Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts

Abstract

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.

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

“…As bleaching is typically initiated by oxidative damage to Symbiodiniaceae and/or host cells (Oakley & Davy, ), any enhancements to the heat tolerance of Symbiodiniaceae partners is expected to confer bleaching resistance in the symbiosis. A diversity of Symbiodiniaceae taxa from at least four genera ( Symbiodinium , Breviolum , Cladocopium , Durusdinium ; formerly, Symbiodinium clades A–D; LaJeunesse et al, ) routinely associate with corals (reviewed by Coffroth & Santos, ). Heat tolerance varies widely among and within these genera (Swain, Chandler, Backman, & Marcelino, ; Tchernov et al, ), theoretically providing the opportunity for corals to replace sensitive symbionts with more tolerant taxa (Buddemeier & Fautin, ).…”

Environmental latitudinal gradients and host‐specificity shape Symbiodiniaceae distribution in Red Sea Porites corals

“…Different patterns of host–symbiont associations have been documented in response to latitudinal, longitudinal and environmental gradients, for various geographic locations and host taxa (Huang et al, ; Hume et al, , ; Keshavmurthy et al, ; Oliver & Palumbi, ; Tonk, Sampayo, Chai, Schrameyer, & Hoegh‐Guldberg, ; Ziegler, Roder, Büchel, & Voolstra, ). Nevertheless, our knowledge of the specificity and diversity of these associations is still poor, limiting our understanding of the ecological benefits that different associations provide (LaJeunesse et al, ).…”

Transcriptomic resilience, symbiont shuffling, and vulnerability to recurrent bleaching in reef‐building corals

“…These changes to disturbance regimes are gradually eroding the capacity of marine populations to recover from heat stress. Ocean warming is particularly stressful on coral reefs, where thermal stress triggers the breakdown of the symbiotic relationship between the coral host and their photosynthetic algal endosymbiont (family Symbiodiniaceae [LaJeunesse et al, ]). This process is known as coral bleaching.…”