Anemonefish are better taxonomists than humans

The symbiosis between giant sea anemones, algae of the family Symbiodiniaceae, and anemonefish is an iconic example of a mutualistic trio1Hoepner C.M. Fobert E.K. Abbott C.A. Burke da Silva K. No place like home: Can omics uncover the secret behind the sea anemone and anemonefish symbiotic relationship?.in: Laudet V. Ravasi T. Evolution, Development and Ecology of Anemonefish. Model organisms for Marine Science. CRC Press, Boca Raton2022: 197-208Crossref Google Scholar,2Roux N. Salis P. Lee S.H. Besseau L. Laudet V. Anemone fishes, a model for Eco-Evo-Devo.EvoDevo. 2020; 11: 20Crossref Scopus (21) Google Scholar. Molecular analyses have shown that giant sea anemones hosting anemonefish belong to three clades: Entacmaea, Stichodactyla, and Heteractis3Titus B.M. Benedict C. Laroche C. Gusmão L.C. Van Deusen V. Chiodo T. Meyer C.P. Berumen M.L. Bartholomew A. Yanagi K. et al.Phylogenetic relationships among the clownfish-hosting sea anemones.Mol. Phyl. Evol. 2019; 139106526Crossref Scopus (23) Google Scholar,4Nguyen H.T.T. Dang B.T. Glenner H. Geffen A.J. Cophylogenetic analysis of the relationship between anemonefish Amphiprion (Perciformes: Pomacentridae) and their symbiotic host anemones (Anthozoa: Actiniaria).Mar. Biol. Res. 2019; 16: 117-133Crossref Scopus (8) Google Scholar,5Kashimoto R. Tanimoto M. Miura S. Satoh N. Laudet V. Khalturin K. Transcriptomes of giant sea anemones from Okinawa as a tool for understanding their phylogeny and symbiotic relationships with anemonefish.Zool. Sci. 2022; 39: 374-387Crossref Scopus (0) Google Scholar (Figure 1A). Associations among 28 species of anemonefish and 10 species of giant sea anemone hosts are complex. Some fish species are highly specialized to only one anemone species (e.g., Amphiprion frenatus with Entacmaea quadricolor), whereas others are more generalist (e.g., Amphiprion clarkii)1Hoepner C.M. Fobert E.K. Abbott C.A. Burke da Silva K. No place like home: Can omics uncover the secret behind the sea anemone and anemonefish symbiotic relationship?.in: Laudet V. Ravasi T. Evolution, Development and Ecology of Anemonefish. Model organisms for Marine Science. CRC Press, Boca Raton2022: 197-208Crossref Google Scholar,2Roux N. Salis P. Lee S.H. Besseau L. Laudet V. Anemone fishes, a model for Eco-Evo-Devo.EvoDevo. 2020; 11: 20Crossref Scopus (21) Google Scholar,6Fautin D.G. The anemonefish symbiosis: What is known and what is not.Symbiosis. 1991; 10: 23-46Google Scholar. Reasons for host preferences are obscured, among other things, by the lack of resolution in the giant sea anemone phylogeny. Here, we generated a transcriptomic dataset from 55 sea anemones collected from southern Japan to reconstruct these phylogenetic relationships. We observed that the bubble-tip sea anemone E. quadricolor, currently considered a single species, can be separated into at least four cryptic lineages (A–D). Surprisingly, these lineages can be precisely distinguished by observing their association with anemonefish: A. frenatus only associates with lineage D, whereas A. clarkii lives in the other three lineages.