Unioverse: a phylogenomic resource for reconstructing the evolution of freshwater mussels (Bivalvia, Unionoida)

Freshwater mussels (order Unionoida) are a diverse radiation of parasitic bivalves that require temporary larval encystment on vertebrate hosts to complete metamorphosis to their free-living phase. The freshwater mussel-fish symbiosis represents a useful relationship for understanding eco-evolutionary dynamics in freshwater ecosystems but the practicality of this promising model system is undermined by the absence of a stable freshwater mussel phylogeny. Inadequate character sampling is the primary analytical impediment obfuscating a coherent phylogeny of freshwater mussels, specifically the lack of nuclear molecular markers appropriate for reconstructing supraspecific relationships and testing macroevolutionary hypotheses. The objective of this study is to develop a phylogenomic resource, specifically an anchored hybrid enrichment probe set, capable of capturing hundreds of molecular markers from taxa distributed across the entirety of freshwater mussel biodiversity. Our freshwater mussel specific anchored hybrid enrichment probe set, called Unioverse, successfully captures hundreds of nuclear protein-coding loci from all major lineages of the Unionoida and will facilitate more data-rich and taxonomically inclusive reconstructions of freshwater mussel evolution. We demonstrate the utility of this resource at three disparate evolutionary scales by estimating a backbone phylogeny of the Bivalvia with a focus on the order Unionoida, reconstructing the subfamily-level relationships of the Unionidae, and recovering the systematic position of the phylogenetically unstable genus Plectomerus.

淡水蚌类隶属于珠蚌目 (Unionoida)，是一类具有多样辐射演化特征的寄生双壳类，其幼虫需暂时寄生在脊椎动物宿主体内形成包囊，方能完成变态发育并进入自由生活阶段。淡水蚌类与鱼类的共生关系是研究淡水生态系统生态-进化动态的理想模型，但这一极具潜力的模型体系的实用性，却因缺乏稳定的淡水蚌类系统发育框架而受到制约。导致无法构建清晰统一的淡水蚌类系统发育的主要分析障碍在于特征采样不足，具体表现为缺乏适用于重建种以上类群亲缘关系、验证大进化假说的核分子标记。本研究旨在开发一套系统基因组学资源 (phylogenomic resource)——锚定杂交富集探针组 (anchored hybrid enrichment probe set)——该探针组可从覆盖所有淡水蚌类生物多样性的类群中捕获数百个分子标记。本研究开发的淡水蚌类专属锚定杂交富集探针组命名为Unioverse，可成功从珠蚌目所有主要演化支中捕获数百个核编码蛋白基因座，将助力开展数据量更丰富、类群覆盖更全面的淡水蚌类演化重建研究。本研究通过三个不同演化尺度验证了该资源的实用性：一是构建以珠蚌目为核心的双壳纲 (Bivalvia) 主干系统发育树，二是重建蚌科 (Unionidae) 的亚科级亲缘关系，三是解析系统发育位置长期不稳定的弯蚌属 (Plectomerus) 的分类学地位。