Microhabitat acclimatization alters sea anemone–algal symbiosis and thermal tolerance across the intertidal zone

Contemporary symbioses in extreme environments can give an insight into mechanisms that stabilize species interactions during environmental change. The intertidal sea anemone, Anthopleura elegantissima, engages in a nutritional symbiosis with microalgae similar to tropical coral, but withstands more intense environmental fluctuations during tidal inundations. In this study, we compare baseline symbiotic traits and their sensitivity to thermal stress within and among anemone aggregations across the intertidal using a laboratory-based tank experiment to better understand how fixed genotypic and plastic environmental effects contribute to the successful maintenance of this symbiosis in extreme habitats. High intertidal anemones had lower baseline symbiont-to-host cell ratios under control conditions, but their symbionts had higher baseline photosynthetic efficiency compared to low intertidal anemone symbionts. Symbiont communities were identical across all samples, suggesting that shifts in symbiont density and photosynthetic performance could be an acclimatory mechanism to maintain symbiosis in different environments. Despite lower baseline symbiont-to-host cell ratios, high intertidal anemones maintained greater symbiont-to-host cell ratios under heat stress compared with low intertidal anemones, suggesting greater thermal tolerance of high intertidal holobionts. However, the thermal tolerance of clonal anemones acclimatized to different zones was not explained by tidal height alone, indicating additional environmental variables contribute to physiological differences. Host genotype significantly influenced anemone weight, but only explained a minor proportion of variation among symbiotic traits and their response to thermal stress, further implicating environmental history as the primary driver of holobiont tolerance. These results indicate that this symbiosis is highly plastic and may be able to acclimatize to climate change over ecological timescales, defying the convention that symbiotic organisms are more susceptible to environmental stress.