Tethyidae (Sara, 2002)

Sorokin, Shirley J., Ekins, Merrick G., Yang, Qi & Cárdenas, Paco, 2019, A new deep-water Tethya (Porifera, Tethyida, Tethyidae) from the Great Australian Bight and an updated Tethyida phylogeny, European Journal of Taxonomy 529, pp. 1-26 : 17-19

Phylogeny of Tethyidae

The first phylogenetic analyses of Tethya , using COI and morphology ( Heim et al. 2007; Heim & Nickel 2010) revealed four main clades: 1) the seychellensis-wilhelma complex, 2 + 3) the citrinia-actinia complex divided in two subclades (European species and western Atlantic species + eastern Pacific) and 4) the aurantium clade. Our COI and 28S analyses with extended datasets retrieve these four clades, but with a higher biogeographical diversity. The seychellensis-wilhelma complex now includes specimens from Israel, Vietnam, Panama, China and Queensland; the aurantium clade now includes species from the Mediterranean Sea, the Red Sea and Panama. All clades are well-supported in the COI tree except for clade 3, the western Atlantic/Pacific clade. This is precisely the group joined by the COI sequence of T. irisae sp. nov.; its position within this group, however, remains unclear. These same four clades are not as clear in our 28S tree, their inter-relationships are also different, and not supported at all. This may be due to the fact that our 28S alignment is a mix of different 28S domains and different sampling than COI, both of which may influence some of the groupings. The seychellensis-wilhelma and aurantium clades are well supported with 28S as well. On the other hand, the citrinia and actinia subclades are unclear, and this is probably due to the addition in this dataset of many different genera of Tethyidae ( Tethytimea , Tectitethya , Stellitethya , Xenospongia Gray, 1858 , Laxotethya ). As suggested by Sarà et al. (2001) and Heim et al. (2007), Tethya wilhelma and T. gracilis Sarà, Sarà, Nickel & Brümmer, 2001 , both described from aquaria in Germany belong to the seychellensis-wilhelma complex. There is only 1 bp difference between the COI of T. wilhelma and Tethya sp. (Mediterranean Sea, Israel) so this specimen should be re-examined to see if it could be conspecific with T. wilhelma . Heim et al. (2007) showed that the most reliable characters for Tethya taxonomy were morphometric spicule data, but none could actually make good morphological synapomorphies for the two Tethya clades supported with COI and 28S. New characters (e.g., chemical compounds, specialized cells, associated microbes) must be explored in order to find independent support for these groups.

External colour may be a reliable character to discriminate those clades, as shown previously in some calcareous sponges ( Rossi et al. 2011). Indeed, most shallow water Tethya species have a yellow, orange to red surface colour, probably due to different carotenoids ( Tanaka et al. 1982) some of which they can synthesise themselves ( Liaaen-Jensen et al. 1982) and therefore have a genetic basis. All species currently in the citrina subclade ( T. norvegica Bowerbank, 1872 , T. citrina and T. hibernica ) are light-yellow coloured. Species from the actinia subclade and aurantium clade are usually bright yellow to orange to bright orange, except for the ‘aquarium’ species T. minuta Sarà, Sarà, Nickel & Brümmer, 2001 (white, in artificial conditions at least). Finally, the seychellensis-wilhelma clade seems to include especially bright red/carmine surface-coloured species ( T. seychellensis , Tethya sp. from Bocas, T. coccinea Bergquist & Kelly-Borges, 1991 , Tethya sp. 3 from Saudi Arabia, T. taboga , T. samaaii Ribeiro & Muricy, 2011 ), except for the Tethya sp. from Israel which was more light orange, and except again for the ‘aquarium’ species ( T. wilhelma and T. gracilis ). In red surface-coloured species, the choanosome is usually orange. However, more colours exist: some Tethya can be green (e.g., Tethya brasiliana Ribeiro & Muricy, 2004 ), dark blue (e.g., Tethya cyanea Ribeiro & Muricy, 2004 ), or pink (e.g., Tethya bergquistae ) but none of these species have been sequenced yet. We can probably dismiss the green colour. It is found in species that can also be orange; Laubenfels (1950) suggested the green colour of T. actinia in Bermuda was due to symbiotic algae (a specimen may “turn orange” when fixed in alcohol, as the chlorophyll is extracted). More problematic are species with varying colours, from yellow to orange and red (e.g., Tethya fastigata ). As for the few deep-sea species of Tethya , some have lost their colours (e.g., Tethya irisae sp. nov.) while others have retained them: e.g., Tethya levii Sarà, 1988 from New Caledonia is light orange, and groups in the actinia clade, in accordance with our hypothesis (P. Cárdenas, unpublished data). This groupingby-colour hypothesis should be further tested with the sequencing of new species of Tethya . Other genera of Tethyidae included in our dataset have usually irregular massive forms or are disc-shaped (instead of subspherical forms), and all have dark colours: black-brownish for Tectitethya spp., beige-gray for Xenospongia , and whitish-brown in ethanol for Laxotethya and Stellitethya (the live colour is unknown). Since all except Laxotethya are sister group to a bright orange Tethya sp. from South Australia (possibly in the actinia clade) ( Fig. 5 , 28S tree), we suppose the common ancestor of these other genera lost its yellow-orange colours, and so its capacity to produce carotenoids.

Our COI and 28S dataset include type species of four Tethyidae genera (of the 14 valid genera): Tethya ( T. aurantium , COI), Tectitethya ( T. crypta , 28S), Xenospongia ( X. patelliformis , 28S) and Laxotethya ( L. dampierensis , 28S). In addition to that, two other Tethyidae genera are represented in our 28S tree: Stellitethya and Tethytimea . All these genera are essentially defined by different skeletal structures and therefore body shape; all these genera have an indistinct or ill-defined cortex (vs a distinct thick cortex for Tethya ) and an irregular massive or encrusting shape (vs (sub)spherical shape in Tethya ). Our 28S tree suggests that Xenospongia , Stellitethya , Tectitethya and Tethytimea are grouping with Tethya ( Fig. 5 ), while Laxotethya groups with Hemiasterellidae , albeit with no support. Tethytimea carmelita , Tectitethya and Stellitethya / Xenospongia evolved independently within Tethya thus suggesting that the loss of a distinct cortex and of the subspherical shape happened several times. More sequences from Australian Tethya are needed to understand the origin and relationships of these other Tethyidae genera. One clade that is moderately supported (bootstrap of 69) is the sister-group relationship of Xenospongia and Stellitethya , with a 5–6 bp difference in 28S (D3–D5). Both genera have a poorly defined cortex but different shapes: discoid for Xenospongia , massive irregular for Stellitethya . These two genera also share megasters reaching large sizes (> 150 µm), as in T. irisae sp. nov., grouping nearby (bootstrap of 62) with Tectitethya (which does not have very large megasters).

Figures

Fig. 5 (opposite page). Tethyida COI and 28S maximum-likelihood (RaxML) trees. ML bootstrap supports (1000 bootstrap replicates)> 70 are indicated. After the species name, locality of the specimen is given (when known), followed by the GenBank accession number(s). For 28S, we also indicated the 28S region that was sequenced as well as the first author + date of the publication where the sequence first appeared. Type species of genera are in red boxes while Tethya irisae sp. nov. appears in red.