Speciation network in Laurasiatheria: retrophylogenomic signals

Rapid species radiation due to adaptive changes or occupation of new ecospaces challenges our understanding of ancestral speciation and the relationships of modern species. At the molecular level, rapid radiation with successive speciations over short time periods—too short to fix polymorphic alleles—is described as incomplete lineage sorting. Incomplete lineage sorting leads to random fixation of genetic markers and hence, random signals of relationships in phylogenetic reconstructions. The situation is further complicated when you consider that the genome is a mosaic of ancestral and modern incompletely sorted sequence blocks that leads to reconstructed affiliations to one or the other relative, depending on the fixation of their shared ancestral polymorphic alleles. The laurasiatherian relationships among Chiroptera, Perissodactyla, Cetartiodactyla, and Carnivora present a prime example for such enigmatic affiliations. We performed whole-genome screenings for phylogenetically diagnostic retrotransposon insertions involving the representatives bat (Chiroptera), horse (Perissodactyla), cow (Cetartiodactyla), and dog (Carnivora), and extracted among 162,000 preselected cases 102 virtually homoplasy-free, phylogenetically informative retroelements to draw a complete picture of the highly complex evolutionary relations within Laurasiatheria. All possible evolutionary scenarios received considerable retrotransposon support, leaving us with a network of affiliations. However, the Cetartiodactyla–Carnivora relationship as well as the basal position of Chiroptera and an ancestral laurasiatherian hybridization process did exhibit some very clear, distinct signals. The significant accordance of retrotransposon presence/absence patterns and flanking nucleotide changes suggest an important influence of mosaic genome structures in the reconstruction of species histories.

由适应性演化或开拓新生态空间驱动的快速物种辐射（rapid species radiation），正对我们解析祖先物种形成过程与现生物种间的演化亲缘关系构成挑战。在分子层面，短时间内连续发生物种形成且时长不足以固定多态等位基因的快速辐射演化，被定义为不完全谱系分选（incomplete lineage sorting）。不完全谱系分选会引发遗传标记的随机固定，进而在系统发育重建中产生随机的物种亲缘关系信号。若考虑到基因组是由祖先与现代的不完全分选序列片段构成的镶嵌体，这一情形将更为复杂：这类基因组镶嵌体可依据共享祖先多态等位基因的固定情况，使系统发育重建将物种归类至不同的近缘类群中。翼手目（Chiroptera）、奇蹄目（Perissodactyla）、鲸偶蹄目（Cetartiodactyla）与食肉目（Carnivora）之间的劳亚兽总目（Laurasiatheria）亲缘关系，正是这类难以厘清的类群归属的典型范例。本研究以翼手目代表物种蝙蝠、奇蹄目代表物种马、鲸偶蹄目代表物种牛以及食肉目代表物种犬为研究对象，开展了全基因组水平的系统发育诊断性反转录转座子（retrotransposon）插入位点筛选；在162000个预先筛选出的候选位点中，我们最终提取得到102个几乎无同塑性、具备系统发育信息价值的反转录转座子标记，以完整解析劳亚兽总目内高度复杂的演化关系。所有可能的演化场景均获得了反转录转座子标记的显著支持，最终得到了一张类群亲缘关系的网状图谱。然而，鲸偶蹄目与食肉目的亲缘关系、翼手目的基部演化位置，以及劳亚兽总目祖先的杂交演化过程，均呈现出极为明确且清晰的信号。反转录转座子的存在/缺失模式与其侧翼核苷酸序列变异之间的高度一致性，表明基因组镶嵌结构对物种演化历史的重建具有重要影响。