Phylogenetic analysis of symbiont transmission mechanisms reveal evolutionary patterns in thermotolerance and host specificity that enhance bleaching resistance among vertically transmitted Symbiodinium

Vertical transmission of Symbiodinium symbionts between generations of coral hosts has been hypothesized to result in superior matches between host and symbiont physiologies, and to form holobionts that are generally more resistant to thermal stress. Alternatively, horizontal transmission, with its greater potential for assembling physiologically diverse associations as well as being capable of substituting symbionts in response to stimuli, may result in holobionts that are generally more resistant to thermal stress. While the most common mode of transmission among Scleractinia-Symbiodinium symbioses is horizontal, mixed-modes transmission only occurs in vertically transmitting corals, allowing the maintenance of highly specialized associations across generations as well as transiently critical relationships. These advantages of mixed-modes transmission may serve to rescue otherwise susceptible corals, or alternatively, reinforce otherwise resistant corals, depending upon the other attributes of vertically transmitted Symbiodinium phylotypes. Here we ask if vertically transmitted symbionts tend to be more thermotolerant and specific. Because significant relationships between traits can be overestimated or obscured by patterns of shared evolutionary history, we inferred a novel molecular phylogeny for 97 Symbiodinium phylotypes representing clades A-F to evaluate the relationship between phylotype transmission-mode, thermotolerance and specificity to coral hosts. Thermotolerance and specificity have been independently derived multiple times during the evolutionary history of Symbiodinium, and cannot be predicted by clade membership. The probability of phylotype transmission being predominantly vertical increased by more than 200% across the observed ranges of increase of thermotolerance and specificity, even though phylotype thermotolerance is not correlated with host specificity. Higher thermotolerance and specificity of vertically transmitted Symbiodinium may contribute to robust bleaching resistance among vertically transmitting corals that could reinforce the potential benefits of mixed-modes transmission.