"Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition

Abstract

Endosymbiotic dinoflagellates, or "zooxanthellae," are required for the survival of a diverse community of invertebrates that construct and dominate shallow, tropical coral reef ecosystems. Molecular systematics applied to this once understudied symbiont partner, Symbiodinium spp., divide the group into divergent lineages or subgeneric "clades." Within each clade, numerous closely related "types," or species, exhibit distinctive host taxon, geographic, and/or environmental distributions. This diversity is greatest in clade C, which dominates the Indo-Pacific host fauna and shares dominance in the Atlantic-Caribbean with clade B. Two "living" ancestors in this group, C1 and C3, are common to both the Indo-Pacific and Atlantic-Caribbean. With these exceptions, each ocean possesses a diverse clade C assemblage that appears to have independently evolved (adaptively radiated) through host specialization and allopatric differentiation. This phylogeographic evidence suggests that a worldwide selective sweep of C1/C3, or their progenitor, must have occurred before both oceans separated. The probable timing of this event corresponds with the major climactic changes and low CO(2) levels of the late Miocene and/or early Pliocene. Subsequent bursts of diversification have proceeded in each ocean since this transition. An ecoevolutionary expansion to numerous and taxonomically diverse hosts by a select host-generalist symbiont followed by the onset of rapid diversification suggests a radical process through which coral-algal symbioses respond and persist through the vicissitudes of planetary climate change.