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1.  Mitochondrial Genome Rearrangements in the Scleractinia/Corallimorpharia Complex: Implications for Coral Phylogeny 
Genome Biology and Evolution  2014;6(5):1086-1095.
Corallimorpharia is a small Order of skeleton-less animals that is closely related to the reef-building corals (Scleractinia) and of fundamental interest in the context of understanding the potential impacts of climate change in the future on coral reefs. The relationship between the nominal Orders Corallimorpharia and Scleractinia is controversial—the former is either the closest outgroup to the Scleractinia or alternatively is derived from corals via skeleton loss. This latter scenario, the “naked coral” hypothesis, is strongly supported by analyses based on mitochondrial (mt) protein sequences, whereas the former is equally strongly supported by analyses of mt nucleotide sequences. The “naked coral” hypothesis seeks to link skeleton loss in the putative ancestor of corallimorpharians with a period of elevated oceanic CO2 during the Cretaceous, leading to the idea that these skeleton-less animals may be harbingers for the fate of coral reefs under global climate change. In an attempt to better understand their evolutionary relationships, we examined mt genome organization in a representative range (12 species, representing 3 of the 4 extant families) of corallimorpharians and compared these patterns with other Hexacorallia. The most surprising finding was that mt genome organization in Corallimorphus profundus, a deep-water species that is the most scleractinian-like of all corallimorpharians on the basis of morphology, was much more similar to the common scleractinian pattern than to those of other corallimorpharians. This finding is consistent with the idea that C. profundus represents a key position in the coral <-> corallimorpharian transition.
PMCID: PMC4040992  PMID: 24769753
naked coral hypothesis; gene order; mitochondrial genome; coral evolution
2.  The “Naked Coral” Hypothesis Revisited – Evidence for and Against Scleractinian Monophyly 
PLoS ONE  2014;9(4):e94774.
The relationship between Scleractinia and Corallimorpharia, Orders within Anthozoa distinguished by the presence of an aragonite skeleton in the former, is controversial. Although classically considered distinct groups, some phylogenetic analyses have placed the Corallimorpharia within a larger Scleractinia/Corallimorpharia clade, leading to the suggestion that the Corallimorpharia are “naked corals” that arose via skeleton loss during the Cretaceous from a Scleractinian ancestor. Scleractinian paraphyly is, however, contradicted by a number of recent phylogenetic studies based on mt nucleotide (nt) sequence data. Whereas the “naked coral” hypothesis was based on analysis of the sequences of proteins encoded by a relatively small number of mt genomes, here a much-expanded dataset was used to reinvestigate hexacorallian phylogeny. The initial observation was that, whereas analyses based on nt data support scleractinian monophyly, those based on amino acid (aa) data support the “naked coral” hypothesis, irrespective of the method and with very strong support. To better understand the bases of these contrasting results, the effects of systematic errors were examined. Compared to other hexacorallians, the mt genomes of “Robust” corals have a higher (A+T) content, codon usage is far more constrained, and the proteins that they encode have a markedly higher phenylalanine content, leading us to suggest that mt DNA repair may be impaired in this lineage. Thus the “naked coral” topology could be caused by high levels of saturation in these mitochondrial sequences, long-branch effects or model violations. The equivocal results of these extensive analyses highlight the fundamental problems of basing coral phylogeny on mitochondrial sequence data.
PMCID: PMC3989238  PMID: 24740380
3.  Cnidarian phylogenetic relationships as revealed by mitogenomics 
Cnidaria (corals, sea anemones, hydroids, jellyfish) is a phylum of relatively simple aquatic animals characterized by the presence of the cnidocyst: a cell containing a giant capsular organelle with an eversible tubule (cnida). Species within Cnidaria have life cycles that involve one or both of the two distinct body forms, a typically benthic polyp, which may or may not be colonial, and a typically pelagic mostly solitary medusa. The currently accepted taxonomic scheme subdivides Cnidaria into two main assemblages: Anthozoa (Hexacorallia + Octocorallia) – cnidarians with a reproductive polyp and the absence of a medusa stage – and Medusozoa (Cubozoa, Hydrozoa, Scyphozoa, Staurozoa) – cnidarians that usually possess a reproductive medusa stage. Hypothesized relationships among these taxa greatly impact interpretations of cnidarian character evolution.
We expanded the sampling of cnidarian mitochondrial genomes, particularly from Medusozoa, to reevaluate phylogenetic relationships within Cnidaria. Our phylogenetic analyses based on a mitochogenomic dataset support many prior hypotheses, including monophyly of Hexacorallia, Octocorallia, Medusozoa, Cubozoa, Staurozoa, Hydrozoa, Carybdeida, Chirodropida, and Hydroidolina, but reject the monophyly of Anthozoa, indicating that the Octocorallia + Medusozoa relationship is not the result of sampling bias, as proposed earlier. Further, our analyses contradict Scyphozoa [Discomedusae + Coronatae], Acraspeda [Cubozoa + Scyphozoa], as well as the hypothesis that Staurozoa is the sister group to all the other medusozoans.
