Theory suggests that the direct transmission of endosymbionts from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile’s ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following acquisition, similar changes occurred in larval energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the algae did not provide the energetic benefits characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host’s life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.

Hartmann_etal_MEC_Fig_1_dataThe gene expression data obtained from Orbicella faveolata larvae and used to generate Figure 1. The data matrix was filtered to only the genes that successfully hybridized (i.e., produced data) in at least three replicates for each treatment. Missing values were imputed and all values were normalized to a mean of zero and the same unit variance in each gene. The 'Name' column provides the gene annotation, if there is one. The subsequent columns contain data for the 20 samples. The sample names refer treatment group, which includes light status (L = Light, D = Dark), symbiont status (S = Symb, NS = NoSymb), and replicate number (1-5).Hartmann_etal_MEC_Fig_2_dataThe lipid content of Orbicella faveolata larvae used to generate Figure 2. Data were taken at the time of photosymbiont infection (T = 0) and two days later (T = 48) for the four treatment groups. Data columns contain lipid quantifications (µg/larva) for the lipid classes WE = wax esters, TAG = triacylglycerol, and PL = phospholipids.Hartmann_etal_MEC_Fig_3_dataThe behavioral responses of Orbicella faveolata larvae to photosymbiont infection with cells obtained from conspecific adults on the natal reef and presented in Figure 3.Hartmann_etal_MEC_Fig_4_dataThe behavioral responses of Orbicella faveolata larvae to photosymbiont infection with cells obtained from two cultured species and presented in Figure 4. The photosymbiont species include Breviolum minutum and Symbiodinium microadriaticum.