The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals

Abstract

BackgroundScleractinian corals are currently a focus of major interest because of their ecological importance and the uncertain fate of coral reefs in the face of increasing anthropogenic pressure. Despite this, remarkably little is known about the evolutionary origins of corals. The Scleractinia suddenly appear in the fossil record about 240 Ma, but the range of morphological variation seen in these Middle Triassic fossils is comparable to that of modern scleractinians, implying much earlier origins that have so far remained elusive. A significant weakness in reconstruction(s) of early coral evolution is that deep-sea corals have been poorly represented in molecular phylogenetic analyses.ResultsBy adding new data from a large and representative range of deep-water species to existing molecular datasets and applying a relaxed molecular clock, we show that two exclusively deep-sea families, the Gardineriidae and Micrabaciidae, diverged prior to the Complexa/Robusta coral split around 425 Ma, thereby pushing the evolutionary origin of scleractinian corals deep into the Paleozoic.ConclusionsThe early divergence and distinctive morphologies of the extant gardineriid and micrabaciid corals suggest a link with Ordovician "scleractiniamorph" fossils that were previously assumed to represent extinct anthozoan skeletonized lineages. Therefore, scleractinian corals most likely evolved from Paleozoic soft-bodied ancestors. Modern shallow-water Scleractinia, which are dependent on symbionts, appear to have had several independent origins from solitary, non-symbiotic precursors. The Scleractinia have survived periods of massive climate change in the past, suggesting that as a lineage they may be less vulnerable to future changes than often assumed.

The New Systematics of Scleractinia: Integrating Molecular and Morphological Evidence

“…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.…”

“…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 future of evolutionary diversity in reef corals

“…On the other hand, PD has been shown to poorly capture trait or functional diversity [19,103] especially on a regional scale [44,45]. More importantly, the most recent common ancestor of modern reef corals probably lived about 400 million years ago in the Palaeozoic [58], and many major coral lineages are relatively old [36]. Given their long history it is likely that some of the old lineages (e.g.…”

“…We used BEAST 1.8 [55][56][57] to fit the DNA sequence data mentioned above onto the supertree topology using fossil node calibrations detailed in Stolarski et al [58]. These calibrations date the origins of Caryophyllia to the Oxfordian (Late Jurassic), Dendrophylliidae to the Barremian (Early Cretaceous) and Flabellum to the Campanian (Late Cretaceous).…”