Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

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.journal articl

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

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

The population genetic structure of coral reef fishes on the Great Barrier Reef

The population genetic structure of species may be determined by complex interactions among many ecological, evolutionary and genetic processes. I investigated the population genetic structure of coral reef fishes on the Great Barrier Reef (GBR), Australia to better understand how these various processes may interact in a natural system. I firstly examined the spatial genetic structure of a low dispersal species to determine if its genetic structure varied among spatial scales and among regions located in the centre and on the periphery of its distributional range. I then examined the population genetic structure of species with different dispersal potentials and among species sampled at central and peripheral locations in their species range. Using mtDNA control region sequences and three microsatellite loci, I examined the spatial genetic structure of a direct developing coral reef fish, Acanthochromis polyacanthus, with comparatively low dispersal rates. The spatial genetic structure of this species was scale-dependent with evidence of isolation-by-distance among regions, but not within regions. Very strong genetic structure was detected among reefs within regions consistent with a metapopulation model. Pairwise genetic distances increased from offshore and older populations, to inshore and younger ones, supporting a metapopulation propagule-pool model of colonisation. Genetic diversities, mismatch, and coalescence analyses all identified large variation in the demographic history of this species among populations and regions. Evidence of genetic bottlenecks was detected by mismatch analysis in the majority of populations sampled, but in most populations these bottlenecks appeared to be older since genetic diversities and coalescence based population growth estimates did not indicate recent genetic bottlenecks. In contrast, three populations displayed low genetic diversities and large population growth rates indicating a more recent genetic bottleneck. Reductions in genetic diversities of local populations resulted in overall lower genetic diversity and a higher regional expansion rate in the southern region located towards the distributional margin of this species. In all, these results suggest that A. polyacanthus exists as a metapopulation within regions on the GBR and that metapopulation dynamics may differ among regions located in the centre and on the periphery of this species. The pelagic larval duration (PLD) can both affect and record the ecology and evolution of coral reef fishes and emerging evidence suggests that this trait displays considerable intraspecific variation. Here I present new estimates of PLD for ten species of Pomacentridae and two species of Gobiidae, and coupled with previously published estimates, examine spatial and temporal variation of PLDs within and among these species. In eight of the twelve species examined here, within-population mean PLDs differed between sampling times, locations within regions, and among regions. In contrast, the range of these same PLD estimates overlapped at all spatial and temporal scales examined in eleven of the twelve species, but not between regions in one species (Amphiprion melanopus). Therefore, despite tight error estimates typically associated with estimates of PLD taken from a particular population at a particular time in some taxa, the overlapping ranges in PLD reported here indicate that the length of the pelagic larval phase is a much more plastic trait than previously appreciated. Pelagic larval duration (PLD) is a commonly used proxy for dispersal potential in coral reef fishes. Here I examine the relationship between PLD, genetic structure and genetic variability in coral reef fishes from one family (Pomacentridae) that differ in mean larval duration by more than a month. Genetic structure was estimated in eight species using a mitochondrial molecular marker (control region) and in a sub-set of five species using nuclear molecular markers (ISSRs). Estimates of genetic differentiation were similar among species with pelagic larvae, but differed between molecular markers. The mtDNA indicated no structure while the ISSR indicated some structure between the sampling locations. I detected a relationship between PLD and genetic structure using both markers. These relationships, however, were caused by a single species, Acanthochromis polyacanthus, which differs from all the other species examined here in lacking a larval phase. With this species excluded, there was no relationship between PLD and genetic structure using either marker. Genetic diversities were generally high in all species and did not differ significantly among species and locations. Nucleotide diversity and total heterozygosity were negatively related to maximum PLD, but again, these relationships were caused by A. polyacanthus and disappeared when this species was excluded from these analyses. These genetic patterns are consistent with moderate gene flow among well-connected locations and indicate that at this phylogenetic level (i.e., within family) the duration of the pelagic larval phase is not the primary factor affecting patterns of genetic differentiation. Using mtDNA (control region) and nuclear (ISSR) markers, I investigated the population genetic structure of three congeneric species pairs of pomacentrid coral reef fishes (Pomacentridae) in the context of species’ borders theory. This theory predicts that population located on the periphery of the species’ range should be smaller and more fragmented and hence, display stronger genetic structure and lower genetic diversities compared to more centrally located populations. Each species pair consisted of one species sampled at two central locations within its geographic range, and another species sampled at the same locations but which constituted one location toward the centre of its range and another close to its edge. Contrary to expectations from theory, I did not find the predicted border effects in the population genetic structure of the species examined. Gene flow estimates did not differ among central and peripheral species. Genetic diversities were not lower in peripheral populations compared to central populations or in species sampled towards the periphery compared to those sampled in the centre of their ranges. Indeed, genetic diversities were much greater in the peripheral species compared to their central counterparts. The distribution of genetic variation indicated that secondary contact among differentiated lineages may, in part, be responsible for the high genetic diversity in these peripheral species. Elevated mutation rates mediated by environmental stress on the species’ margin may have contributed further genetic variability in these species

