Dendrophyllia

Aurelle, Didier, Haguenauer, Anne, Blaise, Chloé, Reynes, Lauric, Arnaud-Haond, Sophie, Boavida, Joana, Cabau, Cédric, Klopp, Christophe, Lundalv, Tomas, Noûs, Camille, Sartoretto, Stéphane, Wienberg, Claudia, Jiménez, Carlos E. & Orejas, Covadonga, 2024, On the specific status of eastern Mediterranean Dendrophyllia corals (Cnidaria, Anthozoa): Genetic characterization and speciation scenarios, Zoologica Scripta 53 (2), pp. 235-247 : 242-244

4.2 | Speciation scenarios in Dendrophyllia

The analysis of speciation scenario clearly supported a current isolation for the populations of D.ramea and D. cornigera studied here: though corresponding to geographically distant populations, this result points to a complete speciation with well-separated evolutionary lineages. It might also be noted that the F ST estimated here for this comparison (around 0.53) is around the F ST value (0.56) used by De Jode et al. (2022) and Roux et al. (2016) as the upper limit of their grey zone of speciation, above which most comparisons involved well-separated species. The only uncertainty regarding speciation scenarios here was between ancestral migration and strict isolation (i.e., no past gene flow): such uncertainty can be observed when the period of ancient gene flow is short ( Fraïsse et al., 2021). Accordingly, with the scenario of ancestral migration, the length of the period of gene flow was short compared to the total divergence time. The median of the estimated divergence time was around 1.3–1.7 million generations depending on the model. This estimate depends on an unknown mutation rate. Without further information, we used the default prior mutation rate of DILS, i.e., 3 × 10 −9 per generation and per nucleotide, but this should be refined with a dedicated genomic study with calibration points. The generation time of Dendrophyllia species is not known. As a comparison, for another Mediterranean, but solitary, Dendrophyllidae coral: Balanophyllia europaea , sexual maturity occurs approximately when specimens reach the age of 3 years ( Goffredo et al., 2002). If we use this value as a surrogate of generation time for the species analysed here, the divergence time between D. ramea and D. cornigera would be between 3.9 and 5.1 million years (Ma). This result is in line with other analyses of divergence time in Scleractinians: Johnston et al. (2017) estimated a maximum divergence time around 3 Ma for five Pocillopora species and 9 Ma for two Seratiopora species. Such estimates evidently depend on the species or populations used for comparison. It would then be interesting to analyse not only other populations from these two species but also other Dendrophyllia species to refine our scenarios of speciation in this genus.

The two competing speciation scenarios retained here then involve a relatively long time without gene flow. Both Dendrophyllia species have overlapping distribution range in the Mediterranean Sea and eastern Atlantic Ocean ( Gori et al., 2014; Salvati et al., 2021; Zibrowius, 1980). Dendrophyllia ramea is present in shallower areas (20 to ca. 170 m depth) than D.cornigera (70 to more than 700 m depth) ( Castellan et al., 2019), but with some possible overlap as well. Therefore, it seems possible that these two species may be currently in contact but do not hybridize because of reproductive incompatibilities (i.e., complete speciation). The evolution of reproductive isolation could have taken place thanks to past allopatric ranges (e.g., in different basins because of past fluctuations of sea level). In this context, the Messinian salinity crisis, between 6.3 and 5.3 Ma ago (according to estimates; Krijgsman et al., 1999; Manzi et al., 2013; Rouchy & Caruso, 2006), could have played a role in the first divergence steps of these two Dendrophyllia species. Differences in depth range could also be involved in speciation, as proposed for the evolution of the Paramuricea octocoral genus ( Quattrini et al., 2022). The oldest known Dendrophyllia fossils have been found from early–middle Miocene deposits ( Vertino et al., 2014). The more recent divergence time estimated here (during Pliocene) is then consistent with this datation.

Regarding the estimates of current effective population size (the size of an ideal population with the same rate of genetic change as the real one; Waples, 2002), we obtained contrasting results, with higher population size for D.cornigera or D.ramea depending on the inclusion or not of variable population size in the model. These differences in the estimate of effective population size could indicate different demographic histories for the two species. The main difference was observed for D. cornigera , with a lower estimate of current effective size when variable population size was allowed: it would be interesting to test different demographic scenarios in this species to analyse the origin of this effect. At a genomic level, both with ancestral migration and strict isolation, there was a clear signal towards models including heterogeneous effective size: this can be the consequence of background selection, that is, the elimination of deleterious mutations in the genome ( Charlesworth et al., 1997; De Jode et al., 2022). As previously mentioned, our analysis of speciation scenarios involved allopatric samples from the western Mediterranean for D. cornigera and the sample from the eastern Mediterranean for D. ramea . It would then be interesting to extend this study to samples from the same area, to take into account potential phylogeographic breaks across the Mediterranean Sea ( Borsa et al., 1997) .

5 | CONCLUSION AND

P E RSPECTIVES

Our results clearly confirm that Dendrophyllia DSC from Cyprus indeed correspond to D. ramea . This population appears original by its morphology and with potential genetic differences with other Mediterranean D.ramea populations. The geographical location of these populations in the eastern Mediterranean probably makes them well-isolated from other Mediterranean ones. The presence of Dendrophyllia corals in this area could also point to particular adaptation to this local environment. Along with the ecological importance of DSC ecosystems, these particularities underline the need for protection of these populations. Further genomic comparisons with other Mediterranean populations will be helpful to study the evolutionary history of Dendrophyllia in Cyprus.