Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis

Coral endosymbionts in the dinoflagellate genus Symbiodinium are known to impact host physiology and have led to the evolution of reef-building, but less is known about how symbiotic communities in early life-history stages and their interactions with host parental identity shape the structure of coral communities on reefs. Differentiating the roles of environmental and biological factors driving variation in population demographic processes, particularly larval settlement, early juvenile survival and the onset of symbiosis is key to understanding how coral communities are structured and to predicting how they are likely to respond to climate change. We show that maternal effects (that here include genetic and/or effects related to the maternal environment) can explain nearly 24% of variation in larval settlement success and 5–17% of variation in juvenile survival in an experimental study of the reef-building scleractinian coral, Acropora tenuis. After 25 days on the reef, Symbiodinium communities associated with juvenile corals differed significantly between high mortality and low mortality families based on estimates of taxonomic richness, composition and relative abundance of taxa. Our results highlight that maternal and familial effects significantly explain variation in juvenile survival and symbiont communities in a broadcast-spawning coral, with Symbiodinium type A3 possibly a critical symbiotic partner during this early life stage

Meta-population structure in a coral reef fish demonstrated by genetic data on patterns of migration, extinction and re-colonisation

Background: Management strategies for coral reefs are dependant on information about the spatial population structure and connectivity of reef organisms. Genetic tools can reveal important information about population structure, however, this information is lacking for many reef species. We used a mitochondrial molecular marker to examine the population genetic structure and the potential for meta-population dynamics in a direct developing coral reef fish using 283 individuals from 15 reefs on the Great Barrier Reef, Australia. We employed a hierarchical sampling design to test genetic models of population structure at multiple geographical scales including among regions, among shelf position and reefs within regions. Predictions from island, isolation-by-distance and meta-population models, including the potential for asymmetric migration, local extinction and patterns of re-colonisation were examined.\ud \ud Results: Acanthochromis polyacanthus displayed strong genetic structure among regions (ΦST = 0.81, P < 0.0001) that supported an equilibrium isolation-by-distance model (r = 0.77, P = 0.001). Significant structuring across the continental shelf was only evident in the northern region (ΦST = 0.31, P < 0.001) and no evidence of isolation-by-distance was found within any region. Pairwise ΦST values indicated overall strong but variable genetic structure (mean ΦST among reefs within regions = 0.28, 0.38, 0.41), and asymmetric migration rates among reefs with low genetic structure. Genetic differentiation among younger reefs was greater than among older reefs supporting a meta-population propagule-pool colonisation model. Variation in genetic diversities, demographic expansion and population growth estimates indicated more frequent genetic bottlenecks/founder effects and subsequent population expansion in the central and southern regions compared to the northern one.\ud \ud Conclusion: Our findings provide genetic evidence for meta-population dynamics in a direct developing coral reef fish and we reject the equilibrium island and isolation-by distance models at local spatial scales. Instead, strong non-equilibrium genetic structure appears to be generated by genetic bottlenecks/founder effects associated with population reductions/extinctions and asymmetric migration/(re)-colonisation of such populations. These meta-population dynamics varied across the geographical range examined with edge populations exhibiting lower genetic diversities and higher rates of population expansion than more central populations. Therefore, coral reef species may experience local population reductions/extinctions that promote overall meta-population genetic differentiation

Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis

Coral endosymbionts in the dinoflagellate genus Symbiodinium are known to impact host physiology and have led to the evolution of reef-building, but less is known about how symbiotic communities in early life-history stages and their interactions with host parental identity shape the structure of coral communities on reefs. Differentiating the roles of environmental and biological factors driving variation in population demographic processes, particularly larval settlement, early juvenile survival and the onset of symbiosis is key to understanding how coral communities are structured and to predicting how they are likely to respond to climate change. We show that maternal effects (that here include genetic and/or effects related to the maternal environment) can explain nearly 24% of variation in larval settlement success and 5–17% of variation in juvenile survival in an experimental study of the reef-building scleractinian coral, Acropora tenuis. After 25 days on the reef, Symbiodinium communities associated with juvenile corals differed significantly between high mortality and low mortality families based on estimates of taxonomic richness, composition and relative abundance of taxa. Our results highlight that maternal and familial effects significantly explain variation in juvenile survival and symbiont communities in a broadcast-spawning coral, with Symbiodinium type A3 possibly a critical symbiotic partner during this early life stage

