the great tit HapMap project: a continental-scale analysis of genomic variation in a songbird

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographic range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugiam, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear “islands of differentiation”, even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species’ range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.

Methods
Genotype data was obtained by typing great tit blood samples collected by a research consortium, mostly from around Europe. Genotyping was performed on an Affymetrix high density SNP chip. Data were converted to Plink format, and from those Plink files various population genetic analyses were performed. All of the scripts are available on GitHub at https://github.com/lgs85/SpurginBosse_Hapmap/tree/main.

A manuscript describing the work has been submitted to Molecular Ecology Resources.

进化生物学的核心目标之一，是解析类群内部以及空间尺度下基因组多样性格局的变异成因。针对广布物种开展的大规模基因组研究，有助于探究环境与种群历史如何塑造基因组分化格局。本研究描述了迄今为止针对野生脊椎动物开展的地理覆盖最全面的基因组变异调查之一——大山雀（Parus major）HapMap计划。我们对覆盖约30个纬度跨度、40个经度跨度的29个种群的647份个体样本，筛选了约50万个单核苷酸多态性（Single Nucleotide Polymorphism, SNP）标记。该采样范围几乎涵盖了该物种欧洲亚种的全部地理分布范围。
全基因组变异模式与东南欧避难所种群近期向欧洲全境扩散的假说一致，岛屿种群中存在瓶颈效应与遗传多样性降低的特征。全基因组范围内的分化水平呈现高度异质性，即便在全基因组分化水平极低的种群之间，也存在清晰的“分化岛”区域。局部低重组率是局部高基因组固定指数（Fixation Index, FST）的强预测因子，这一效应在岛屿种群与大陆边缘种群中尤为显著，表明遗传漂变与重组的相互作用塑造了高度异质的基因组分化景观。
我们还检测到仅分布于一个或多个边缘大山雀种群的基因组异常区域，这大概率是物种分布边界近期受到定向选择的结果。基于单倍型的选择检测指标与重组率存在关联（尽管关联强度较弱），并揭示了可能由正向选择导致的种群特异性选择性清除事件。
本研究凸显了对野生生物开展全面基因组变异筛查，能够为时空尺度下的进化动力学提供独特的研究视角。

方法
本研究的基因型数据来源于某研究联盟采集的大山雀血液样本，样本主要采集自欧洲各地。基因分型实验采用Affymetrix高密度单核苷酸多态性芯片完成。原始数据被转换为Plink格式，并基于该格式文件开展了各类群体遗传学分析。所有分析脚本已上传至GitHub仓库：https://github.com/lgs85/SpurginBosse_Hapmap/tree/main。
描述本研究的学术论文已提交至《Molecular Ecology Resources》期刊。