Naked corals: skeleton loss in Scleractinia

Abstract

Stony corals, which form the framework for modern reefs, are classified as Scleractinia (Cnidaria, Anthozoa, and Hexacorallia) in reference to their external aragonitic skeletons. However, persistent notions, collectively known as the "naked coral" hypothesis, hold that the scleractinian skeleton does not define a natural group. Three main lines of evidence have suggested that some stony corals are more closely related to one or more of the soft-bodied hexacorallian groups than they are to other scleractinians: (i) morphological similarities; (ii) lack of phylogenetic resolution in molecular analyses of scleractinians; and (iii) discrepancy between the commencement of a diverse scleractinian fossil record at 240 million years ago (Ma) and a molecule-based origination of at least 300 Ma. No molecular evidence has been able to clearly reveal relationships at the base of a well supported clade composed of scleractinian lineages and the nonskeletonized Corallimorpharia. We present complete mitochondrial genome data that provide strong evidence that one clade of scleractinians is more closely related to Corallimorpharia than it is to a another clade of scleractinians. Thus, the scleractinian skeleton, which we estimate to have originated between 240 and 288 Ma, was likely lost in the ancestry of Corallimorpharia. We estimate that Corallimorpharia originated between 110 and 132 Ma during the late- to mid-Cretaceous, coinciding with high levels of oceanic CO(2), which would have impacted aragonite solubility. Corallimorpharians escaped extinction from aragonite skeletal dissolution, but some modern stony corals may not have such fortunate fates under the pressure of increased anthropogenic CO(2) in the ocean.

Fig. 1.

Phylogenetic relationships among sampled hexacorallians. Bayesian posterior probabilities and maximum parsimony bootstrap values are shown at each node. A single 100 indicates that both values equal 100. Ranges of estimated divergence dates are shown for nodes indicated by open circles. Fixed divergence dates based on earliest fossil appearances are shown at nodes indicated by filled circles.

Fig. 2.

Linearized mitochondrial gene orders for each group. The boxes for trnM and trnW represent the methione and tryptophan tRNAs. Black boxes represent noncoding regions of the nad5 intron. Lines connecting the different genomes highlight intron expansion in the different anthozoan genomes. The black bar at the bottom of the octocorallian genomes represents the opposite transcriptional orientation of that region in the genome.

Fig. 3.

Pairwise comparison of gene rearrangements between the scleractinian and corallimorpharian gene orders. Black bars highlighting seven pairs of genes in the two genomes are connected by lines indicating the relative positional rearrangement of each pair. In one case only the rearrangement involved an inversion.