天然种群，我们检测了生长、冷害、生长启动与生长停止表型与18600个单核苷酸多态性（Single Nucleotide Polymorphisms, SNPs）的关联，以鉴定正效应等位基因（positive effect alleles, PEAs）。针对不同气候来源的育种种群，我们量化了速生人工选择对各性状正效应等位基因频率的影响。经过两代针对树高的选择性育种后，多个基因座上的正效应等位基因比例与频率均发生显著变化，且与物候相关的正效应等位基因的响应在不同气候区域间差异显著。不同性状间存在广泛的遗传重叠现象：与更高树高强相关的等位基因往往同时与更严重的冷害以及物候延迟相关，尽管目前尚不清楚这种潜在的权衡是直接由多效性（pleiotropy）引起，还是通过遗传连锁间接产生。多个基因座上的正效应等位基因频率在种群间存在小幅差异，但这种差异与显著的表型差异和强烈的气候梯度相关，为辅助基因流（assisted gene flow）政策提供了支持依据。天然种群中基因型、表型与气候之间的关联在选择性育种后得以保留甚至增强。但如果选择性育种进一步提高了参与气候相关性状间适应性权衡的单核苷酸多态性的正效应等位基因频率，则未来的适应性表型与辅助基因流可能会受到损害。 使用说明 所有使用说明均详见随附的README.txt文件以及所提供分析脚本中的注释内容。