Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Abstract

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Keywords: Cnidarian; Collaborative; Community; Coral; Genetic diversity; ITS2; Population; Species; Symbiodiniaceae; Symbiosis.

Figure 1. A representation of the various degrees of complexity in Symbiodiniaceae genetic diversity among different habitats (e.g., cultures, corals, and sediments).

Communities of Symbiodiniaceae within a given sample can encompass multiple strains, populations, species, and genera.

Figure 2. A simplified representation of Symbiodiniaceae speciation, species concepts (SC), and associated biological evidence.

In this example, one ancestral species splits and diverges to become two descendant lineages after barriers to gene flow are established. Through selection and drift, these lineages evolve different properties, which satisfy the criteria of different species concepts (represented by horizontal lines). Because these properties may arise at different times and in different orders, there is a “gray zone” where conflict among species concepts may result in controversy about whether one or two species exist. Modified from De Queiroz (2007) and Leliaert et al. (2014).

Figure 3. Recommendations for designing microsatellite-based Symbiodiniaceae population genetics experiments.

Sample collection, marker choice, and analytical pipeline should be considered from the outset.

Figure 4. An example of ITS2 rDNA copy number variation (CNV) between the genomes of two Symbiodiniaceae species from different genera (Breviolum minutum and Cladocopium goreaui).

Bar graphs demonstrate how original, uncorrected values (lighter bars) can lead to inaccurate perceptions regarding the proportional representation and numerical dominance of a species. In this case, raw C. goreaui ITS2 counts need to be divided by ~10 to correct for CNV (darker bars). Modified from Saad et al. (2020).

Figure 5. Considerations for efforts to measure Symbiodiniaceae phenotypes across three states (axenic monoclonal culture, xenic monoclonal culture, and in hospite).