Mitochondrial and Nuclear Genes Suggest that Stony Corals Are Monophyletic but Most Families of Stony Corals Are Not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria)

Abstract

Modern hard corals (Class Hexacorallia; Order Scleractinia) are widely studied because of their fundamental role in reef building and their superb fossil record extending back to the Triassic. Nevertheless, interpretations of their evolutionary relationships have been in flux for over a decade. Recent analyses undermine the legitimacy of traditional suborders, families and genera, and suggest that a non-skeletal sister clade (Order Corallimorpharia) might be imbedded within the stony corals. However, these studies either sampled a relatively limited array of taxa or assembled trees from heterogeneous data sets. Here we provide a more comprehensive analysis of Scleractinia (127 species, 75 genera, 17 families) and various outgroups, based on two mitochondrial genes (cytochrome oxidase I, cytochrome b), with analyses of nuclear genes (ß-tubulin, ribosomal DNA) of a subset of taxa to test unexpected relationships. Eleven of 16 families were found to be polyphyletic. Strikingly, over one third of all families as conventionally defined contain representatives from the highly divergent “robust” and “complex” clades. However, the recent suggestion that corallimorpharians are true corals that have lost their skeletons was not upheld. Relationships were supported not only by mitochondrial and nuclear genes, but also often by morphological characters which had been ignored or never noted previously. The concordance of molecular characters and more carefully examined morphological characters suggests a future of greater taxonomic stability, as well as the potential to trace the evolutionary history of this ecologically important group using fossils.

The New Systematics of Scleractinia: Integrating Molecular and Morphological Evidence

“…This analysis showed that all five genera and nine of ten families for which more than one taxon were tested formed monophyletic groups. However, of the seven suborders examined, only three-Meandriina, Poritiina and Dendrophylliinawere recovered unambiguously as clades, although only Dendrophylliina remains the only monophyletic suborder to emerge from recent studies (e.g., Fukami et al 2008;Arrigoni et al 2014a). …”

“…Therefore, these genes are more informative for reconstructing deep coral phylogenies. Other than the 16S rDNA that established widespread subordinal non-monophyly Palumbi 1996, 1997;Le GoffVitry et al 2004), 12S rDNA, cytochrome b and cytochrome c oxidase subunit I (COI) were purposed for corals relatively early (Medina et al 1999;van Oppen et al 1999;Fukami et al 2000) and have been used for inferring large scleractinian trees effectively (Chen et al 2002;Fukami et al 2004bFukami et al , 2008Barbeitos et al 2010;Kitahara et al 2010bKitahara et al , 2013Stolarski et al 2011;Arrigoni et al 2012Arrigoni et al , 2014cHuang 2012;Huang andRoy 2013, 2015;Marcelino et al 2013;Curnick et al 2015; Fig. 4.1).…”

“…The second limitation concerns traits that may evolve at distinct rates in different lineages. Not surprisingly, the small number of "reliable" macromorphological characters, as indicated by Cairns (2001), and the uncertain impact of environmental variables on skeletal morphology have severely hampered attempts to infer relationships among scleractinian suborders and families (Romano and Cairns 2000;Stolarski and Roniewicz 2001;Le Goff-Vitry et al 2004;Fukami et al 2008). As such, evolutionary hypotheses based on morphological characters have resulted in several different taxonomic schemes (e.g., Vaughan and Wells 1943;Alloiteau 1952;Wells 1956;Chevalier and Beauvais 1987;Veron 1995; for a review of the first four schemes, see Stolarski and Roniewicz 2001).…”

“…Stony corals belonging to the order Scleractinia (Anthozoa: Hexacorallia) are a clade of cnidarians that build a calcium carbonate skeleton in the form of aragonite, and are sister group to the non-stony corallimorpharians (Daly et al 2003;Fukami et al 2008;Kitahara et al 2014;Lin et al 2014). At present, Scleractinia contains 31 families, about 240 genera, and over 1,500 species (Cairns 1999(Cairns , 2009Appeltans et al 2012;Huang and Roy 2015), including both zooxanthellate-hosting the symbiotic dinoflagallate Symbiodiniumand azooxanthellate corals.…”

Faunal breaks and species composition of Indo-Pacific corals: the role of plate tectonics, environment and habitat distribution

“…The model included three random effects: faunal break, clade [49] and suborder [50]; the latter two were nested and included to account for any phylogenetic non-independence that was not explicitly captured within sexuality or genus age [51]. We investigated all combinations of main effects and interaction terms that were judged to be biologically feasible (see the electronic supplementary material, methods (g)).…”