Animal Ecology, Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 D, 752 36 Uppsala, Sweden.
Department of Medical Biochemistry and Microbiology, Uppsala University, 751 23 Uppsala, Sweden.
Syst Biol. 2024 May 27;73(1):12-25. doi: 10.1093/sysbio/syad062.
Instances of parallel phenotypic evolution offer great opportunities to understand the evolutionary processes underlying phenotypic changes. However, confirming parallel phenotypic evolution and studying its causes requires a robust phylogenetic framework. One such example is the "black-and-white wagtails," a group of 5 species in the songbird genus Motacilla: 1 species, Motacilla alba, shows wide intra-specific plumage variation, while the 4r others form 2 pairs of very similar-looking species (M. aguimp + M. samveasnae and M. grandis + M. maderaspatensis, respectively). However, the 2 species in each of these pairs were not recovered as sisters in previous phylogenetic inferences. Their relationships varied depending on the markers used, suggesting that gene tree heterogeneity might have hampered accurate phylogenetic inference. Here, we use whole genome resequencing data to explore the phylogenetic relationships within this group, with a special emphasis on characterizing the extent of gene tree heterogeneity and its underlying causes. We first used multispecies coalescent methods to generate a "complete evidence" phylogenetic hypothesis based on genome-wide variants, while accounting for incomplete lineage sorting (ILS) and introgression. We then investigated the variation in phylogenetic signal across the genome to quantify the extent of discordance across genomic regions and test its underlying causes. We found that wagtail genomes are mosaics of regions supporting variable genealogies, because of ILS and inter-specific introgression. The most common topology across the genome, supporting M. alba and M. aguimp as sister species, appears to be influenced by ancient introgression. Additionally, we inferred another ancient introgression event, between M. alba and M. grandis. By combining results from multiple analyses, we propose a phylogenetic network for the black-and-white wagtails that confirms that similar phenotypes evolved in non-sister lineages, supporting parallel plumage evolution. Furthermore, the inferred reticulations do not connect species with similar plumage coloration, suggesting that introgression does not underlie parallel plumage evolution in this group. Our results demonstrate the importance of investing genome-wide patterns of gene tree heterogeneity to help understand the mechanisms underlying phenotypic evolution. [Gene tree heterogeneity; incomplete lineage sorting; introgression; parallel evolution; phylogenomics; plumage evolution; wagtails.].
平行表型进化的实例为理解表型变化背后的进化过程提供了极好的机会。然而,确认平行表型进化并研究其原因需要一个稳健的系统发育框架。一个这样的例子是“黑白燕雀”,雀形目燕雀属的 5 个物种:1 个物种,白腰文鸟,表现出广泛的种内羽毛变异,而其他 4 个形成了 2 对非常相似的物种(M. aguimp + M. samveasnae 和 M. grandis + M. maderaspatensis,分别)。然而,这两对中的两个物种在之前的系统发育推断中并没有被归为姐妹种。它们的关系因所使用的标记而异,这表明基因树异质性可能阻碍了准确的系统发育推断。在这里,我们使用全基因组重测序数据来探索该组内的系统发育关系,特别强调了基因树异质性的程度及其潜在原因。我们首先使用多物种聚合法生成基于全基因组变异的“完整证据”系统发育假设,同时考虑不完全谱系分选(ILS)和基因渗入。然后,我们研究了基因组中系统发育信号的变化,以量化基因组区域之间的分歧程度,并检验其潜在原因。我们发现,燕尾基因组是支持可变系统发育的区域的马赛克,这是由于 ILS 和种间基因渗入。在整个基因组中最常见的拓扑结构,支持 M. alba 和 M. aguimp 作为姐妹种,似乎受到了古老基因渗入的影响。此外,我们推断出另一个古老的基因渗入事件,发生在 M. alba 和 M. grandis 之间。通过结合来自多个分析的结果,我们提出了一个黑白燕雀的系统发育网络,该网络证实了相似的表型在非姐妹谱系中进化,支持了羽毛颜色的平行进化。此外,推断的网状结构并没有将具有相似羽毛颜色的物种连接起来,这表明在该组中,基因渗入并不是平行羽毛进化的基础。我们的研究结果表明,投资于全基因组基因树异质性模式对于帮助理解表型进化背后的机制非常重要。