Heritability of the Symbiodinium community in vertically-and horizontally-transmitting broadcast spawning corals

The dinoflagellate-coral partnership influences the coral holobiont's tolerance to thermal stress and bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of the initial Symbiodinium communities for two broadcast-spawning corals with different symbiont transmission modes: Acropora tenuis has environmental acquisition, whereas Montipora digitata has maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parents, juveniles and eggs, we describe previously undocumented Symbiodinium diversity and dynamics in both corals. After one month of uptake in the field, Symbiodinium communities associated with A. tenuis juveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances conserved between experiments in two years. M. digitata eggs were predominantly characterized by C15, D1, and A3. In contrast to current paradigms, host genetic influences accounted for a surprising 29% of phenotypic variation in Symbiodinium communities in the horizontally-transmitting A. tenuis, but only 62% in the vertically-transmitting M. digitata. Our results reveal hitherto unknown flexibility in the acquisition of Symbiodinium communities and substantial heritability in both species, providing material for selection to produce partnerships that are locally adapted to changing environmental conditions

Evolutionary consequences of DNA methylation in a basal Metazoan

Gene body methylation (gbM) is an ancestral and widespread feature in Eukarya, yet its adaptive value and evolutionary implications remain unresolved. The occurrence of gbM within protein-coding sequences is particularly puzzling, because methylation causes cytosine hypermutability and hence is likely to produce deleterious amino acid substitutions. We investigate this enigma using an evolutionarily basal group of Metazoa, the stony corals (order Scleractinia, class Anthozoa, phylum Cnidaria). We show that patterns of coral gbM are similar to other invertebrate species, predicting wide and active transcription and slower sequence evolution. We also find a strong correlation between gbM and codon bias, resulting from systematic replacement of CpG bearing codons. We conclude that gbM has strong effects on codon evolution and speculate that this may influence establishment of optimal codons

Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral

Sensitive molecular analyses show that most corals host a complement of Symbiodinium genotypes that includes thermotolerant types in low abundance. While tolerant symbiont types are hypothesized to facilitate tolerance to temperature and recovery from bleaching, empirical data on their distribution and relative abundance in corals under ambient and stress conditions are still rare. We quantified visual bleaching and mortality of coral hosts, along with relative abundance of C- and D-type Symbiodinium cells in 82 Acropora millepora colonies from three locations on the Great Barrier Reef transplanted to a central inshore site over a 13 month period. Our analyses reveal dynamic change in symbiont associations within colonies and among populations over time. Coral bleaching and declines in C-but not D-type symbionts were observed in transplanted corals. Survival and recovery of 25% of corals from one population was associated with either initial D-dominance or an increase in D-type symbionts that could be predicted by a minimum pre-stress D:C ratio of 0.003. One-third of corals from this population became D dominated at the bleached stage despite no initial detection of this symbiont type, but failed to recover and died in mid to late summer. These results provide a predictive threshold minimum density of background D-type symbionts in A. millepora, above which survival following extreme thermal stress is increased

Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral

Sensitive molecular analyses show that most corals host a complement of Symbiodinium genotypes that includes thermotolerant types in low abundance. While tolerant symbiont types are hypothesized to facilitate tolerance to temperature and recovery from bleaching, empirical data on their distribution and relative abundance in corals under ambient and stress conditions are still rare. We quantified visual bleaching and mortality of coral hosts, along with relative abundance of C- and D-type Symbiodinium cells in 82 Acropora millepora colonies from three locations on the Great Barrier Reef transplanted to a central inshore site over a 13 month period. Our analyses reveal dynamic change in symbiont associations within colonies and among populations over time. Coral bleaching and declines in C-but not D-type symbionts were observed in transplanted corals. Survival and recovery of 25% of corals from one population was associated with either initial D-dominance or an increase in D-type symbionts that could be predicted by a minimum pre-stress D:C ratio of 0.003. One-third of corals from this population became D dominated at the bleached stage despite no initial detection of this symbiont type, but failed to recover and died in mid to late summer. These results provide a predictive threshold minimum density of background D-type symbionts in A. millepora, above which survival following extreme thermal stress is increased