The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral–algal associations

Abstract

Reef-building corals owe much of their success to a symbiosis with dinoflagellate microalgae in the genus Symbiodinium. In this association, the performance of each organism is tied to that of its partner, and together the partners form a holobiont that can be subject to selection. Climate change affects coral reefs, which are declining globally as a result. Yet the extent to which coral holobionts will be able to acclimate or evolve to handle climate change and other stressors remains unclear. Selection acts on individuals and evidence from terrestrial systems demonstrates that intraspecific genetic diversity plays a significant role in symbiosis ecology and evolution. However, we have a limited understanding of the effects of such diversity in corals. As molecular methods have advanced, so too has our recognition of the taxonomic and functional diversity of holobiont partners. Resolving the major components of the holobiont to the level of the individual will help us assess the importance of intraspecific diversity and partner interactions in coral–algal symbioses. Here, we hypothesize that unique combinations of coral and algal individuals yield functional diversity that affects not only the ecology and evolution of the coral holobiont, but associated communities as well. Our synthesis is derived from reviewing existing evidence and presenting novel data. By incorporating the effects of holobiont extended phenotypes into predictive models, we may refine our understanding of the evolutionary trajectory of corals and reef communities responding to climate change.

Intraspecific variation in growth rate is a poor predictor of fitness for reef corals

“…). Effectively, therefore, the present study evaluates the role of holobiont identity in determining the success of coral colonies, which is consistent with the notion that natural selection can act at this level (Parkinson and Baums ). High resolution genetic analyses of Symbiodinium identity over time in permanently marked corals would be required to resolve the role of symbiont variation in determining colony success, and such analyses probably would need to combined mensurative surveys with controlled laboratory experiments.…”

“…Genetic variation in functional traits allows organisms to respond in beneficial ways to differing conditions, and with profound changes in the environment expected as a result of climate change and ocean acidification (Doney et al. , IPCC ), the genotype‐fitness paradigm is receiving renewed attention to better understand which organisms will survive in the anthropocene (Parkinson and Baums , Barshis et al. , Gaylord et al.…”

“…). Intraspecific variation that is genetically determined creates the possibility for natural selection to improve the tolerance to future conditions of individual species (Fisher , Reusch ), or the holobiont (Parkinson and Baums ). For these possibilities to be realized, genetically determined aspects of coral performance must respond in beneficial ways to the rate at which environment conditions are changing (van Oppen et al.…”

Size-dependent physiological responses of the branching coralPocillopora verrucosato elevated temperature andPCO2

“…Finally, fundamental aspects of coral biology favor allometry. For example, as the density and genotypes of the Symbiodinium symbionts of most reef corals can vary among locations within a colony (Rowan et al, 1997;Kemp et al, 2008), and Symbiodinium genotypes can have unique physiological properties (Sampayo et al, 2008;Parkinson and Baums, 2014), large colonies with numerous microhabitats among their branches may be capable of hosting a wider range of Symbiodinium genotypes, so that the physiology of large versus small colonies will not be proportional to their difference in size. Integration among polyps also can favor allometry, and while it contradicts the key assumption of module independence that underpins the expectation of isometry in colonial modular designs (Hughes, 2005), it is facilitated by the common gastrovascular cavity of colonial corals.…”

Molecular characterization reveals the complexity of previously overlooked coral-exosymbiont interactions and the implications for coral-guild ecology

“…This preliminary assumption will need further investigation to be confirmed by obtaining more balanced sample sizes of types α and β from the same site. Furthermore, an effect of the host genet as a driver of exosymbiont community composition (e.g 5657…”