Revival of Philozoon Geddes for host-specialized dinoflagellates, ‘zooxanthellae’, in animals from coastal temperate zones of northern and southern hemispheres

ABSTRACT

The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differences in diversity, ecology and geographic distribution. An evolutionarily divergent lineage common in temperate symbiotic cnidarians and designated in the literature by several informal names including ‘temperate–A’, A_I, Phylotype A´ (A-prime) and ‘Mediterranean A’, is here assigned to the genus Philozoon. This genus was proposed by Geddes (1882) in one of the earliest papers that recognized ‘yellow cells’ as distinct biological entities separate from their animal and protist hosts. Using phylogenetic data from nuclear (rDNA), chloroplast (cp23S) and mitochondrial genes (cob and cox1), as well as morphology (cell size), ecological traits (host affinity) and geographic distributions, we emend the genus Philozoon Geddes and two of its species, P. medusarum and P. actiniarum, and describe six new species. Each symbiont species exhibits high host fidelity for particular species of sea anemone, soft coral, stony coral and a rhizostome jellyfish. Philozoon is most closely related to Symbiodinium (formerly Clade A), but, unlike its tropical counterpart, occurs in hosts in shallow temperate marine habitats in northern and southern hemispheres including the Mediterranean Sea, north-eastern Atlantic Ocean, eastern Australia, New Zealand and Chile. The existence of a species-diverse lineage adapted to cnidarian hosts living in high latitude habitats with inherently wide fluctuations in temperature calls further attention to the ecological and biogeographic reach of the Symbiodiniaceae.

HIGHLIGHTS

• A dinoflagellate genus symbiotic with temperate invertebrates is characterized and named using a discarded taxonomic term revived from the golden age of Natural Historians.

• The work highlights how animal–algal mutualisms are evolved to thrive under a broad range of environmental conditions.

KEYWORDS:

• Adaptive radiation
• ecological specialization
• Mediterranean Sea
• Symbiodiniaceae
• temperate zone
• zooxanthellae

Acknowledgements

We appreciate Paul W. Gabrielson for help in abiding by ICN rules. We thank Richard Taylor, University of Auckland, for contributing samples of Anthopleura hermaphroditica; Julia Crespo, Jacinto Martínez, Raúl Tomás and Pascal Romans helped with sample collections from the coast of Spain. María García and Fabrizio Atzori provided samples from Cape Carbonara MPA (Sardinia). Raffaella Casotti, Leo Brunet, Lorenzo and Leonardo Auciello, Francesca Margiotta, Marco Cannavacciuolo, Augusto Passarelli, Gianluca Zazo and Ferdinando Tramontano helped with collection of samples from Italy. Avery W. LaJeunesse helped with genetic analyses and Hannah Reich provided graphing assistance. Finally, thanks to the Penn State Microscopy and Cytometry Facility, University Park, Pennsylvania, USA.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary information

The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2021.1914863

Supplemental table S1. Sample metadata including host species, geographic locality, depth of collection and latitude–longitude coordinates.

Supplementary data S1. Nexus file containing the alignment of concatenated LSU, cp23S, cob and cox1 sequences corresponding to species of Philozoon and Symbiodinium and used to create Fig. 7.

Supplementary data S2. Nexus file containing the alignment of psbA^ncr sequences representative of each Philozoon spp. used to create Figs 16 and and 17.

Author contributions

T. C. LaJeunesse: original concept, conducted genetic analyses, microscopy, morphological analysis, created figures, led drafting and editing manuscript; J. Wiedenmann: original concept, sampling, drafting and editing manuscript; P. Casado-amezúa: original concept, sampling, drafting and editing manuscript; I. D’Ambra: sampling and editing manuscript; K. E. Turnham: microscopy and editing manuscript; M. R. Nitschke: sampling, microscopy, morphological analysis, editing manuscript; C. A. Oakley: sampling and editing manuscript; S. Goffredo: sampling and editing manuscript; C. A. Spano: sampling and editing manuscript; V. M. Cubillos: sampling and editing manuscript; S. K. Davy: sampling and editing manuscript; D. J. Suggett: sampling and editing manuscript.

Additional information

Funding

Wiedenmann was funded by the University of Southampton. Casado-Amezúa was funded by the Association of Marine Biology Laboratories Program (ASSEMBLE) grant no. 227799 the University of Southampton and the Natural Environmental Research Council (grant number NE/T001364/1. D’Ambra was funded by the ABBaCo project (Restauro Ambientale e Balneabilità del SIN Bagnoli-Coroglio) and PO FEAMP Campania (2014–2020) cup B69E19000690009. Simon Davy and Clint Oakley were supported by a grant from the Royal Society of New Zealand Marsden Fund (grant number VUW1601) Suggett and Nitschke were funded through an Australian Research Council (ARC) Discovery Grant (DP160100271). LaJeunesse and Turnham were supported by funding from the USA National Science Foundation (grant OCE-1636022).