Evolutionary History of Photosymbiosis and Its Implications for the Future of Reefs

Photosymbiosis is a common, plastic, and very powerful evolutionary strategy that has most likely been extant on earth since at least the early Proterozoic and possibly much longer (>2.5 Ga). It is ancient, repetitive and polyphyletic across many symbiont types and hosts, indicating that it is a highly successful strategy driven by strong selection. All major eukaryotic groups have extant and ancient photosymbiosis along a continuum. Dinoflagelates and diatoms, hosted by diverse animals, fungi, foraminifera, radiolaria, and ciliates, are loosely associated photosymbioses. Intermediate are the plastid nucleomorphs in cryptomonads and chlorarachniophytes. Complete association occurs in eukaryotic algae harboring genomically-integrated plastids that evolved long ago.

Six major extinction events decimated photosymbionts and reefs in the Phanerozoic. Both reradiated within a few million years. Photosymbionts likely re-evolved, just as metazoans did, to flourish with new reefs. They tolerated periods of extreme CO2 concentrations far exceeding those predicted for the near future. Pleistocene fluctuations of temperature (several degrees) and CO2 (~180 to >300 ppm) had little effect on reefs or symbionts. In modern seas, photosymbionts like Symbiodinium occur in distinct genetic clades (up to seven?) with seemingly different ecologic and habitat requirements in some clades that live in many different metazoan and protistan hosts on the same reef. Their variety, ecologies and hosts indicate that symbionts a large pool that functions across the entire reef. Photosynthetically-driven reefs are complex, integrated ecosystems selected for resistance to shallow-water disturbances and variations, likely driven by the need for light. Only major oceanic reorganization on the scale of the major natural extinctions was sufficient to cause extinction on photoendosymbiotic reefs in the past. Thus reefs are not fragile but resilient, and although they may experience temporary bleaching and population changes, they are unlikely to become extinct due to these symbiont-related phenomena.