A Comprehensive Phylogenetic Analysis of the Scleractinia (Cnidaria, Anthozoa) Based on Mitochondrial CO1 Sequence Data

Abstract

BackgroundClassical morphological taxonomy places the approximately 1400 recognized species of Scleractinia (hard corals) into 27 families, but many aspects of coral evolution remain unclear despite the application of molecular phylogenetic methods. In part, this may be a consequence of such studies focusing on the reef-building (shallow water and zooxanthellate) Scleractinia, and largely ignoring the large number of deep-sea species. To better understand broad patterns of coral evolution, we generated molecular data for a broad and representative range of deep sea scleractinians collected off New Caledonia and Australia during the last decade, and conducted the most comprehensive molecular phylogenetic analysis to date of the order Scleractinia.MethodologyPartial (595 bp) sequences of the mitochondrial cytochrome oxidase subunit 1 (CO1) gene were determined for 65 deep-sea (azooxanthellate) scleractinians and 11 shallow-water species. These new data were aligned with 158 published sequences, generating a 234 taxon dataset representing 25 of the 27 currently recognized scleractinian families.Principal Findings/ConclusionsThere was a striking discrepancy between the taxonomic validity of coral families consisting predominantly of deep-sea or shallow-water species. Most families composed predominantly of deep-sea azooxanthellate species were monophyletic in both maximum likelihood and Bayesian analyses but, by contrast (and consistent with previous studies), most families composed predominantly of shallow-water zooxanthellate taxa were polyphyletic, although Acroporidae, Poritidae, Pocilloporidae, and Fungiidae were exceptions to this general pattern. One factor contributing to this inconsistency may be the greater environmental stability of deep-sea environments, effectively removing taxonomic “noise” contributed by phenotypic plasticity. Our phylogenetic analyses imply that the most basal extant scleractinians are azooxanthellate solitary corals from deep-water, their divergence predating that of the robust and complex corals. Deep-sea corals are likely to be critical to understanding anthozoan evolution and the origins of the Scleractinia.

The New Systematics of Scleractinia: Integrating Molecular and Morphological Evidence

“…In contrast, the molecular evolutionary hypothesis posits that most families composed exclusively or predominantly of azooxanthellate corals are monophyletic. Therefore, apart from Caryophylliidae and Oculinidae, molecular groupings of azooxanthellate taxa are broadly consistent with classical taxonomy (Kitahara et al 2010b;Stolarski et al 2011).…”

“…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).…”

“…Various degrees of incongruence between morphological and molecular phylogenies are seen at all taxonomic levels, but the most striking is found at the subordinal level. While five suborders are recognised in the most widely-accepted morphological scheme (Wells 1956), only three main clades at the deepest nodes-"basal", "complex" and "robust"-have been recovered based on molecular analyses (Romano and Palumbi 1996;Kitahara et al 2010b;Stolarski et al 2011;Huang 2012). Nearly every genetic locus tested to date supports these latter groupings.…”

“…The 28S rDNA (Chen et al 1995;Cuif et al 2003), 16S rDNA Palumbi 1996, 1997;Le Goff-Vitry et al 2004;Kitahara et al 2010a), 12S rDNA (Chen et al 2002), combined 16S rDNA and 28S rDNA (Romano and Cairns 2000), combined cytochrome b and COI, as well as β-tubulin (Fukami et al 2008) all support the split between the "complex" and "robust" clades. The sister relationship between the "basal" clade and the rest of Scleractinia has been recovered by 12S rDNA, COI, 28S rDNA (Kitahara et al 2010b;Stolarski et al 2011), and most other mitochondrial loci (Huang 2012;Huang andRoy 2013, 2015;Kitahara et al 2014;Lin et al 2014). To date, no morphological characters associated with the hard skeleton have been found to correlate directly with the molecular splits.…”

“…Rhizangiidae is represented only by the mitochondrial genome of an Astrangia species , which is closely related to Oculina (Huang 2012;Huang andRoy 2013, 2015). Stenocyathidae consists of three monotypic genera, of which only Stenocyathus has been sequenced and found nested within Caryophylliidae (Cuif et al 2003;Kitahara et al 2010b;Stolarski et al 2011). Schizocyathidae contains three monotypic genera that have never been sampled for genetic data.…”