Phylogenomics and pervasive genome-wide phylogenetic discordance among fin whales (Balaenoptera physalus)

Phylogenomics has the power to uncover complex phylogenetic scenarios across the genome. In most cases, no single topology is reflected across the entire genome as the phylogenetic signal differs among genomic regions due to processes, such as introgression and incomplete lineage sorting. Baleen whales are among the largest vertebrates on Earth with a high dispersal potential in a relatively unrestricted habitat, the oceans. The fin whale (Balaenoptera physalus) is one of the most enigmatic baleen whale species, currently divided into four subspecies. It has been a matter of debate whether phylogeographic patterns explain taxonomic variation in fin whales. Here we present a chromosome-level whole genome analysis of the phylogenetic relationships among fin whales from multiple ocean basins. First, we estimated concatenated and consensus phylogenies for both the mitochondrial and nuclear genomes. The consensus phylogenies based upon the autosomal genome uncovered monophyletic clades associated with each ocean basin, aligning with the current understanding of subspecies division. Nevertheless, discordances were detected in the phylogenies based on the Y chromosome, mitochondrial, autosomal genome and X chromosome. Furthermore, we detected signs of introgression and pervasive phylogenetic discordance across the autosomal genome. This complex phylogenetic scenario could be explained by a puzzle of introgressive events, not yet documented in fin whales. Similarly, incomplete lineage sorting and a low phylogenetic signal could equally be the mechanisms leading to such phylogenetic discordances. Our study reinforces the pitfalls of relying on concatenated or single locus phylogenies to determine taxonomic relationships below the species level by illustrating the underlying nuances which some phylogenetic approaches may fail to capture. We emphasize the significance of accurate taxonomic delineation in fin whales by exploring crucial information revealed through genome-wide assessments.

系统基因组学 (Phylogenomics) 能够揭示全基因组范围内复杂的系统发育演化场景。多数情况下，全基因组不存在统一的系统发育拓扑结构——由于基因渐渗（introgression）、不完全谱系分选（incomplete lineage sorting）等演化过程，不同基因组区域的系统发育信号存在差异。须鲸是地球上体型最大的脊椎动物类群之一，在相对开放的海洋生境中具备极强的扩散能力。长须鲸（*Balaenoptera physalus*）是最具学术争议的须鲸物种之一，目前被划分为4个亚种。长须鲸的系统地理格局（phylogeographic patterns）能否解释其分类学变异，长期以来存在学术争议。本研究针对多个大洋盆地的长须鲸种群，开展了染色体级别的全基因组分析，以解析其系统发育关系。首先，我们分别基于线粒体基因组（mitochondrial genome）与核基因组（nuclear genome），构建了串联系统发育树与共识系统发育树。基于常染色体基因组（autosomal genome）构建的共识系统发育树显示，每个大洋盆地的长须鲸种群各自形成单系群（monophyletic clades），这与当前对长须鲸亚种划分的认知一致。然而，基于Y染色体、线粒体基因组、常染色体基因组与X染色体构建的系统发育树均存在拓扑结构冲突。此外，我们在全常染色体基因组中检测到了基因渐渗信号与广泛存在的系统发育拓扑冲突。这种复杂的系统发育演化场景，可由一系列尚未在长须鲸中被报道过的渐渗事件来解释。同理，不完全谱系分选与较弱的系统发育信号，同样可能是导致此类拓扑冲突的潜在机制。本研究通过揭示部分系统发育分析方法难以捕捉的演化细节，进一步印证了仅依赖串联序列或单基因座系统发育树来界定物种以下分类单元关系的局限性。本研究通过全基因组分析揭示的关键信息，强调了对长须鲸开展精准分类界定的重要意义。