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Microbiome assemblages of plants and animals often show a degree of correlation with host phylogeny; an eco-evolutionary pattern known as phylosymbiosis. Using 16S rRNA gene sequencing to profile the microbiome, paired with COI, 18S rRNA and ITS1 host phylogenies, phylosymbiosis was investigated in four groups of coral reef invertebrates (scleractinian corals, octocorals, sponges and ascidians). We tested three commonly used metrics to evaluate the extent of phylosymbiosis: (a) intraspecific versus interspecific microbiome variation, (b) topological comparisons between host phylogeny and hierarchical clustering (dendrogram) of host-associated microbial communities, and (c) correlation of host phylogenetic distance with microbial community dissimilarity. In all instances, intraspecific variation in microbiome composition was significantly lower than interspecific variation. Similarly, topological congruency between host phylogeny and the associated microbial dendrogram was more significant than would be expected by chance across all groups, except when using unweighted UniFrac distance (compared with weighted UniFrac and Bray–Curtis dissimilarity). Interestingly, all but the ascidians showed a significant positive correlation between host phylogenetic distance and associated microbial dissimilarity. Our findings provide new perspectives on the diverse nature of marine phylosymbioses and the complex roles of the microbiome in the evolution of marine invertebrates.

Larvae of the sponge R. odorabile survived exposure to high concentrations of petroleum hydrocarbons; however, their ability to settle and metamorphose was adversely affected at environmentally relevant concentrations, and these effects were paralleled by marked changes in sponge gene expression and preceded by disruption of the symbiotic microbiome. Given the ecological importance of sponges, uncontrolled hydrocarbon releases from shipping accidents or production could affect sponge recruitment, which would have concomitant consequences for reef ecosystem function. Accidental oil spills from shipping and during extraction can threaten marine biota, particularly coral reef species which are already under pressure from anthropogenic disturbances. Marine sponges are an important structural and functional component of coral reef ecosystems; however, despite their ecological importance, little is known about how sponges and their microbial symbionts respond to petroleum products. Here, we use a systems biology-based approach to assess the effects of water-accommodated fractions (WAF) of crude oil, chemically enhanced water-accommodated fractions of crude oil (CWAF), and dispersant (Corexit EC9500A) on the survival, metamorphosis, gene expression, and microbial symbiosis of the abundant reef sponge Rhopaloeides odorabile in larval laboratory-based assays. Larval survival was unaffected by the 100% WAF treatment (107 μg liter −1 polycyclic aromatic hydrocarbon [PAH]), whereas significant decreases in metamorphosis were observed at 13% WAF (13.9 μg liter −1 PAH). The CWAF and dispersant treatments were more toxic, with decreases in metamorphosis identified at 0.8% (0.58 μg liter −1 PAH) and 1.6% (38 mg liter −1 Corexit EC9500A), respectively. In addition to the negative impact on larval settlement, significant changes in host gene expression and disruptions to the microbiome were evident, with microbial shifts detected at the lowest treatment level (1.6% WAF; 1.7 μg liter −1 PAH), including a significant reduction in the relative abundance of a previously described thaumarchaeal symbiont. The responsiveness of the R. odorabile microbial community to the lowest level of hydrocarbon treatment highlights the utility of the sponge microbiome as a sensitive marker for exposure to crude oils and dispersants. IMPORTANCE Larvae of the sponge R. odorabile survived exposure to high concentrations of petroleum hydrocarbons; however, their ability to settle and metamorphose was adversely affected at environmentally relevant concentrations, and these effects were paralleled by marked changes in sponge gene expression and preceded by disruption of the symbiotic microbiome. Given the ecological importance of sponges, uncontrolled hydrocarbon releases from shipping accidents or production could affect sponge recruitment, which would have concomitant consequences for reef ecosystem function. Author Video : An author video summary of this article is available.