Cnidarian mitochondrial genomic data contain phylogenetic signal informative for understanding the evolutionary history of this phylum. Mitogenome-based phylogenies, which reject the monophyly of Anthozoa, provide further evidence for the polyp-first hypothesis. By rejecting the traditional Acraspeda and Scyphozoa hypotheses, these analyses suggest that the shared morphological characters in these groups are plesiomorphies, originated in the branch leading to Medusozoa. The expansion of mitogenomic data along with improvements in phylogenetic inference methods and use of additional nuclear markers will further enhance our understanding of the phylogenetic relationships and character evolution within Cnidaria.
PMCID: PMC3598815  PMID: 23302374
Cnidaria; Medusozoa; Acraspeda; Anthozoa; mito-phylogenomics
4.  A Comprehensive Phylogenetic Analysis of the Scleractinia (Cnidaria, Anthozoa) Based on Mitochondrial CO1 Sequence Data 
PLoS ONE  2010;5(7):e11490.
Classical morphological taxonomy places the approximately 1400 recognized species of Scleractinia (hard corals) into 27 families, but many aspects of coral evolution remain unclear despite the application of molecular phylogenetic methods. In part, this may be a consequence of such studies focusing on the reef-building (shallow water and zooxanthellate) Scleractinia, and largely ignoring the large number of deep-sea species. To better understand broad patterns of coral evolution, we generated molecular data for a broad and representative range of deep sea scleractinians collected off New Caledonia and Australia during the last decade, and conducted the most comprehensive molecular phylogenetic analysis to date of the order Scleractinia.
Partial (595 bp) sequences of the mitochondrial cytochrome oxidase subunit 1 (CO1) gene were determined for 65 deep-sea (azooxanthellate) scleractinians and 11 shallow-water species. These new data were aligned with 158 published sequences, generating a 234 taxon dataset representing 25 of the 27 currently recognized scleractinian families.
Principal Findings/Conclusions
There was a striking discrepancy between the taxonomic validity of coral families consisting predominantly of deep-sea or shallow-water species. Most families composed predominantly of deep-sea azooxanthellate species were monophyletic in both maximum likelihood and Bayesian analyses but, by contrast (and consistent with previous studies), most families composed predominantly of shallow-water zooxanthellate taxa were polyphyletic, although Acroporidae, Poritidae, Pocilloporidae, and Fungiidae were exceptions to this general pattern. One factor contributing to this inconsistency may be the greater environmental stability of deep-sea environments, effectively removing taxonomic “noise” contributed by phenotypic plasticity. Our phylogenetic analyses imply that the most basal extant scleractinians are azooxanthellate solitary corals from deep-water, their divergence predating that of the robust and complex corals. Deep-sea corals are likely to be critical to understanding anthozoan evolution and the origins of the Scleractinia.
PMCID: PMC2900217  PMID: 20628613
5.  Desmophyllum dianthus (Esper, 1794) in the Scleractinian Phylogeny and Its Intraspecific Diversity 
PLoS ONE  2012;7(11):e50215.
The cosmopolitan solitary deep-water scleractinian coral Desmophyllum dianthus (Esper, 1794) was selected as a representative model species of the polyphyletic Caryophylliidae family to (1) examine phylogenetic relationships with respect to the principal Scleractinia taxa, (2) check population structure, (3) test the widespread connectivity hypothesis and (4) assess the utility of different nuclear and mitochondrial markers currently in use. To carry out these goals, DNA sequence data from nuclear (ITS and 28S) and mitochondrial (16S and COI) markers were analyzed for several coral species and for Mediterranean populations of D. dianthus. Three phylogenetic methodologies (ML, MP and BI), based on data from the four molecular markers, all supported D. dianthus as clearly belonging to the “robust” clade, in which the species Lophelia pertusa and D. dianthus not only grouped together, but also shared haplotypes for some DNA markers. Molecular results also showed shared haplotypes among D. dianthus populations distributed in regions separated by several thousands of kilometers and by clear geographic barriers. These results could reflect limited molecular and morphological taxonomic resolution rather than real widespread connectivity. Additional studies are needed in order to find molecular markers and morphological features able to disentangle the complex phylogenetic relationship in the Order Scleractinia and to differentiate isolated populations, thus avoiding the homoplasy found in some morphological characters that are still considered in the literature.
PMCID: PMC3509136  PMID: 23209679
6.  The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals 
Scleractinian corals are currently a focus of major interest because of their ecological importance and the uncertain fate of coral reefs in the face of increasing anthropogenic pressure. Despite this, remarkably little is known about the evolutionary origins of corals. The Scleractinia suddenly appear in the fossil record about 240 Ma, but the range of morphological variation seen in these Middle Triassic fossils is comparable to that of modern scleractinians, implying much earlier origins that have so far remained elusive. A significant weakness in reconstruction(s) of early coral evolution is that deep-sea corals have been poorly represented in molecular phylogenetic analyses.
By adding new data from a large and representative range of deep-water species to existing molecular datasets and applying a relaxed molecular clock, we show that two exclusively deep-sea families, the Gardineriidae and Micrabaciidae, diverged prior to the Complexa/Robusta coral split around 425 Ma, thereby pushing the evolutionary origin of scleractinian corals deep into the Paleozoic.
The early divergence and distinctive morphologies of the extant gardineriid and micrabaciid corals suggest a link with Ordovician "scleractiniamorph" fossils that were previously assumed to represent extinct anthozoan skeletonized lineages. Therefore, scleractinian corals most likely evolved from Paleozoic soft-bodied ancestors. Modern shallow-water Scleractinia, which are dependent on symbionts, appear to have had several independent origins from solitary, non-symbiotic precursors. The Scleractinia have survived periods of massive climate change in the past, suggesting that as a lineage they may be less vulnerable to future changes than often assumed.
