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Physiological performance, disease and bleaching prevalence are often patchy within individual coral colonies. These responses are largely influenced by coral-associated microbes, but how the coral microbiome changes over small spatial scales has never been quantified before. We performed a high-resolution quantification of the spatial scale of microbial species turnover (β-diversity) within skeletons of boulder-forming Porites corals. We found very strong prokaryotic species turnover across spatial scales ranging from 4 mm to 2 m within individual colonies, possibly resulting from dispersal limitation and microbial interactions. The microalgal community was more homogeneously distributed, which is likely due to these photosymbionts actively boring through limestone. Our findings highlight unprecedented levels of intra-colony heterogeneity in the skeletal microbiome, which has implications for the experimental design of coral microbiome studies and for our understanding of coral resilience.

Symbiodinium, the dinoflagellate photosymbiont of corals, is posited to become more susceptible to viral infections when heat-stressed. To investigate this hypothesis, we mined transcriptome data of a thermosensitive and a thermotolerant type C1 Symbiodinium population at ambient (27 °C) and elevated (32°C) temperatures. We uncovered hundreds of transcripts from nucleocytoplasmic large double-stranded DNA viruses (NCLDVs) and the genome of a novel positive-sense single-stranded RNA virus (+ssRNAV). In the transcriptome of the thermosensitive population only, +ssRNAV transcripts had remarkable expression levels in the top 0.03% of all transcripts at 27 °C, but at 32 °C, expression levels of +ssRNAV transcripts decreased, while expression levels of anti-viral transcripts increased. In both transcriptomes, expression of NCLDV transcripts increased at 32 °C, but thermal induction of NCLDV transcripts involved in DNA manipulation was restricted to the thermosensitive population. Our findings reveal that viruses infecting Symbiodinium are affected by heat stress and may contribute to Symbiodinium thermal sensitivity.

Reef-building corals possess a range of acclimatisation and adaptation mechanisms to respond to seawater temperature increases. In some corals, thermal tolerance increases through community composition changes of their dinoflagellate endosymbionts (Symbiodinium spp.), but this mechanism is believed to be limited to the Symbiodinium types already present in the coral tissue acquired during early life stages. Compelling evidence for symbiont switching, that is, the acquisition of novel Symbiodinium types from the environment, by adult coral colonies, is currently lacking. Using deep sequencing analysis of Symbiodinium rDNA internal transcribed spacer 2 (ITS2) PCR amplicons from two pocilloporid coral species, we show evidence consistent with de novo acquisition of Symbiodinium types from the environment by adult corals following two consecutive bleaching events. Most of these newly detected symbionts remained in the rare biosphere (background types occurring below 1% relative abundance), but one novel type reached a relative abundance of ~33%. Two de novo acquired Symbiodinium types belong to the thermally resistant clade D, suggesting that this switching may have been driven by consecutive thermal bleaching events. Our results are particularly important given the maternal mode of Symbiodinium transmission in the study species, which generally results in high symbiont specificity. These findings will cause a paradigm shift in our understanding of coral-Symbiodinium symbiosis flexibility and mechanisms of environmental acclimatisation in corals.

Corals rely on photosynthesis by their endosymbiotic dinoflagellates (Symbiodinium spp.) to form the basis of tropical coral reefs. High sea surface temperatures driven by climate change can trigger the loss of Symbiodinium from corals (coral bleaching), leading to declines in coral health. Different putative species (genetically distinct types) as well as conspecific populations of Symbiodinium can confer differing levels of thermal tolerance to their coral host, but the genes that govern dinoflagellate thermal tolerance are unknown. Here we show physiological and transcriptional responses to heat stress by a thermo-sensitive (physiologically susceptible at 32 °C) type C1 Symbiodinium population and a thermo-tolerant (physiologically healthy at 32 °C) type C1 Symbiodinium population. After nine days at 32 °C, neither population exhibited physiological stress, but both displayed up-regulation of meiosis genes by ≥ 4-fold and enrichment of meiosis functional gene groups, which promote adaptation. After 13 days at 32 °C, the thermo-sensitive population suffered a significant decrease in photosynthetic efficiency and increase in reactive oxygen species (ROS) leakage from its cells, whereas the thermo-tolerant population showed no signs of physiological stress. Correspondingly, only the thermo-tolerant population demonstrated up-regulation of a range of ROS scavenging and molecular chaperone genes by ≥ 4-fold and enrichment of ROS scavenging and protein-folding functional gene groups. The physiological and transcriptional responses of the Symbiodinium populations to heat stress directly correlate with the bleaching susceptibilities of corals that harbored these same Symbiodinium populations. Thus, our study provides novel, foundational insights into the molecular basis of dinoflagellate thermal tolerance and coral bleaching., (© The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

