Dating the species network: allopolyploidy and repetitive DNA evolution in American daisies (Melampodium sect. Melampodium, Asteraceae)

Allopolyploidy has played an important role in the evolution of the flowering plants. Genome mergers are often accompanied by significant and rapid alterations of genome size and structure via chromosomal rearrangements and altered dynamics of tandem and dispersed repetitive DNA families. Recent developments in sequencing technologies and bioinformatic methods allow for a comprehensive investigation of the repetitive component of plant genomes. Interpretation of evolutionary dynamics following allopolyploidization requires both the knowledge of parentage and the age of origin of an allopolyploid. Whereas parentage is typically inferred from cytogenetic and phylogenetic data, age inference is hampered by the reticulate nature of the phylogenetic relationships. Treating subgenomes of allopolyploids as if they belonged to different species (i.e., no recombination among subgenomes) and applying cross-bracing (i.e., putting a constraint on the age difference of nodes pertaining to the same event), we can infer the age of allopolyploids within the framework of the multi-species coalescent within BEAST2. Together with a comprehensive characterization of the repetitive DNA fraction using the RepeatExplorer pipeline, we apply the dating approach in a group of closely related allopolyploids and their progenitor species in the plant genus Melampodium (Asteraceae). We dated the origin of both the allotetraploid, M. strigosum, and its two allohexaploid derivatives, M. pringlei and M. sericeum, which share both parentage and the direction of the cross, to the Pleistocene (less than 1.4 Ma). Thus, Pleistocene climatic fluctuations may have triggered formation of allopolyploids possibly in short intervals, contributing to difficulties in inferring the precise temporal order of allopolyploid species divergence of M. sericeum and M. pringlei. The relatively recent origin of the allopolyploids likely played a role in the near-absence of major changes in the repetitive fraction of the polyploids’ genomes. The repetitive elements most affected by the post-polyploidization changes represented retrotransposons of the Ty1-copia lineage Maximus and, to a lesser extent, also Athila elements of Ty3-gypsy family.

异源多倍化（Allopolyploidy）在被子植物的演化进程中发挥了关键作用。基因组融合往往伴随基因组大小与结构的显著快速改变，具体表现为染色体重排，以及串联重复与分散重复DNA家族的动态变化失调。近年来测序技术与生物信息学方法的进步，使得对植物基因组重复组分的全面研究成为可能。解析异源多倍化后的进化动态，需要同时明确异源多倍体的亲本来源与起源时间。通常可通过细胞遗传学与系统发育数据推断亲本来源，但起源时间的推断却受限于系统发育关系的网状结构特性。若将异源多倍体的各亚基因组视为独立物种（即假设亚基因组间无重组），并应用交叉约束策略（即对同一事件相关节点的年龄差异施加约束），便可在BEAST2的多物种溯祖模型框架内完成异源多倍体的起源时间推断。本研究结合使用RepeatExplorer流程对重复DNA组分进行全面表征，并将该定年方法应用于菊科（Asteraceae）黑足菊属（Melampodium）中一组紧密相关的异源多倍体及其亲本物种。我们对异源四倍体M. strigosum，以及其两个共享亲本来源与杂交方向的异源六倍体衍生种M. pringlei和M. sericeum的起源时间进行了定年，结果均指向更新世（距今不足1.4 Ma）。由此可见，更新世的气候波动可能在较短时间间隔内多次触发异源多倍体的形成，这也为推断M. sericeum与M. pringlei的异源多倍体物种分化精确时序带来了困难。这些异源多倍体的起源相对较近，可能是其基因组重复组分几乎未发生显著改变的重要原因。受多倍化后变化影响最显著的重复元件为Ty1-copia超家族Maximus分支的反转录转座子，其次为Ty3-gypsy家族的Athila元件。