PMCID: PMC3224782  PMID: 22034946
7.  Polyphyly and hidden species among Hawaiʻi’s dominant mesophotic coral genera, Leptoseris and Pavona (Scleractinia: Agariciidae) 
PeerJ  2013;1:e132.
Widespread polyphyly in stony corals (order Scleractinia) has prompted efforts to revise their systematics through approaches that integrate molecular and micromorphological evidence. To date, these approaches have not been comprehensively applied to the dominant genera in mesophotic coral ecosystems (MCEs) because several species in these genera occur primarily at depths that are poorly explored and from which sample collections are limited. This study is the first integrated morphological and molecular systematic analysis of the genera Leptoseris and Pavona to examine material both from shallow-water reefs (<30 m) and from mid- to lower-MCEs (>60 m). Skeletal and tissue samples were collected throughout the Hawaiian Archipelago between 2–127 m. A novel mitochondrial marker (cox1-1-rRNA intron) was sequenced for 70 colonies, and the micromorphologies of 94 skeletons, plus selected type material, were analyzed. The cox1-1-rRNA intron resolved 8 clades, yet Leptoseris and Pavona were polyphyletic. Skeletal micromorphology, especially costal ornamentation, showed strong correspondence and discrete differences between mitochondrial groups. One putative new Leptoseris species was identified and the global depth range of the genus Pavona was extended to 89 m, suggesting that the diversity of mesophotic scleractinians has been underestimated. Examination of species’ depth distributions revealed a pattern of depth zonation: Species common in shallow-water were absent or rare >40 m, whereas others occurred only >60 m. These patterns emphasize the importance of integrated systematic analyses and more comprehensive sampling by depth in assessing the connectivity and diversity of MCEs.
PMCID: PMC3747016  PMID: 24032091
Leptoseris; Pavona; Mesophotic coral ecosystems; Integrated systematics; Molecular phylogenetics; Micromorphology; cox1-1-rRNA intron; Depth zonation; Zooxanthellate corals; Taxonomy
8.  Transcriptome Analysis of the Scleractinian Coral Stylophora pistillata 
PLoS ONE  2014;9(2):e88615.
The principal architects of coral reefs are the scleractinian corals; these species are divided in two major clades referred to as “robust” and “complex” corals. Although the molecular diversity of the “complex” clade has received considerable attention, with several expressed sequence tag (EST) libraries and a complete genome sequence having been constructed, the “robust” corals have received far less attention, despite the fact that robust corals have been prominent focal points for ecological and physiological studies. Filling this gap affords important opportunities to extend these studies and to improve our understanding of the differences between the two major clades. Here, we present an EST library from Stylophora pistillata (Esper 1797) and systematically analyze the assembled transcripts compared to putative homologs from the complete proteomes of six well-characterized metazoans: Nematostella vectensis, Hydra magnipapillata, Caenorhabditis elegans, Drosophila melanogaster, Strongylocentrotus purpuratus, Ciona intestinalis and Homo sapiens. Furthermore, comparative analyses of the Stylophora pistillata ESTs were performed against several Cnidaria from the Scleractinia, Actiniaria and Hydrozoa, as well as against other stony corals separately. Functional characterization of S. pistillata transcripts into KOG/COG categories and further description of Wnt and bone morphogenetic protein (BMP) signaling pathways showed that the assembled EST library provides sufficient data and coverage. These features of this new library suggest considerable opportunities for extending our understanding of the molecular and physiological behavior of “robust” corals.
PMCID: PMC3923803  PMID: 24551124
9.  Cleaning up the 'Bigmessidae': Molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae 
Molecular phylogenetic studies on scleractinian corals have shown that most taxa are not reflective of their evolutionary histories. Based principally on gross morphology, traditional taxonomy suffers from the lack of well-defined and homologous characters that can sufficiently describe scleractinian diversity. One of the most challenging clades recovered by recent analyses is 'Bigmessidae', an informal grouping that comprises four conventional coral families, Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae, interspersed among one another with no apparent systematic pattern. There is an urgent need for taxonomic revisions in this clade, but it is vital to first establish phylogenetic relationships within the group. In this study, we reconstruct the evolutionary history of 'Bigmessidae' based on five DNA sequence markers gathered from 76 of the 132 currently recognized species collected from five reef regions in the central Indo-Pacific and the Atlantic.
We present a robust molecular phylogeny of 'Bigmessidae' based on the combined five-gene data, achieving a higher degree of resolution compared to previous analyses. Two Pacific species presumed to be in 'Bigmessidae' are more closely related to outgroup clades, suggesting that other unsampled taxa have unforeseen affinities. As expected, nested within 'Bigmessidae' are four conventional families as listed above, and relationships among them generally corroborate previous molecular analyses. Our more resolved phylogeny supports a close association of Hydnophora (Merulinidae) with Favites + Montastraea (Faviidae), rather than with the rest of Merulinidae, i.e., Merulina and Scapophyllia. Montastraea annularis, the only Atlantic 'Bigmessidae' is sister to Cyphastrea, a grouping that can be reconciled by their septothecal walls, a microstructural feature of the skeleton determined by recent morphological work. Characters at the subcorallite scale appear to be appropriate synapomorphies for other subclades, which cannot be explained using macromorphology. Indeed, wide geographic sampling here has revealed more instances of possible cryptic taxa confused by evolutionary convergence of gross coral morphology.