We applied independent species concepts to clarify the phylogeographic structure of the ascidian Ciona intestinalis, a powerful model system in chordate biology and for comparative genomic studies. Intensive research with this marine invertebrate is based on the assumption that natural populations globally belong to a single species. Therefore, understanding the true taxonomic classification may have implications for experimental design and data management. Phylogenies inferred from mitochondrial and nuclear DNA markers accredit the existence of two cryptic species: C. intestinalis sp. A, genetically homogeneous, distributed in the Mediterranean, northeast Atlantic, and Pacific, and C. intestinalis sp. B, geographically structured and encountered in the North Atlantic. Species-level divergence is further entailed by cross-breeding estimates. C. intestinalis A and B from allopatric populations cross-fertilize, but hybrids remain infertile because of defective gametogenesis. Although anatomy illustrates an overall interspecific similarity lacking in diagnostic features, we provide consistent tools for in-field and in-laboratory species discrimination. Finding of two cryptic taxa in C. intestinalis raises interest in a new tunicate genome as a gateway to studies in speciation and ecological adaptation of chordates.

SOUL homologs constitute a heme-binding protein superfamily putatively involved in heme and tetrapyrrole metabolisms associated with a number of physiological processes. Despite their omnipresence across the tree of life and the biochemical characterization of many SOUL members, their functional role and the evolutionary events leading to such remarkable protein repertoire still remain cryptic. To explore SOUL evolution, we apply a computational phylogenetic approach, including a relevant number of SOUL homologs, to identify paralog forms and reconstruct their genealogy across the tree of life and within species. In animal lineages, multiple gene duplication or loss events and paralog functional specializations underlie SOUL evolution from the dawn of ancestral echinoderm and mollusc SOUL forms. In photosynthetic organisms, SOUL evolution is linked to the endosymbiosis events leading to plastid acquisition in eukaryotes. Derivative features, such as the F2L peptide and BH3 domain, evolved in vertebrates and provided innovative functionality to support immune response and apoptosis. The evolution of elements such as the N-terminal protein domain DUF2358, the His42 residue, or the tetrapyrrole heme-binding site is modern, and their functional implications still unresolved. This study represents the first in-depth analysis of SOUL protein evolution and provides novel insights in the understanding of their obscure physiological role.

Maskrays of the genus Neotrygon (Dasyatidae) have dispersed widely in the Indo‐West Pacific being represented largely by an assemblage of narrow‐ranging coastal endemics. Phylogenetic reconstruction methods reproduced nearly identical and statistically robust topologies supporting the monophyly of the genus Neotrygon within the family Dasyatidae, the genus Taeniura being consistently basal to Neotrygon, and Dasyatis being polyphyletic to the genera Taeniurops and Pteroplatytrygon. The Neotrygon kuhlii complex, once considered to be an assemblage of color variants of the same biological species, is the most derived and widely dispersed subgroup of the genus. Mitochondrial (COI, 16S) and nuclear (RAG1) phylogenies used in synergy with molecular dating identified paleoclimatic fluctuations responsible for periods of vicariance and dispersal promoting population fragmentation and speciation in Neotrygon. Signatures of population differentiation exist in N. ningalooensis and N. annotata, yet a large‐scale geological event, such as the collision between the Australian and Eurasian Plates, coupled with subsequent sea‐level falls, appears to have separated a once homogeneous population of the ancestral form of N. kuhlii into southern Indian Ocean and northern Pacific taxa some 4–16 million years ago. Repeated climatic oscillations, and the subsequent establishment of land and shallow sea connections within and between Australia and parts of the Indo‐Malay Archipelago, have both promoted speciation and established zones of secondary contact within the Indian and Pacific Ocean basins. We used molecular phylogenetics and phylogeography to assess the evolutionary history of Neotrygon Maskrays (Dasyatidae) across the geologically and climatically dynamic tropical Indo‐West Pacific. Molecular clock approximations suggest that the group may have arrived in the region via tectonic rafting and dispersed across the tropics. Sharp genetic breaks recovered within Neotrygon kuhlii, N.  annotata, and, to a lesser extent, N. ningalooensis are indicative of multiple cryptic speciation events likely due to glacio‐eustatic sea‐level oscillations responsible for vicariant divergences.

