Gene flow and an anomaly zone complicate phylogenomic inference in a rapidly radiated avian family (Prunellidae)

BackgroundResolving the phylogeny of rapidly radiating lineages presents a challenge when building theTree of Life. An Old World avian family Prunellidae (Accentors) comprises twelve species that rapidly diversified at the Pliocene-Pleistocene boundary.ResultsHere we investigate the phylogenetic relationships of all species of Prunellidae using a chromosome-level de novo assembly of Prunella strophiata and 36 high-coverage resequenced genomes. We use homologous alignments of thousands of exonic and intronic loci to build the coalescent and concatenated phylogenies and recover four different species trees. Topology tests show a large degree of gene tree-species tree discordance but only 40-54%% of intronic gene trees and 36-75% of exonic genic trees can be explained by incomplete lineage sorting and gene tree estimation errors. Estimated branch lengths for three successive internal branches in the inferred species trees suggest the existence of an empirical anomaly zone. The most common topology recovered for species in this anomaly zone was not similar to any coalescent or concatenated inference phylogenies, suggesting presence of anomalous gene trees. However, this interpretation is complicated by the presence of gene flow because extensive introgression was detected among these species. When exploring tree topology distributions, introgression, and regional variation in recombination rate, we find that many autosomal regions contain signatures of introgression and thus may mislead phylogenetic inference. Conversely, the phylogenetic signal is concentrated to regions with low-recombination rate, such as the Z chromosome, which are also more resistant to interspecific introgression.ConclusionsCollectively, our results suggest that phylogenomic inference should consider the underlying genomic architecture to maximize the consistency of phylogenomic signal.

背景：解析快速辐射类群的系统发育（phylogeny）关系，是构建生命之树（Tree of Life）过程中面临的核心挑战之一。旧大陆鸟类类群岩鹨科（Prunellidae，岩鹨Accentors）包含12个物种，这些物种在上新世-更新世交界发生了快速辐射分化。
结果：本研究针对岩鹨科所有物种的系统发育关系展开探究：首先完成了棕胸岩鹨（Prunella strophiata）的染色体水平从头组装（de novo assembly）基因组，并结合36份高覆盖度重测序基因组开展分析。本研究借助数千个外显子与内含子位点的同源序列比对，分别构建溯祖法与串联法系统发育树，最终得到4种互不相同的物种树拓扑结构。拓扑检验结果显示，基因树与物种树间存在广泛的拓扑冲突，但仅有40%~54%的内含子基因树与36%~75%的外显子基因树可通过不完全谱系分选（Incomplete Lineage Sorting, ILS）与基因树估算误差得到合理解释。对推断物种树中3个连续内部分支的分支长度进行估算后发现，该类群系统发育存在一处经验异常区（empirical anomaly zone）。该异常区内物种所对应的最常见拓扑结构，与所有溯祖法或串联法推断得到的系统发育树均无相似性，提示存在异常基因树（anomalous gene trees）。但由于在这些物种间检测到广泛的基因流（gene flow）与基因渐渗（introgression），该结论的解释性变得更为复杂。在探究拓扑结构分布、基因渐渗与重组率（recombination rate）的区域异质性时，本研究发现众多常染色体（autosomal）区域均携带基因渐渗的特征信号，因而可能对系统发育推断产生误导。与之相反，系统发育信号则富集于低重组率区域，例如Z染色体（Z chromosome），这类区域同样更能抵御种间基因渐渗。
结论：综上，本研究结果表明，系统发育组学（phylogenomic）推断应充分考量基因组的基础结构特征，以最大化系统发育组学信号的一致性。