Numerous examples of cryptic taxa determined in this study support the assertion that diversity estimates of scleractinian corals are erroneous. Fortunately, the recovery of most 'Bigmessidae' genera with only minor degrees of paraphyly offers some hope for impending taxonomic amendments. Subclades are well defined and supported by subcorallite morphological features, providing a robust framework for further systematic work.
PMCID: PMC3042006  PMID: 21299898
10.  Diversity and Evolution of Coral Fluorescent Proteins 
PLoS ONE  2008;3(7):e2680.
GFP-like fluorescent proteins (FPs) are the key color determinants in reef-building corals (class Anthozoa, order Scleractinia) and are of considerable interest as potential genetically encoded fluorescent labels. Here we report 40 additional members of the GFP family from corals. There are three major paralogous lineages of coral FPs. One of them is retained in all sampled coral families and is responsible for the non-fluorescent purple-blue color, while each of the other two evolved a full complement of typical coral fluorescent colors (cyan, green, and red) and underwent sorting between coral groups. Among the newly cloned proteins are a “chromo-red” color type from Echinopora forskaliana (family Faviidae) and pink chromoprotein from Stylophora pistillata (Pocilloporidae), both evolving independently from the rest of coral chromoproteins. There are several cyan FPs that possess a novel kind of excitation spectrum indicating a neutral chromophore ground state, for which the residue E167 is responsible (numeration according to GFP from A. victoria). The chromoprotein from Acropora millepora is an unusual blue instead of purple, which is due to two mutations: S64C and S183T. We applied a novel probabilistic sampling approach to recreate the common ancestor of all coral FPs as well as the more derived common ancestor of three main fluorescent colors of the Faviina suborder. Both proteins were green such as found elsewhere outside class Anthozoa. Interestingly, a substantial fraction of the all-coral ancestral protein had a chromohore apparently locked in a non-fluorescent neutral state, which may reflect the transitional stage that enabled rapid color diversification early in the history of coral FPs. Our results highlight the extent of convergent or parallel evolution of the color diversity in corals, provide the foundation for experimental studies of evolutionary processes that led to color diversification, and enable a comparative analysis of structural determinants of different colors.
PMCID: PMC2481297  PMID: 18648549
11.  Hidden among Sea Anemones: The First Comprehensive Phylogenetic Reconstruction of the Order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) Reveals a Novel Group of Hexacorals 
PLoS ONE  2014;9(5):e96998.
Sea anemones (order Actiniaria) are among the most diverse and successful members of the anthozoan subclass Hexacorallia, occupying benthic marine habitats across all depths and latitudes. Actiniaria comprises approximately 1,200 species of solitary and skeleton-less polyps and lacks any anatomical synapomorphy. Although monophyly is anticipated based on higher-level molecular phylogenies of Cnidaria, to date, monophyly has not been explicitly tested and at least some hypotheses on the diversification of Hexacorallia have suggested that actiniarians are para- or poly-phyletic. Published phylogenies have demonstrated the inadequacy of existing morphological-based classifications within Actiniaria. Superfamilial groups and most families and genera that have been rigorously studied are not monophyletic, indicating conflict with the current hierarchical classification. We test the monophyly of Actiniaria using two nuclear and three mitochondrial genes with multiple analytical methods. These analyses are the first to include representatives of all three currently-recognized suborders within Actiniaria. We do not recover Actiniaria as a monophyletic clade: the deep-sea anemone Boloceroides daphneae, previously included within the infraorder Boloceroidaria, is resolved outside of Actiniaria in several of the analyses. We erect a new genus and family for B. daphneae, and rank this taxon incerti ordinis. Based on our comprehensive phylogeny, we propose a new formal higher-level classification for Actiniaria composed of only two suborders, Anenthemonae and Enthemonae. Suborder Anenthemonae includes actiniarians with a unique arrangement of mesenteries (members of Edwardsiidae and former suborder Endocoelantheae). Suborder Enthemonae includes actiniarians with the typical arrangement of mesenteries for actiniarians (members of former suborders Protantheae, Ptychodacteae, and Nynantheae and subgroups therein). We also erect subgroups within these two newly-erected suborders. Although some relationships among these newly-defined groups are still ambiguous, morphological and molecular results are consistent enough to proceed with a new higher-level classification and to discuss the putative functional and evolutionary significance of several morphological attributes within Actiniaria.
PMCID: PMC4013120  PMID: 24806477
12.  Differential expression of three galaxin-related genes during settlement and metamorphosis in the scleractinian coral Acropora millepora 
The coral skeleton consists of CaCO3 deposited upon an organic matrix primarily as aragonite. Currently galaxin, from Galaxea fascicularis, is the only soluble protein component of the organic matrix that has been characterized from a coral. Three genes related to galaxin were identified in the coral Acropora millepora.