Marine fungi are an understudied group of eukaryotic microorganisms characterized by unresolved genealogies and unstable classification. Whereas DNA barcoding via the nuclear ribosomal internal transcribed spacer (ITS) provides a robust and rapid tool for fungal species delineation, accurate classification of fungi is often arduous given the large number of partial or unknown barcodes and misidentified isolates deposited in public databases. This situation is perpetuated by a paucity of cultivable fungal strains available for phylogenetic research linked to these data sets. We analyze ITS barcodes produced from a subsample (290) of 1781 cultured isolates of marine-derived fungi in the Bioresources Library located at the Australian Institute of Marine Science (AIMS). Our analysis revealed high levels of under-explored fungal diversity. The majority of isolates were ascomycetes including representatives of the subclasses Eurotiomycetidae, Hypocreomycetidae, Sordariomycetidae, Pleosporomycetidae, Dothideomycetidae, Xylariomycetidae and Saccharomycetidae. The phylum Basidiomycota was represented by isolates affiliated with the genera Tritirachium and Tilletiopsis. BLAST searches revealed 26 unknown OTUs and 50 isolates corresponding to previously uncultured, unidentified fungal clones. This study makes a significant addition to the availability of barcoded, culturable marine-derived fungi for detailed future genomic and physiological studies. We also demonstrate the influence of commonly used alignment algorithms and genetic distance measures on the accuracy and comparability of estimating Operational Taxonomic Units (OTUs) by the automatic barcode gap finder (ABGD) method. Large scale biodiversity screening programs that combine datasets using algorithmic OTU delineation pipelines need to ensure compatible algorithms have been used because the algorithm matters.

Biofilms of the bacterium Pseudoalteromonas induce metamorphosis of acroporid coral larvae. The bacterial metabolite tetrabromopyrrole (TBP), isolated from an extract of Pseudoalteromonas sp. associated with the crustose coralline alga (CCA) Neogoniolithon fosliei, induced coral larval metamorphosis (100%) with little or no attachment (0-2%). To better understand the molecular events and mechanisms underpinning the induction of Acropora millepora larval metamorphosis, including cell proliferation, apoptosis, differentiation, migration, adhesion and biomineralisation, two novel coral gene expression assays were implemented. These involved the use of reverse-transcriptase quantitative PCR (RT-qPCR) and employed 47 genes of interest (GOI), selected based on putative roles in the processes of settlement and metamorphosis. Substantial differences in transcriptomic responses of GOI were detected following incubation of A. millepora larvae with a threshold concentration and 10-fold elevated concentration of TBP-containing extracts of Pseudoalteromonas sp. The notable and relatively abrupt changes of the larval body structure during metamorphosis correlated, at the molecular level, with significant differences (p<0.05) in gene expression profiles of 24 GOI, 12 hours post exposure. Fourteen of those GOI also presented differences in expression (p<0.05) following exposure to the threshold concentration of bacterial TBP-containing extract. The specificity of the bacterial TBP-containing extract to induce the metamorphic stage in A. millepora larvae without attachment, using a robust, low cost, accurate, ecologically relevant and highly reproducible RT-qPCR assay, allowed partially decoupling of the transcriptomic processes of attachment and metamorphosis. The bacterial TBP-containing extract provided a unique opportunity to monitor the regulation of genes exclusively involved in the process of metamorphosis, contrasting previous gene expression studies that utilized cues, such as crustose coralline algae, biofilms or with GLW-amide neuropeptides that stimulate the entire onset of larval metamorphosis and attachment.

