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Phylogenomics of Palythoa (Hexacorallia: Zoantharia): probing species boundaries in a globally distributed genus

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Abstract

Zoantharians (Cnidaria: Hexacorallia: Zoantharia) of the genus Palythoa are ubiquitous species that occupy reef habitats in every tropical ocean. Disagreements among classifications based on morphology, reproductive traits, and molecular techniques have generated taxonomic challenges within this group. Molecular studies provide limited phylogenetic resolution between species, and discordance is frequently attributed to slow mitochondrial rates and lack of resolution among molecular markers. Here we conducted the first phylogenomic survey of Palythoa, using a reduced representation genomic approach (ezRAD) to resolve relationships among eight described and four putative Palythoa species (N = 22 plus two outgroups) across the Pacific and Atlantic Oceans. We constructed nearly complete mitochondrial genomes and assembled transcriptome loci datasets by reference mapping. A de novo assembly was performed for the holobiont dataset, and we compared a range of filtering strategies from unfiltered data down to 136 unlinked high-quality biallelic SNPs shared by all samples to resolve evolutionary lineages within Palythoa. Across all these datasets, the resulting Bayesian and ML trees revealed six highly concordant and well-supported clades, however, the phylogenomic data were inconclusive in resolving species relationships within the clades. We detected putative species complexes within two well sampled Palythoa clades (clades I and II), but species delimitation results were inconsistent in whether these clades contain multiple nominal species or represent a single variable species. Polyphyly in the broadly distributed species Palythoa tuberculosa and P. mutuki highlight the need for additional study. Consistency among nuclear and mitogenomic datasets points to a lack of biological understanding of species boundaries among these zoantharians rather than limitations of the molecular markers. More complete taxonomic sampling of nominal species across the geographic ranges of distribution is necessary to resolve species boundaries and evolutionary histories among members of this genus.

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Acknowledgements

Special thanks to Kyle Hobson for many thoughtful discussions about the manuscript. We appreciate Richard Coleman for helpful feedback throughout this project and assistance with figures. For valuable advice we thank Evan Barba, Richard Coleman, Emily Conklin, Zac Forsman, Erika Johnston, Derek Kraft, and the other members of the ToBo lab. Thanks to Ingrid Knapp at HIMB for ezRAD protocol training. We thank the HIMB EPSCoR core facility and the University of Hawai‘i’s Advanced Studies in Genomics, Proteomics, and Bioinformatics facility for their assistance with DNA sequencing. JDR thanks Drs. Holger Jenke-Kodama and Tomoko Yamazaki (OIST) and John Gorman (Maui Ocean Center) for logistical support in sampling in Maui, and Prof. Bert Hoeksema (Naturalis) and Temminck Fellowships for supporting sampling in St. Eustatius and Curacao. Thanks to Prof. Jorge Cortes (U. Costa Rica) for support in Costa Rica, and Prof. Keryea Soong (NSYSU) and a DARS award for sampling in Dongsha Atoll. Field work by JDR was also supported by ORCHIDS internal grants at the University of the Ryukyus. This research was supported by the National Science Foundation grants GRFP 1329626 to AD and OA-1416889 to RJT. Further support was provided to AD by the Carol Ann & Myron L. Hayashida Scholarship and the Lord Scholarship during this project. The views expressed herein are those of the authors and may not reflect the views of the NOAA or its sub-agencies. This is contribution #1832 from the Hawai‘i Institute of Marine Biology, and #11173 from the School of Ocean and Earth Science and Technology. We appreciate comments from three reviewers and the editor. We dedicate this work to Joshua Copus.

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  1. Hawai‘i Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawai‘i At Mānoa, Kāne‘ohe, HI, USA

    ‘Ale‘alani Dudoit & Robert J. Toonen

  2. Zoology Graduate Program, University of Hawai‘i At Mānoa, Honolulu, HI, USA

    ‘Ale‘alani Dudoit

  3. Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, Nishihara, Okinawa, Japan

    Maria E. A. Santos & James D. Reimer

  4. Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, Japan

    James D. Reimer

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  1. ‘Ale‘alani Dudoit
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Dudoit, ‘., Santos, M.E.A., Reimer, J.D. et al. Phylogenomics of Palythoa (Hexacorallia: Zoantharia): probing species boundaries in a globally distributed genus. Coral Reefs 41, 655–672 (2022). https://doi.org/10.1007/s00338-021-02128-4

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