One of the Acropora genes (Amgalaxin) encodes a clear galaxin ortholog, while the others (Amgalaxin-like 1 and Amgalaxin-like 2) encode larger and more divergent proteins. All three proteins are predicted to be extracellular and share common structural features, most notably the presence of repetitive motifs containing dicysteine residues. In situ hybridization reveals distinct, but partially overlapping, spatial expression of the genes in patterns consistent with distinct roles in calcification. Both of the Amgalaxin-like genes are expressed exclusively in the early stages of calcification, while Amgalaxin continues to be expressed in the adult, consistent with the situation in the coral Galaxea.
Comparisons with molluscs suggest functional convergence in the two groups; lustrin A/pearlin proteins may be the mollusc counterparts of galaxin, whereas the galaxin-like proteins combine characteristics of two distinct proteins involved in mollusc calcification. Database searches indicate that, although sequences with high similarity to the galaxins are restricted to the Scleractinia, more divergent members of this protein family are present in other cnidarians and some other metazoans. We suggest that ancestral galaxins may have been secondarily recruited to roles in calcification in the Triassic, when the Scleractinia first appeared. Understanding the evolution of the broader galaxin family will require wider sampling and expression analysis in a range of cnidarians and other animals.
PMCID: PMC2726143  PMID: 19638240
13.  Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis 
PLoS Biology  2009;7(1):e1000020.
For more than a century, the origin of metazoan animals has been debated. One aspect of this debate has been centered on what the hypothetical “urmetazoon” bauplan might have been. The morphologically most simply organized metazoan animal, the placozoan Trichoplax adhaerens, resembles an intriguing model for one of several “urmetazoon” hypotheses: the placula hypothesis. Clear support for a basal position of Placozoa would aid in resolving several key issues of metazoan-specific inventions (including, for example, head–foot axis, symmetry, and coelom) and would determine a root for unraveling their evolution. Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question. Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa. Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized “urmetazoon” hypothesis.
Author Summary
Following one of the basic principles in evolutionary biology that complex life forms derive from more primitive ancestors, it has long been believed that the higher animals, the Bilateria, arose from simpler (diploblastic) organisms such as the cnidarians (corals, polyps, and jellyfishes). A large number of studies, using different datasets and different methods, have tried to determine the most ancestral animal group as well as the ancestor of the higher animals. Here, we use “total evidence” analysis, which incorporates all available data (including morphology, genome, and gene expression data) and come to a surprising conclusion. The Bilateria and Cnidaria (together with the other diploblastic animals) are in fact sister groups: that is, they evolved in parallel from a very simple common ancestor. We conclude that the higher animals (Bilateria) and lower animals (diploblasts), probably separated very early, at the very beginning of metazoan animal evolution and independently evolved their complex body plans, including body axes, nervous system, sensory organs, and other characteristics. The striking similarities in several complex characters (such as the eyes) resulted from both lineages using the same basic genetic tool kit, which was already present in the common ancestor. The study identifies Placozoa as the most basal diploblast group and thus a living fossil genome that nicely demonstrates, not only that complex genetic tool kits arise before morphological complexity, but also that these kits may form similar morphological structures in parallel.
Total evidence analyses reveal a surprise: Higher animals did not evolve from any known lower animal group.
PMCID: PMC2631068  PMID: 19175291
14.  Threatened Corals Provide Underexplored Microbial Habitats 
PLoS ONE  2010;5(3):e9554.
Contemporary in-depth sequencing of environmental samples has provided novel insights into microbial community structures, revealing that their diversity had been previously underestimated. Communities in marine environments are commonly composed of a few dominant taxa and a high number of taxonomically diverse, low-abundance organisms. However, studying the roles and genomic information of these “rare” organisms remains challenging, because little is known about their ecological niches and the environmental conditions to which they respond. Given the current threat to coral reef ecosystems, we investigated the potential of corals to provide highly specialized habitats for bacterial taxa including those that are rarely detected or absent in surrounding reef waters. The analysis of more than 350,000 small subunit ribosomal RNA (16S rRNA) sequence tags and almost 2,000 nearly full-length 16S rRNA gene sequences revealed that rare seawater biosphere members are highly abundant or even dominant in diverse Caribbean corals. Closely related corals (in the same genus/family) harbored similar bacterial communities. At higher taxonomic levels, however, the similarities of these communities did not correlate with the phylogenetic relationships among corals, opening novel questions about the evolutionary stability of coral-microbial associations. Large proportions of OTUs (28.7–49.1%) were unique to the coral species of origin. Analysis of the most dominant ribotypes suggests that many uncovered bacterial taxa exist in coral habitats and await future exploration. Our results indicate that coral species, and by extension other animal hosts, act as specialized habitats of otherwise rare microbes in marine ecosystems. Here, deep sequencing provided insights into coral microbiota at an unparalleled resolution and revealed that corals harbor many bacterial taxa previously not known. Given that two of the coral species investigated are listed as threatened under the U.S. Endangered Species Act, our results add an important microbial diversity-based perspective to the significance of conserving coral reefs.