Infection dynamics vary between Symbiodinium types and cell surface treatments during establishment of endosymbiosis with coral larvae

Symbioses between microbes and higher organisms underpin high diversity in many ecosystems, including coral reefs, however mechanisms underlying the early establishment of symbioses remain unclear. Here we examine the roles of Symbiodinium type and cell surface recognition in the establishment of algal endosymbiosis in the reef-building coral, Acropora tenuis. We found 20–70% higher infection success (proportion of larvae infected) and five-fold higher Symbiodinium abundance in larvae exposed to ITS-1 type C1 compared to ITS-1 type D in the first 96 h following exposure. The highest abundance of Symbiodinium within larvae occurred when C1-type cells were treated with enzymes that modified the 40–100 kD glycome, including glycoproteins and long chain starch residues. Our finding of declining densities of Symbiodinium C1 through time in the presence of intact cell surface molecules supports a role for cell surface recognition molecules in controlling post-phagocytosis processes, leading to rejection of some Symbiodinium types in early ontogeny. Reductions in the densities of unmodified C1 symbionts after 96 h, in contrast to increases in D symbionts may suggest the early initiation of a winnowing process contributing to the establishment of Symbiodinium D as the dominant type in one-month old juveniles of A. tenuis

Isolation, characterisation and cross amplification of thirteen microsatellite loci for coral endo-symbiotic dinoflagellates (Symbiodinium clade C)

The health and productivity of coral reefs is underpinned by the symbiosis between corals and dinoflagellates\ud (Symbiodinium spp.). To enable population genetic analyses of Symbiodinium spp, required for coral reef conservation, seven microsatellite loci were isolated from Symbiodinium clade C from the Great Barrier Reef, Australia. These microsatellite primer pairs consistently amplified between 1 and 8 alleles per coral host colony, with mean number of alleles ranging from 1.9 to 4.0 and generally high genetic diversities (Shannon’s Index = 0.71–2.76). The novel microsatellite loci amplified between 1 and 10 alleles in four other C strains, but did not amplify a D strain.\ud Three of six previously published clade C microsatellite loci amplified 1–6 alleles in two or more of five C strains tested. The primers and cross amplifications presented here therefore provide a useful tool for elucidating the population genetic structure of clade C Symbiodinium populations

A framework for understanding climate change impacts on coral reef social–ecological systems

International audienceCorals and coral-associated species are highly vulnerable to the emerging effects of global climate change. The widespread degradation of coral reefs, which will be accelerated by climate change, jeopardizes the goods and services that tropical nations derive from reef ecosystems. However, climate change impacts to reef social–ecological systems can also be bi-directional. For example, some climate impacts, such as storms and sea level rise, can directly impact societies, with repercussions for how they interact with the environment. This study identifies the multiple impact pathways within coral reef social–ecological systems arising from four key climatic drivers: increased sea surface temperature, severe tropical storms, sea level rise and ocean acidification. We develop a novel framework for investigating climate change impacts in social–ecological systems, which helps to highlight the diverse impacts that must be considered in order to develop a more complete understanding of the impacts of climate change, as well as developing appropriate management actions to mitigate climate change impacts on coral reef and people

Building Consensus around the Assessment and Interpretation of Symbiodiniaceae Diversity

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