The role of vertical symbiont transmission in altering cooperation and fitness of coral-Symbiodinium symbioses

Abstract

The coral symbiosis is the linchpin of the reef ecosystem, yet the mechanisms that promote and maintain cooperation between hosts and symbionts have not been fully resolved. We used a phylogenetically controlled design to investigate the role of vertical symbiont transmission, an evolutionary mechanism in which symbionts are inherited directly from parents, predicted to enhance cooperation and holobiont fitness. Six species of coral, three vertical transmitters and their closest horizontally transmitting relatives, which exhibit environmental acquisition of symbionts, were fragmented and subjected to a two-week thermal stress experiment. Symbiont cell density, photosynthetic function and translocation of photosynthetically fixed carbon between symbionts and hosts were quantified to assess changes in physiological performance and cooperation. All species exhibited similar decreases in symbiont cell density and net photosynthesis in response to elevated temperature, consistent with the onset of bleaching. Yet baseline cooperation, i.e. translocation of photosynthate, in ambient conditions and the reduction in cooperation in response to elevated temperature differed among species. Although Porites lobata and Galaxea acrhelia did exhibit the highest levels of baseline cooperation, we did not observe universally higher levels of cooperation in vertically transmitting species. Post hoc sequencing of the Symbiodinium ITS-2 locus was used to investigate the potential role of differences in symbiont community composition. Interestingly, reductions in cooperation at the onset of bleaching tended to be associated with increased symbiont community diversity among coral species. The theoretical benefits of evolving vertical transmission are based on the underlying assumption that the host-symbiont relationship becomes genetically uniform, thereby reducing competition among symbionts. Taken together, our results suggest that it may not be vertical transmission per se that influences host-symbiont cooperation, but genetic uniformity of the symbiont community, although additional work is needed to test this hypothesis.