PMCID: PMC2832684  PMID: 20221265
15.  A time-calibrated molecular phylogeny of the precious corals: reconciling discrepancies in the taxonomic classification and insights into their evolutionary history 
Seamount-associated faunas are often considered highly endemic but isolation and diversification processes leading to such endemism have been poorly documented at those depths. Likewise, species delimitation and phylogenetic studies in deep-sea organisms remain scarce, due to the difficulty in obtaining samples, and sometimes controversial. The phylogenetic relationships within the precious coral family Coralliidae remain largely unexplored and the monophyly of its two constituent genera, Corallium Cuvier and Paracorallium Bayer & Cairns, has not been resolved. As traditionally recognized, the diversity of colonial forms among the various species correlates with the diversity in shape of their supporting axis, but the phylogenetic significance of these characters remains to be tested. We thus used mitochondrial sequence data to evaluate the monophyly of Corallium and Paracorallium and the species boundaries for nearly all named taxa in the family. Species from across the coralliid range, including material from Antarctica, Hawaii, Japan, New Zealand, Taiwan, Tasmania, the eastern Pacific and the western Atlantic were examined.
The concatenated analysis of five mitochondrial regions (COI, 16S rRNA, ND2, and ND3-ND6) recovered two major coralliid clades. One clade is composed of two subgroups, the first including Corallium rubrum, the type species of the genus, together with a small group of Paracorallium species (P. japonicum and P. tortuosum) and C. medea (clade I-A); the other subgroup includes a poorly-resolved assemblage of six Corallium species (C. abyssale, C. ducale, C. imperiale, C. laauense, C. niobe, and C. sulcatum; clade I-B). The second major clade is well resolved and includes species of Corallium and Paracorallium (C. elatius, C. kishinouyei, C. konojoi, C. niveum, C. secundum, Corallium sp., Paracorallium nix, Paracorallium thrinax and Paracorallium spp.). A traditional taxonomic study of this clade delineated 11 morphospecies that were congruent with the general mixed Yule-coalescent (GMYC) model. A multilocus species-tree approach also identified the same two well-supported clades, being Clade I-B more recent in the species tree (18.0-15.9 mya) than in the gene tree (35.2-15.9 mya). In contrast, the diversification times for Clade II were more ancient in the species tree (136.4-41.7 mya) than in the gene tree (66.3-16.9 mya).
Our results provide no support for the taxonomic status of the two currently recognized genera in the family Coralliidae. Given that Paracorallium species were all nested within Corallium, we recognize the coralliid genus Corallium, which includes the type species of the family, and thus consider Paracorallium a junior synonym of Corallium. We propose the use of the genus Hemicorallium Gray for clade I-B (species with long rod sclerites, cylindrical autozooids and smooth axis). Species delimitation in clade I-B remains unclear and the molecular resolution for Coralliidae species is inconsistent in the two main clades. Some species have wide distributions, recent diversification times and low mtDNA divergence whereas other species exhibit narrower allopatric distributions, older diversification times and greater levels of mtDNA resolution.
PMCID: PMC3565870  PMID: 23249327
16.  Identification of Scleractinian Coral Recruits Using Fluorescent Censusing and DNA Barcoding Techniques 
PLoS ONE  2014;9(9):e107366.
The identification of coral recruits has been problematic due to a lack of definitive morphological characters being available for higher taxonomic resolution. In this study, we tested whether fluorescent detection of coral recruits used in combinations of different DNA-barcoding markers (cytochrome oxidase I gene [COI], open reading frame [ORF], and nuclear Pax-C intron [PaxC]) could be useful for increasing the resolution of coral spat identification in ecological studies. One hundred and fifty settlement plates were emplaced at nine sites on the fringing reefs of Kenting National Park in southern Taiwan between April 2011 and September 2012. A total of 248 living coral spats and juveniles (with basal areas ranging from 0.21 to 134.57 mm2) were detected on the plates with the aid of fluorescent light and collected for molecular analyses. Using the COI DNA barcoding technique, 90.3% (224/248) of coral spats were successfully identified into six genera, including Acropora, Isopora, Montipora, Pocillopora, Porites, and Pavona. PaxC further separated I. cuneata and I. palifera of Isopora from Acropora, and ORF successfully identified the species of Pocillopora (except P. meandrina and P. eydouxi). Moreover, other cnidarian species such as actinarians, zoanthids, and Millepora species were visually found using fluorescence and identified by COI DNA barcoding. This combination of existing approaches greatly improved the taxonomic resolution of early coral life stages, which to date has been mainly limited to the family level based on skeletal identification. Overall, this study suggests important improvements for the identification of coral recruits in ecological studies.
PMCID: PMC4161427  PMID: 25211345
17.  A comprehensive and integrative reconstruction of evolutionary history for Anomura (Crustacea: Decapoda) 
The infraorder Anomura has long captivated the attention of evolutionary biologists due to its impressive morphological diversity and ecological adaptations. To date, 2500 extant species have been described but phylogenetic relationships at high taxonomic levels remain unresolved. Here, we reconstruct the evolutionary history—phylogeny, divergence times, character evolution and diversification—of this speciose clade. For this purpose, we sequenced two mitochondrial (16S and 12S) and three nuclear (H3, 18S and 28S) markers for 19 of the 20 extant families, using traditional Sanger and next-generation 454 sequencing methods. Molecular data were combined with 156 morphological characters in order to estimate the largest anomuran phylogeny to date. The anomuran fossil record allowed us to incorporate 31 fossils for divergence time analyses.
