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. 2019 Jul 1;11(11):3082-3093.
doi: 10.1093/gbe/evz120.

Phylogenomic Analysis of a Putative Missing Link Sparks Reinterpretation of Leech Evolution

Anna J Phillips  1 , Alex Dornburg  2 , Katerina L Zapfe  2   3 , Frank E Anderson  4 , Samuel W James  5 , Christer Erséus  6 , Emily Moriarty Lemmon  7 , Alan R Lemmon  8 , Bronwyn W Williams  2
Affiliations

Phylogenomic Analysis of a Putative Missing Link Sparks Reinterpretation of Leech Evolution

Anna J Phillips et al. Genome Biol Evol. .

Expression of concern in

Abstract

Leeches (Hirudinida) comprise a charismatic, yet often maligned group of organisms. Despite their ecological, economic, and medical 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 clade that includes all major lineages of hirudinidans, but found Acanthobdella to be nested within Oceanobdelliformes. These results 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.

Keywords: Acanthobdella; Hirudinida; anchored hybrid enrichment; phylogeny; sanguivory; symbiosis.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.
—Images of adult (NCSM 90081) and juvenile (NCSM 90080) Acanthobdella peledina specimens, the former from which we obtained one of the two sequences used in this study. (A) Adult, whole body; (B) Adult, close-up of anterior end, showing the diagnostic paired chaetae surrounding the oral region, and; (C) juvenile, close-up of anterior end, showing the diagnostic chaetae, albeit less distinct than in the adult.
<sc>Fig</sc>. 2.
Fig. 2.
—Phylogenetic relationships of major leech and branchiobdellidan lineages and host associations. (A) Evolutionary relationships based on Bayesian and maximum likelihood analyses of DNA sequence data captured through anchored hybrid enrichment. Clade support values are indicated by circles at nodes (Bayesian posterior probability = BPP; Bootstrap support = BSS). Branches are color-coded to show historically accepted higher taxa: brown = Hirudinida, green = Rhynchobdellida (now Oceanobdelliformes and Glossiphoniiformes), yellow = Arhynchobdellida (represented in this study by members of what are now Erpobdelliformes and Hirudiniformes), red = Acanthobdellida, blue = Branchiobdellida. (B) Matrix indicates associations of leeches (columns aligned to phylogeny) with generalized hosts (rows) depicted graphically as 1) invertebrates, 2) fishes (marine, brackish, and freshwater), 3) amphibians and reptiles except turtles, 4) turtles (both marine and freshwater), 5) birds, and 6) mammals. Dark shaded cells in the matrix indicate leech-host affiliation. Upward lines stemming from the matrix link the matrix in A with dots color coded by respective branches, horizontal lines correspond with generalized hosts.
<sc>Fig</sc>. 3.
Fig. 3.
—Simplified cladograms displaying postulated relationships among Acanthobdellida (Acan), Branchiobdellida (Bran), and Hirudinida (Hir) based on prior molecular and/or morphological data: A. Acanthobdellida as sister to Branchiobdellida + Hirudinida; B. Branchiobdellida as sister to Acanthobdellida + Hirudinida, and; C. Hirudinida as sister to Acanthobdellida + Branchiobdellida.
<sc>Fig</sc>. 4.
Fig. 4.
—Quantification of phylogenetic informativeness present in legacy markers. (A) Phylogenetic informativeness profile of the combined information from five legacy markers, COI, ITS-1, 28S rDNA, 18S rDNA, and 16S rDNA. (B) Phylogenetic informativeness profile of individual legacy markers. (C) Heatmaps indicating probabilities of a legacy marker (Y-axis) resolving a phylogenetic problem of a specific internode length (X-axis) for a relatively deep time internode (T = 0.9; left) and a relatively moderate time (T = 0.6). Colors correspond to the predicted probability of correct resolution of the hypothetical quartet, with white indicating higher predictions of loci contributing to correct topological inference. Shading in A & B corresponds to the decline of informativeness and the correlated onset of convergences in character state (i.e., “the rainshadow of noise”) (Dornburg, Townsend, and Wang 2017; Townsend and Leuenberger 2011).
<sc>Fig</sc>. 5.
Fig. 5.
—Quantification of phylogenetic informativeness present in AHE data. (A) Phylogenetic informativeness (PI) profile of the information in each AHE locus represented through a hexbin plot of the relative phylogenetic informativeness (PI) over time. Colors correspond to the number of loci occupying each bin of informativeness through time following (Near et al. 2018). (B) Example of changepoint plot used as filtration criterion following (Dornburg, Townsend, Brooks, et al. 2017). (C) Heatmaps indicating probabilities of the combined AHE data set and representative loci (Y-axis) resolving a phylogenetic problem of a specific internode length (X-axis) for a relatively deep time internode (T = 0.9; left) and a relatively moderate time (T = 0.6). Colors correspond to the predicted probability of correct resolution of the hypothetical quartet. Loci are sorted by length. Counts in A represent the number of loci represented in a given hexbin. Shading in B corresponds to the loci selected possessing levels of phylogenetic noise that exceed the filtration threshold.
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