Understanding the mechanisms by which natural populations cope with environmental stress is paramount to predict their persistence in the face of escalating anthropogenic impacts. Reef-building corals are increasingly exposed to local and global stressors that alter nutritional status causing reduced fitness and mortality, however, these responses can vary considerably across species and populations. We compare the expression of 22 coral host genes in individuals from an inshore and an offshore reef location using quantitative Reverse Transcription-PCR (qRT-PCR) over the course of 26 days following translocation into a shaded, filtered seawater environment. Declines in lipid content and PSII activity of the algal endosymbionts (Symbiodinium ITS-1 type C2) over the course of the experiment indicated that heterotrophic uptake and photosynthesis were limited, creating nutritional deprivation conditions. Regulation of coral host genes involved in metabolism, CO2 transport and oxidative stress could be detected already after five days, whereas PSII activity took twice as long to respond. Opposing expression trajectories of Tgl, which releases fatty acids from the triacylglycerol storage, and Dgat1, which catalyses the formation of triglycerides, indicate that the decline in lipid content can be attributed, at least in part, by mobilisation of triacylglycerol stores. Corals from the inshore location had initially higher lipid content and showed consistently elevated expression levels of two genes involved in metabolism (aldehyde dehydrogenase) and calcification (carbonic anhydrase). Coral host gene expression adjusts rapidly upon change in nutritional conditions, and therefore can serve as an early signature of imminent coral stress. Consistent gene expression differences between populations indicate that corals acclimatize and/or adapt to local environments. Our results set the stage for analysis of these processes in natural coral populations, to better understand the responses of coral communities to global climate change and to develop more efficient management strategies.

Nitric oxide (NO) is essential to many physiological functions and operates in several signaling pathways. It is not understood how and when the different isoforms of nitric oxide synthase (NOS), the enzyme responsible for NO production, evolved in metazoans. This study investigates the number and structure of metazoan NOS enzymes by genome data mining and direct cloning of Nos genes from the lamprey. In total, 181 NOS proteins are analyzed from 33 invertebrate and 63 vertebrate species. Comparisons among protein and gene structures, combined with phylogenetic and syntenic studies, provide novel insights into how NOS isoforms arose and diverged. Protein domains and gene organization—that is, intron positions and phases—of animal NOS are remarkably conserved across all lineages, even in fast-evolving species. Phylogenetic and syntenic analyses support the view that a proto-NOS isoform was recurrently duplicated in different lineages, acquiring new structural configurations through gains and losses of protein motifs. We propose that in vertebrates a first duplication took place after the agnathan–gnathostome split followed by a paralog loss. A second duplication occurred during early tetrapod evolution, giving rise to the three isoforms—I, II, and III—in current mammals. Overall, NOS family evolution was the result of multiple gene and genome duplication events together with changes in protein architecture.

The study of ascidians (Chordata, Tunicata) has made a considerable contribution to our understanding of the origin and evolution of basal chordates. To provide further information to support forward genetics in Ciona intestinalis, we used a combination of natural variation and neutral population genetics as an approach for the systematic identification of new mutations. In addition to the significance of developmental variation for phenotype-driven studies, this approach can encompass important implications in evolutionary and population biology. Here, we report a preliminary survey for naturally occurring mutations in three geographically interconnected populations of C. intestinalis. The influence of historical, geographical and environmental factors on the distribution of abnormal phenotypes was assessed by means of 12 microsatellites. We identified 37 possible mutant loci with stereotyped defects in embryonic development that segregate in a way typical of recessive alleles. Local populations were found to differ in genetic organization and frequency distribution of phenotypic classes. Natural genetic polymorphism of C. intestinalis constitutes a valuable source of phenotypes for studying embryonic development in ascidians. Correlating genetic structure and the occurrence of abnormal phenotypes is a crucial focus for understanding the selective forces that shape natural finite populations, and may provide insights of great importance into the evolutionary mechanisms that generate animal diversity.