One characteristic of Indo-Pacific Acropora spp. is extremely high diversity in rDNA sequences at both the species and individual levels. In order to test the hypothesis that pseudogenes may contribute to this diversity, three kinds of analyses were conducted. First, for A. millepora (the species containing the most diverse suite of rDNA types), RT-PCR was used to determine which 5.8S rDNA types are expressed. Second, as previous studies have indicated that interspecific hybridization has occurred in the genus Acropora and silencing of rDNA loci via nucleolar dominance has been shown in some cases to involve methylation, patterns of variation were examined at methylation-susceptible sites. Third, patterns of substitution at conserved sites (including those that are likely to contribute to secondary structure in rRNA) in the 5.8S rDNA were examined. These analyses consistently indicated that one rDNA sequence type present in a broad range of Indo-Pacific Acropora species is likely to consist predominantly of pseudogenes. Patterns of variation also suggest that species may differ with respect to which rDNA sequence types have been silenced and which are active. These pseudogenes are likely to have arisen as a consequence of the introduction of highly divergent rDNA types into single genomes by interspecific hybridization events, and we attribute the extreme rDNA diversity characteristic of many Acropora species to both the independent evolution of these silenced rDNA types and to the suppressive effects of high sequence diversity on homogenization processes acting on functional loci.

To test the hypothesis of parallel speciation by sexual selection, we examined length variation at six microsatellite loci of samples from four sites of four to six putative species belonging to two subgenera of rocky shore mbuna cichlids from Lake Malawi. Almost all fixation indices were significantly different from zero, suggesting that there is presently little or no gene flow among allopatric populations or sympatric species. Analysis of variance indicated that genetic distances among allopatric populations of putative conspecifics were significantly lower than among sympatric populations of heterospecifics. The topology of trees based on distance matrices was also largely consistent with the hypothesis that the putative species are monophyletic and have thus not evolved in parallel in their present locations. If parallel speciation does occur in Malawi cichlids, it may be on a larger spatial scale than investigated in our study.

This study examines molecular relationships across a wide range of species in the mass spawning scleractinian coral genus Acropora. Molecular phylogenies were obtained for 28 species using DNA sequence analyses of two independent markers, a nuclear intron and the mtDNA putative control region. Although the compositions of the major clades in the phylogenies based on these two markers were similar, there were several important differences. This, in combination with the fact that many species were not monophyletic, suggests either that introgressive hybridization is occurring or that lineage sorting is incomplete. The molecular tree topologies bear little similarity to the results of a recent cladistic analysis based on skeletal morphology and are at odds with the fossil record. We hypothesize that these conflicting results may be due to the same morphology having evolved independently more than once in Acropora and/or the occurrence of extensive interspecific hybridization and introgression in combination with morphology being determined by a small number of genes. Our results indicate that many Acropora species belong to a species complex or syngameon and that morphology has little predictive value with regard to syngameon composition. Morphological species in the genus often do not correspond to genetically distinct evolutionary units. Instead, species that differ in timing of gamete release tend to constitute genetically distinct clades.

Recent studies have suggested that size homoplasy is a prevalent feature of microsatellites and is expected to increase with time of divergence among populations and taxa. In this study, we performed sequence analysis of alleles from a complex microsatellite locus (Pzeb4, initially isolated from Pseudotropheus (Maylandia) zebra) from 1 midwater-feeding and 10 rock-dwelling cichlid fish species from Lake Malawi, East Africa, to investigate how widespread size homoplasy is among closely related taxa at this locus. All cichlid fishes endemic to this lake are believed to have originated within the last 700,000 years, and some species may be less than 200 years old. The number of eletromorphs found per species varied from 3 to 13. Sequence analysis of 95 cloned Pzeb4 PCR products (representing 18 electromorphs) revealed 13 new alleles. Ten of the 13 electromorphs (77%) were found to show size homoplasy due to either single nucleotide substitutions/indels or large indels. To investigate how well this locus fits the single-step mutation model (SMM), the minimum number of mutations required to explain the length differences between pairs of alleles was plotted against their size differences. Of the 300 comparisons, 166 (55.3%) corresponded to SMM expectations and 86 (28.7%) required a smaller number of mutations, and for 48 (16.0%) pairwise comparisons, a larger number of mutations were required to explain the length differences as compared with SMM expectations. Finally, a large deletion in the microsatellite sequence observed in the three rock-dwelling species Pseudotropheus lucerna, Pseudotropheus (Tropheops) 'band,' and Pseudotropheus (Tropheops) 'rust' and the midwater-feeding species Copadichromis sp. is believed to represent a shared ancestral polymorphism.

We report the occurrence of a group I intron, 452 nucleotides in length, in the nuclear small-subunit ribosomal gene of the benthic seaweed Urospora penicilliformis, a member of the green algal class Ulvophyceae. Group I introns have been reported in fungi, myxomycetes, the ciliate genus Tetrahymena, and recently in five unicellular chlorophycean algae. The sequence of the conserved core of the U. penicilliformis group I intron was aligned with that of 15 other introns of this type, and the evolutionary relationships among these introns were examined. Comparison of the "intron" tree with phylogenetic hypotheses of the intron-harboring organisms shows that nuclear group I introns in green algae have arisen several times and are not lineage specific.