Our best phylogenetic hypothesis (morphological + molecular data) supports most anomuran superfamilies and families as monophyletic. However, three families and eleven genera are recovered as para- and polyphyletic. Divergence time analysis dates the origin of Anomura to the Late Permian ~259 (224–296) MYA with many of the present day families radiating during the Jurassic and Early Cretaceous. Ancestral state reconstruction suggests that carcinization occurred independently 3 times within the group. The invasion of freshwater and terrestrial environments both occurred between the Late Cretaceous and Tertiary. Diversification analyses found the speciation rate to be low across Anomura, and we identify 2 major changes in the tempo of diversification; the most significant at the base of a clade that includes the squat-lobster family Chirostylidae.
Our findings are compared against current classifications and previous hypotheses of anomuran relationships. Many families and genera appear to be poly- or paraphyletic suggesting a need for further taxonomic revisions at these levels. A divergence time analysis provides key insights into the origins of major lineages and events and the timing of morphological (body form) and ecological (habitat) transitions. Living anomuran biodiversity is the product of 2 major changes in the tempo of diversification; our initial insights suggest that the acquisition of a crab-like form did not act as a key innovation.
PMCID: PMC3708748  PMID: 23786343
Anomura; Phylogeny; Divergence times; Diversification rates; Molecular; Morphology; Character evolution; Next-generation sequencing
18.  Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia) 
Sexuality and reproductive mode are two fundamental life-history traits that exhibit largely unexplained macroevolutionary patterns among the major groups of multicellular organisms. For example, the cnidarian class Anthozoa (corals and anemones) is mainly comprised of gonochoric (separate sex) brooders or spawners, while one order, Scleractinia (skeleton-forming corals), appears to be mostly hermaphroditic spawners. Here, using the most complete phylogeny of scleractinians, we reconstruct how evolutionary transitions between sexual systems (gonochorism versus hermaphrodism) and reproductive modes (brooding versus spawning) have generated large-scale taxonomic patterns in these characters. Hermaphrodites have independently evolved in three large, distantly related lineages consisting of mostly reef-building species. Reproductive mode in corals has evolved at twice the rate of sexuality, while the evolution of sexuality has been heavily biased: gonochorism is over 100 times more likely to be lost than gained, and can only be acquired by brooders. This circuitous evolutionary pathway accounts for the prevalence of hermaphroditic spawners among reef-forming scleractinians, despite their ancient gonochoric heritage.
PMCID: PMC2992726  PMID: 20659935
coral reef; evolution; life history; phylogeny; reproduction
19.  Evolutionary insights into scleractinian corals using comparative genomic hybridizations 
BMC Genomics  2012;13:501.
Coral reefs belong to the most ecologically and economically important ecosystems on our planet. Yet, they are under steady decline worldwide due to rising sea surface temperatures, disease, and pollution. Understanding the molecular impact of these stressors on different coral species is imperative in order to predict how coral populations will respond to this continued disturbance. The use of molecular tools such as microarrays has provided deep insight into the molecular stress response of corals. Here, we have performed comparative genomic hybridizations (CGH) with different coral species to an Acropora palmata microarray platform containing 13,546 cDNA clones in order to identify potentially rapidly evolving genes and to determine the suitability of existing microarray platforms for use in gene expression studies (via heterologous hybridization).
Our results showed that the current microarray platform for A. palmata is able to provide biological relevant information for a wide variety of coral species covering both the complex clade as well the robust clade. Analysis of the fraction of highly diverged genes showed a significantly higher amount of genes without annotation corroborating previous findings that point towards a higher rate of divergence for taxonomically restricted genes. Among the genes with annotation, we found many mitochondrial genes to be highly diverged in M. faveolata when compared to A. palmata, while the majority of nuclear encoded genes maintained an average divergence rate.
The use of present microarray platforms for transcriptional analyses in different coral species will greatly enhance the understanding of the molecular basis of stress and health and highlight evolutionary differences between scleractinian coral species. On a genomic basis, we show that cDNA arrays can be used to identify patterns of divergence. Mitochondrion-encoded genes seem to have diverged faster than nuclear encoded genes in robust corals. Accordingly, this needs to be taken into account when using mitochondrial markers for scleractinian phylogenies.
PMCID: PMC3469353  PMID: 22994626
Coral reefs; Comparative genomic hybridization (CGH); Microarray; Mitochondria; Evolution
20.  Discordance between morphological and molecular species boundaries among Caribbean species of the reef sponge Callyspongia 
Ecology and Evolution  2015;5(3):663-675.
Sponges are among the most species-rich and ecologically important taxa on coral reefs, yet documenting their diversity is difficult due to the simplicity and plasticity of their morphological characters. Genetic attempts to identify species are hampered by the slow rate of mitochondrial sequence evolution characteristic of sponges and some other basal metazoans. Here we determine species boundaries of the Caribbean coral reef sponge genus Callyspongia using a multilocus, model-based approach. Based on sequence data from one mitochondrial (COI), one ribosomal (28S), and two single-copy nuclear protein-coding genes, we found evolutionarily distinct lineages were not concordant with current species designations in Callyspongia. While C. fallax,C. tenerrima, and C. plicifera were reciprocally monophyletic, four taxa with different morphologies (C. armigera,C. longissima,C. eschrichtii, and C. vaginalis) formed a monophyletic group and genetic distances among these taxa overlapped distances within them. A model-based method of species delimitation supported collapsing these four into a single evolutionary lineage. Variation in spicule size among these four taxa was partitioned geographically, not by current species designations, indicating that in Callyspongia, these key taxonomic characters are poor indicators of genetic differentiation. Taken together, our results suggest a complex relationship between morphology and species boundaries in sponges.
