Phylogenomic analysis of a putative missing link sparks reinterpretation of leech evolution

Abstract

Leeches(Hirudinida) comprise a charismatic, yetoftenmalignedgroupoforganisms.Despitetheir ecological,economic,andmedical importance, a general consensus on the phylogenetic relationships of major hirudinidan lineages is lacking. This absence of a consistent, robust phylogeny of early-diverging lineages has hindered our understanding of the underlying processes that enabled evolutionary diversification of this clade. Here, we used an anchored hybrid enrichment-based phylogenomic approach, capturing hundreds of loci to investigate phylogenetic relationships among major hirudinidan lineages and their closest living relatives. Our results suggest that a dramatic reinterpretation of early leech evolution is warranted. We recovered Branchiobdellida as sister to a cladethat includesallmajor lineagesofhirudinidans,butfoundAcanthobdellatobenestedwithinOceanobdelliformes.Theseresults cast doubt on the utility of Acanthobdella as a "missing link" used to explain the origin of blood-feeding in hirudineans. Further, our results support a deep divergence between predominantly marine and freshwater lineages, while not supporting the reciprocal monophyly of jawed and proboscis-bearing leeches. To sum up, our phylogenomic resolution of early-diverging leeches provides a necessary foundation for illuminating the evolution of host-symbiont associations and key adaptations that have allowed leeches to colonize a wide diversity of habitats worldwide.