Comparing phylogeographies to reveal incompatible geographical histories within genomes

Modern phylogeography aims at reconstructing the geographic movement of organisms based on their genomic sequences and spatial information. Phylogeographic approaches are often applied to pathogen sequences and therefore tend to neglect the possibility of recombination, which decouples the evolutionary and geographic histories of different parts of the genome. Genomic regions of recombining or reassorting pathogens often originate and evolve at different times and locations, which characterise their unique spatial histories. Measuring the extent of these differences requires new methods to compare geographic information on phylogenetic trees reconstructed from different parts of the genome. Here we develop for the first time a set of measures of phylogeographic incompatibility, aimed at detecting differences between geographical histories in terms of distances between phylogeographies. We study the effect of varying demography and recombination on phylogeographic incompatibilities using coalescent simulations. We further apply these measures to the evolutionary history of human and livestock pathogens, either reassorting or recombining, such as the Victoria and Yamagata lineages of influenza B and the O/ME-SA/Ind-2001 foot-and-mouth disease virus strain. Our results reveal diverse geographical paths of migration that characterise the origins and evolutionary histories of different viral genes and genomic segments. These incompatibility measures can be applied to any phylogeography, and more generally to any phylogeny where each tip has been assigned either a continuous or discrete “trait” independent of the sequence. We illustrate this flexibility with an analysis of the interplay between the phylogeography and phylolinguistics of Uralic-speaking human populations, hinting at patrilinear language transmission.

现代系统地理学（phylogeography）旨在基于生物的基因组序列与空间信息，重构其地理迁移历程。系统地理学方法常被应用于病原体序列分析，因此往往忽略了重组的可能性——重组会使基因组不同区域的演化历史与地理历史脱耦。发生重组或重配的病原体，其基因组区域往往在不同的时间与地点起源并演化，由此形成各自独特的空间历史特征。量化这类差异的程度，需要新的方法来比对基于基因组不同区域重构的系统发育（phylogenetic）树上的地理信息。本研究首次提出了一套系统地理学不相容性（phylogeographic incompatibility）量化指标，旨在通过系统地理学之间的距离来识别地理历史间的差异。本研究通过溯祖（coalescent）模拟实验，探究了不同种群动态与重组对系统地理学不相容性的影响。本研究进一步将该套指标应用于发生重组或重配的人类与家畜病原体演化历史分析，例如乙型流感病毒的Victoria系与Yamagata系，以及O/ME-SA/Ind-2001口蹄疫病毒毒株。研究结果揭示了多样的地理迁移路径，这些路径正是不同病毒基因与基因组片段的起源与演化历史的特征体现。这套不相容性指标可应用于任意系统地理学研究，更广泛地说，可应用于所有每个分支末端（tip）被赋予了独立于序列的连续或离散“性状（trait）”的系统发育分析。本研究以乌拉尔语系人群的系统地理学与系统语言学（phylolinguistics）之间的关联分析为例，展示了该方法的灵活性，结果暗示语言传播遵循父系传承模式。