Data from: Introgression underlies phylogenetic uncertainty but not parallel plumage evolution in a recent songbird radiation

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 five species in the songbird genus
Motacilla: one species, the White Wagtail (M. alba), shows wide
intra-specific plumage variation, while the four others form two pairs of
very similar-looking species (African Pied Wagtail M. aguimp + Mekong
Wagtail M. samveasnae and Japanese Wagtail M. grandis + White-browed
Wagtail M. maderaspatensis, respectively). However, the two 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 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
investigation of genome-wide patterns of gene tree heterogeneity to help
understanding the mechanisms underlying phenotypic evolution.

平行表型进化（parallel phenotypic evolution）的实例为理解表型变化背后的演化过程提供了绝佳契机。然而，要验证平行表型进化并探究其成因，需要构建可靠的系统发育框架（phylogenetic framework）。其中一个典型案例便是“黑白鹡鸰”类群：该类群隶属于鹡鸰属（Motacilla），包含5个物种——其中白鹡鸰（M. alba）种内羽色变异丰富，其余4个物种则组成两对形态极为相似的类群：分别为非洲斑鹡鸰（M. aguimp）与湄公鹡鸰（M. samveasnae），以及日本鹡鸰（M. grandis）与白眉鹡鸰（M. maderaspatensis）。不过，过往的系统发育推断并未将每对相似物种恢复为姐妹类群，其亲缘关系随所使用的分子标记不同而发生变化，这提示基因树异质性（gene tree heterogeneity）可能阻碍了准确的系统发育推断。本研究利用全基因组重测序数据（whole genome resequencing data），探究该类群的系统发育关系，重点表征基因树异质性的程度及其潜在成因。我们首先采用多物种溯祖方法（multispecies coalescent methods），基于全基因组变异构建“全证据”系统发育假说，同时考量不完全谱系分选（incomplete lineage sorting）与基因渐渗（introgression）的影响。随后我们分析了全基因组范围内的系统发育信号变异，以量化不同基因组区域间的拓扑冲突程度，并检验其潜在成因。研究发现，由于不完全谱系分选和种间基因渐渗，鹡鸰基因组呈现出支持不同谱系关系的区域镶嵌结构。基因组中最常见的拓扑结构将白鹡鸰与非洲斑鹡鸰作为姐妹类群，该拓扑结构似乎受到古老基因渐渗的影响。此外，我们还推断出白鹡鸰与日本鹡鸰之间存在另一项古老基因渐渗事件。结合多项分析结果，我们为黑白鹡鸰类群构建了系统发育网络（phylogenetic network），证实相似的表型在非姐妹类群中独立演化，支持平行羽色进化假说。进一步分析显示，推断出的网状演化事件并未连接羽色相似的物种，这表明基因渐渗并非该类群平行羽色进化的成因。本研究结果表明，探究全基因组范围的基因树异质性模式，有助于理解表型进化背后的机制。