Abstract

Coral reefs are under major threat from ocean warming. When temperatures become too high corals bleach, expelling their symbiotic, photosynthetic microalgae (Symbiodinium), which they depend on for much of their nutritional requirements. Prolonged bleaching has led to widespread coral mortality and the severity and frequency of bleaching events are predicted to increase in the future. Coral bleaching tolerance is influenced by the thermal tolerance of the Symbiodinium harboured, and these microbial members of the coral holobiont may be able to evolve more rapidly than the coral host itself. Here, we examined the response of replicate cultures of five genetically distinct Symbiodinium strains (A3c, two types of D1, G3, and F1) to increasing temperatures over the course of approximately one year. For three Symbiodinium types (types A3c, G3, and F1), we observed a stable adaptive change at the end of this exposure period, which equated to only 41-69 asexual generations. The long-term selected Symbiodinium culture replicates (SS) showed faster growth rates under short-term, acute heat stress, and in some cases higher photosynthetic efficiencies, compared to wild-type populations (WT). Our results considerably extend the field of experimental evolution in Symbiodinium and with further work into the Symbiodinium-coral association and bleaching response, this approach may become a valuable tool in coral reef conservation and restoration initiatives.

Highlights

  • Coral reefs are the most biodiverse ecosystem in the marine world, contributing billions of dollars’ worth of ecosystem services through tourism, coastal protection and fishing industries, with invaluable cultural and medicinal significance (Moberg and Folke, 1999)

  • Two Symbiodinium types, F1 and G3, were able to grow at the ratchet temperature of 31◦C with all three selected Symbiodinium (SS) populations of both types cultured at 31◦C for up to 69 and 53 generations, respectively

  • Symbiodinium A3c Two of the A3c SS populations (SS@30a and SS@30c) were able to grow significantly faster than the WT@30 population by up to 49% (±8.80%) after longterm culture at 30◦C, with the growth rate of population SS@30a being significantly faster than the WT@27 (t2 = 3.51, P = 0.04, Table S1), by 28% (±7.53% Figure 2A)

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Summary

Introduction

Coral reefs are the most biodiverse ecosystem in the marine world, contributing billions of dollars’ worth of ecosystem services through tourism, coastal protection and fishing industries, with invaluable cultural and medicinal significance (Moberg and Folke, 1999). Reefbuilding corals are under serious threat from rapid ocean warming, driven by global warming, as a consequence of rising anthropogenic carbon emissions. The unprecedented rate of global change is considered too rapid for many marine organisms to keep up, leading to the prediction of mass species extinction by the end of the century (Hoegh-Guldberg and Bruno, 2010; Pereira et al, 2010; Dawson et al, 2011; Pacifici et al, 2015; Urban, 2015). Increases in temperature are one of the main causes of coral bleaching, whereby corals’ symbiotic algae, Symbiodinium spp., are lost from coral tissue in a stress response driven by the Symbiodinium and/or the coral (Pandolfi et al, 2011). Even if corals can re-establish a symbiosis when temperatures return to normal, they may be left prone to disease (e.g., Kushmaro et al, 1997; Harvell et al, 1999; Howells et al, 2016), show reduced growth and can be reproductively compromised (e.g., Baird and Marshall, 2002; Miller et al, 2009)

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