Repeated loss of coloniality and symbiosis in scleractinian corals

Abstract

The combination of coloniality and symbiosis in Scleractinia is thought to confer competitive advantage over other benthic invertebrates, and it is likely the key factor for the dominance of corals in tropical reefs. However, the extant Scleractinia are evenly split between zooxanthellate and azooxanthellate species. Most azooxanthellate species are solitary and nearly absent from reefs, but have much wider geographic and bathymetric distributions than reef corals. Molecular phylogenetic analyses have repeatedly recovered clades formed by colonial/zooxanthellate and solitary/azooxanthellate taxa, suggesting that coloniality and symbiosis were repeatedly acquired and/or lost throughout the history of the Scleractinia. Using Bayesian ancestral state reconstruction, we found that symbiosis was lost at least three times and coloniality lost at least six times, and at least two instances in which both characters were lost. All of the azooxanthellate lineages originated from ancestors that were reconstructed as symbiotic, corroborating the onshore-offshore diversification trend recorded in marine taxa. Symbiotic sister taxa of two of these descendant lineages are extant in Caribbean reefs but disappeared from the Mediterranean before the end of the Miocene, whereas extant azooxanthellate lineages have trans-Atlantic distributions. Thus, the phyletic link between reef and nonreef communities may have played an important role in the dynamics of extinction and recovery that marks the evolutionary history of scleractinians, and some reef lineages may have escaped local extinction by diversifying into offshore environments. However, this macroevolutionary mechanism offers no hope of mitigating the effects of climate change on coral reefs in the next century.

Fig. 1.

Fifty-percent majority rule consensus tree computed from the thinned posterior distribution of trees (n = 312) obtained via MCMC. Column of symbols to the right of the list of families represent suborders (legend on graph). Numbers above nodes correspond to the Bayesian posterior probabilities and numbers below the nodes to bootstrap support obtained under maximum-likelihood and maximum-parsimony criteria, respectively. Filled circles (●) denote colonial taxa; open circles (○) denote solitary taxa. Filled squares (■) denote symbiotic taxa; open squares (□) denote asymbiotic taxa. Circles and squares above nodes indicate reconstructions supported by BFs. Node Q was reconstructed as an MRCA (Methods).

Fig. 2.

(A) Plot of BFs against the number of generations. BFs were computed using the harmonic means of log-likelihood scores calculated under the dependent (correlated) and independent models of evolution. RJ-MCMC runs were replicated five times under each model and BFs were calculated for all 25 pairwise combinations. Dotted line represents median and solid lines represent maximum and minimum BF values at each sampled generation from the chain. Critical regions are denoted by progressively darker shades of gray on the background; region of nonsignificance is white. (B) Histograms of rate parameters sampled under the dependent model of evolution. Paired histograms correspond to rate distributions that are expected to be the same if characters evolved independently of each other. Dark bars indicate the number of times the rate was assigned to the zero-category. Labeling of x axis follows the conventional mathematical notation for intervals, i.e., (0.00, 0.13] is equivalent to 0.00 < x ≤0.13.