Hidden among Sea Anemones: The First Comprehensive Phylogenetic Reconstruction of the Order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) Reveals a Novel Group of Hexacorals

Abstract

Sea anemones (order Actiniaria) are among the most diverse and successful members of the anthozoan subclass Hexacorallia, occupying benthic marine habitats across all depths and latitudes. Actiniaria comprises approximately 1,200 species of solitary and skeleton-less polyps and lacks any anatomical synapomorphy. Although monophyly is anticipated based on higher-level molecular phylogenies of Cnidaria, to date, monophyly has not been explicitly tested and at least some hypotheses on the diversification of Hexacorallia have suggested that actiniarians are para- or poly-phyletic. Published phylogenies have demonstrated the inadequacy of existing morphological-based classifications within Actiniaria. Superfamilial groups and most families and genera that have been rigorously studied are not monophyletic, indicating conflict with the current hierarchical classification. We test the monophyly of Actiniaria using two nuclear and three mitochondrial genes with multiple analytical methods. These analyses are the first to include representatives of all three currently-recognized suborders within Actiniaria. We do not recover Actiniaria as a monophyletic clade: the deep-sea anemone Boloceroides daphneae, previously included within the infraorder Boloceroidaria, is resolved outside of Actiniaria in several of the analyses. We erect a new genus and family for B. daphneae, and rank this taxon incerti ordinis. Based on our comprehensive phylogeny, we propose a new formal higher-level classification for Actiniaria composed of only two suborders, Anenthemonae and Enthemonae. Suborder Anenthemonae includes actiniarians with a unique arrangement of mesenteries (members of Edwardsiidae and former suborder Endocoelantheae). Suborder Enthemonae includes actiniarians with the typical arrangement of mesenteries for actiniarians (members of former suborders Protantheae, Ptychodacteae, and Nynantheae and subgroups therein). We also erect subgroups within these two newly-erected suborders. Although some relationships among these newly-defined groups are still ambiguous, morphological and molecular results are consistent enough to proceed with a new higher-level classification and to discuss the putative functional and evolutionary significance of several morphological attributes within Actiniaria.

Sea Anemones through X-Rays: Visualization of Two Species ofDiadumene(Cnidaria, Actiniaria) Using Micro-CT

“…Diadumenidae has been recovered as monophyletic and closely related to members of Metridiidae Carlgren, 1893, in all molecular phylogenetic analyses including multiple species of the genus (Daly et al, 2008;Rodríguez and Daly, 2010;Gusmão and Daly, 2010;Rodríguez et al, 2012Rodríguez et al, , 2014Grajales and Rodríguez, 2016). Rodríguez et al (2012) erected the clade Metridina for members of Diadumenidae and Metridiidae, emphasizing the morphological similarities among these families, which had been proposed by others (e.g., Stephenson, 1925).…”

“…Remarks: Similar modifications made for the familial diagnosis regarding changes on higher-level classification (i.e., Rodríguez et al, 2012Rodríguez et al, , 2014 and nematocyst terminology (i.e., Sanamyan et al, 2012) were also made here. We have also included specific information on location of cinclides on the scapus (i.e., scattered or arranged in longitudinal rows) and position on top of raised columnar projections (e.g., Diadumene leucolena).…”

“…We include photographs of each type of nematocyst for reliable comparison across terminologies and taxa (see Fautin, 1988). Higher-level classification for Actiniaria follows Rodríguez et al (2014).…”

“…Sequences have been deposited in GenBank (see Supplementary Data: https://doi.org/10.5531/sd.sp.33). DNA sequences for each of the three markers were combined and analyzed with sequences corresponding to superfamily Metridioidea Carlgren, 1893, from Rodríguez et al (2014), using sequences from selected taxa within the superfamily Actinioidea Rafinesque, 1815, as outgroup. Sequences for each marker were separately aligned using MAFFT v.7.017 (Katoh et al, 2002) using the following settings: Strategy, E-INS-I; Scoring matrix for nucleotide sequences, 200PAM/k = 2; Gap open penalty, 1.53; Offset value, 0.05.…”

“…Remarks: We modified the familial diagnosis to reflect recent changes in higher-level classification of Actiniaria (i.e., Rodríguez et al, 2012Rodríguez et al, , 2014 and the terminology used to classify nematocysts in this study (i.e., modified from Sanamayan et al, 2012). These modifications have been made in all other diagnoses included in this study.…”