The advent of molecular data has transformed the science of organizing and studying life on Earth. Genetics-based evidence provides fundamental insights into the diversity, ecology, and origins of many biological systems, including the mutualisms between metazoan hosts and their micro-algal partners. A well-known example is the dinoflagellate endosymbionts ("zooxanthellae") that power the growth of stony corals and coral reef ecosystems. Once assumed to encompass a single panmictic species, genetic evidence has revealed a divergent and rich diversity within the zooxanthella genus Symbiodinium. Despite decades of reporting on the significance of this diversity, the formal systematics of these eukaryotic microbes have not kept pace, and a major revision is long overdue. With the consideration of molecular, morphological, physiological, and ecological data, we propose that evolutionarily divergent Symbiodinium "clades" are equivalent to genera in the family Symbiodiniaceae, and we provide formal descriptions for seven of them. Additionally, we recalibrate the molecular clock for the group and amend the date for the earliest diversification of this family to the middle of the Mesozoic Era (∼160 mya). This timing corresponds with the adaptive radiation of analogs to modern shallow-water stony corals during the Jurassic Period and connects the rise of these symbiotic dinoflagellates with the emergence and evolutionary success of reef-building corals. This improved framework acknowledges the Symbiodiniaceae's long evolutionary history while filling a pronounced taxonomic gap. Its adoption will facilitate scientific dialog and future research on the physiology, ecology, and evolution of these important micro-algae.Copyright © 2018 The Author(s). Published by Elsevier Ltd.. All rights reserved.

Reef-building corals rely on intracellular algal symbionts to meet energetic demands. Increasing extreme weather driven by climate change often leads to disruption of this symbiosis and to coral death. Corals can better withstand stress after previous exposure to sublethal conditions, but the mechanisms for this resilience remain unclear. Here we show that a three-day thermal preconditioning increases tolerance of acute heat stress through modulations in cell death pathways in the stony coral Pocillopora acuta. In preconditioned corals, the ratio of pro-survival (pa-Bcl-2 and pa-BI-1) to pro-death (pa-BAK and pa-BAX) gene expression increased and the corals underwent significantly less bleaching. When treated with Bcl-2 inhibitor, corals lost the improved thermal tolerance, suggesting an important role of programmed cell death in coral bleaching and acclimatization. During heat stress, the activity of acid phosphatase increased but caspase-3 did not, suggesting the involvement of autophagy/symbiophagy rather than apoptosis in this process. A similar shift in gene expression also occurs in thermally stressed corals that have been exposed to naturally higher temperatures during summer thermal maxima in Kāne'ohe Bay, Hawai'i, suggesting that corals can increase their resilience to realistic warming events during high-risk periods through alterations in cell signaling. These data suggest that programmed cell death pathways underly coral acclimatization and resilience and may be important for coral reef conservation and management.This article is protected by copyright. All rights reserved.

Most of the work on the impact of elevated temperature and light on Symbiodinium-invertebrate symbioses have focused primarily on how the photosynthetic (algal) partner is impacted. Understanding how the same stresses affect the invertebrate host, however, is in its infancy. In this study, we re-examined the direct effect of elevated temperatures on the invertebrate host exploring the early transcriptional response of aposymbiotic (without algal symbionts) coral larvae. The temperatures tested in the experimental design were 24 degrees C (ambient seawater temperature), 28 degrees C and 31 degrees C; and the sampling points were 3 and 10 h after temperature exposure. We explored relative changes in transcription using a cDNA microarray constructed for the scleractinian coral, Acropora millepora, and containing 18 142 expressed sequence tag (EST) clones/8386 unigenes. Our study identified 29 genes that were significantly up- and down-regulated when A. millepora coral larvae were exposed to elevated temperatures. Down-regulation of several key components of DNA/RNA metabolism was detected implying inhibition of general cellular processes. The down-regulation of protein synthesis, however, was not simple and random, which suggested that the stress response was a more complicated adjustment of cellular metabolism. We identified four significant outcomes during the very early hours of the transcriptional response to hyperthermal stress in coral larvae. First, the expression of heat-shock proteins increased rapidly (within 3 h) in response to hyperthermal stress. Second, a fluorescent protein homologue, DsRed-type FP, decreased its expression in response to elevated temperature reinforcing a potential role as a molecular marker for monitoring hyperthermal stress in nature. Third, the down-regulation of a coral mannose-binding C-type lectin under elevated temperature suggests that heat stress might compromise some components of the coral immune defence and therefore might bring about susceptibility to pathogenic diseases. And last, genes involved in protecting cells against oxidative stress showed little response at the early hours to heat stress, supporting the proposal that up-regulation of cnidarian host oxidative stress genes may require reactive oxygen species generated by stressed algal symbionts.