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.coral reefs | Bayes Traits | zooxanthellae | ancestral state reconstruction | phylogeny I n most marine organisms, coloniality is thought to have evolved from solitary ancestors and proceeded through progressive weakening of zooidal individuality in favor of increased individualization of the colony (1). In Scleractinia, colonial species are thought to have originated from solitary ancestors, most likely via incomplete asexual budding (2). This notion is almost intuitive, since all sexually produced coral colonies start as a larva that metamorphoses into a single polyp. Colonial integration supposedly increased in evolutionary time through dissolution of skeletal barriers among polyps (2-4). This range of morphological variability is in full display in extant Scleractinia, from the exclusively solitary species within the genus Anthemiphyllia, to the "quasicolonial" Anomocora carinata, in which "the daughter corallites [break] free of the parent before a third generation bud appears" (5), to the loosely integrated colonies of Rhizosmilia maculata in which partial colonial mortality may yield solitary daughter polyps and finally the highly integrated colonies of Favia favus, in which polyp damage invariably results in a colony-wide regenerative response (6). Although most...

The New Systematics of Scleractinia: Integrating Molecular and Morphological Evidence

“…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).…”

Forgotten in the taxonomic literature: resurrection of the scleractinian coral genusSclerophyllia(Scleractinia, Lobophylliidae) from the Arabian Peninsula and its phylogenetic relationships

“…The taxonomic relevance of the solitary condition in corals has been revised in light of molecular phylogeny reconstructions published in recent years. Barbeitos, Romano, and Lasker (2010) provided robust phylogenetic evidence that polystomatism has been repeatedly acquired and/or lost throughout the history of the order Scleractinia. These findings have been subsequently corroborated by detailed phylogenetic analyses revealing that evolution from a solitary to a colonial condition, and the reverse, in the Fungiidae and Dendrophylliidae Gray, 1847, has occurred frequently in these two families characterized by congeneric monostomatous and polystomatous species (Arrigoni et al, 2014c;Gittenberger et al, 2011).…”

Middle Triassic Coral Growth Bands and Their Implication for Photosymbiosis

“…This appears to have merit. Severance of the link between corals and photosymbionts was proposed to explain the reef collapse at the end of the Late Triassic (Stanley and Van de Schootbrugge, 2009) and recent molecular analysis has revealed that both coloniality and symbiosis were repeatedly acquired and or lost throughout the history of the Scleractinia (Barbeitos et al, 2010).…”