PMCID: PMC4328770
Gene tree; Porifera; species delimitation; species tree; spicule
21.  Phylogenetic Relationships and the Evolution of Regulatory Gene Sequences in the Parrotfishes 
Regulatory genes control the expression of other genes and are key components of developmental processes such as segmentation and embryonic construction of the skull in vertebrates. Here we examine the variability and evolution of three vertebrate regulatory genes, addressing issues of their utility for phylogenetics and comparing the rates of genetic change seen in regulatory loci to the rates seen in other genes in the parrotfishes. The parrotfishes are a diverse group of colorful fishes from coral reefs and seagrasses worldwide and have been placed phylogenetically within the family Labridae. We tested phylogenetic hypotheses among the parrotfishes, with a focus on the genera Chlorurus and Scarus, by analyzing eight gene fragments for 42 parrotfishes and eight outgroup species. We sequenced mitochondrial 12s rRNA (967 bp), 16s rRNA (577 bp), and cytochrome b (477 bp). From the nuclear genome, we sequenced part of the protein-coding genes rag2 (715 bp), tmo4c4 (485 bp), and the developmental regulatory genes otx1 (672 bp), bmp4 (488 bp), and dlx2 (522 bp). Bayesian, likelihood, and parsimony analyses on the resulting 4903 bp of DNA sequence produced similar topologies that confirm the monophyly of the scarines and provide a phylogeny at the species level for portions of the genera Scarus and Chlorurus. Four major clades of Scarus were recovered, with three distributed in the Indo-Pacific and one containing Caribbean/Atlantic taxa. Molecular rates suggest a Miocene origin of the parrotfishes (22 mya) and a recent divergence of species within Scarus and Chlorurus, within the past 5 million years. Developmentally important genes made a significant contribution to phylogenetic structure, and rates of genetic evolution were high in bmp4, similar to other coding nuclear genes, but low in otx1 and the dlx2 exons. Synonymous and nonsynonymous substitution patterns in developmental regulatory genes support the hypothesis of stabilizing selection during the history of these genes, with several phylogenetic regions of accelerated nonsynonymous change detected in the phylogeny.
PMCID: PMC3418665  PMID: 18621133
phylogenetics; coral reef fishes; parrotfishes; regulatory genes; molecular clock; bmp4; dlx2; otx1
22.  Molecular phylogeny of microhylid frogs (Anura: Microhylidae) with emphasis on relationships among New World genera 
Over the last ten years we have seen great efforts focused on revising amphibian systematics. Phylogenetic reconstructions derived from DNA sequence data have played a central role in these revisionary studies but have typically under-sampled the diverse frog family Microhylidae. Here, we present a detailed phylogenetic study focused on expanding previous hypotheses of relationships within this cosmopolitan family. Specifically, we placed an emphasis on assessing relationships among New World genera and those taxa with uncertain phylogenetic affinities (i.e., incertae sedis).
One mitochondrial and three nuclear genes (about 2.8 kb) were sequenced to assess phylogenetic relationships. We utilized an unprecedented sampling of 200 microhylid taxa representing 91% of currently recognized subfamilies and 95% of New World genera. Our analyses do not fully resolve relationships among subfamilies supporting previous studies that have suggested a rapid early diversification of this clade. We observed a close relationship between Synapturanus and Otophryne of the subfamily Otophryninae. Within the subfamily Gastrophryninae relationships between genera were well resolved.
Otophryninae is distantly related to all other New World microhylids that were recovered as a monophyletic group, Gastrophryninae. Within Gastrophryninae, five genera were recovered as non-monophyletic; we propose taxonomic re-arrangements to render all genera monophyletic. This hypothesis of relationships and updated classification for New World microhylids may serve as a guide to better understand the evolutionary history of this group that is apparently subject to convergent morphological evolution and chromosome reduction. Based on a divergence analysis calibrated with hypotheses from previous studies and fossil data, it appears that microhylid genera inhabiting the New World originated during a period of gradual cooling from the late Oligocene to mid Miocene.
PMCID: PMC3561245  PMID: 23228209
Microhylidae; Phylogeny; Systematics; Subfamilies; New World genera
23.  An Estimation of Erinaceidae Phylogeny: A Combined Analysis Approach 
PLoS ONE  2012;7(6):e39304.
Erinaceidae is a family of small mammals that include the spiny hedgehogs (Erinaceinae) and the silky-furred moonrats and gymnures (Galericinae). These animals are widely distributed across Eurasia and Africa, from the tundra to the tropics and the deserts to damp forests. The importance of these animals lies in the fact that they are the oldest known living placental mammals, which are well represented in the fossil record, a rarity fact given their size and vulnerability to destruction during fossilization. Although the Family has been well studied, their phylogenetic relationships remain controversial. To test previous phylogenetic hypotheses, we combined molecular and morphological data sets, including representatives of all the genera.
Methodology and Principal Findings
We included in the analyses 3,218 bp mitochondrial genes, one hundred and thirty-five morphological characters, twenty-two extant erinaceid taxa, and five outgroup taxa. Phylogenetic relationships were reconstructed using both partitioned and combined data sets. As in previous analyses, our results strongly support the monophyly of both subfamilies (Galericinae and Erinaceinae), the Hylomys group (to include Neotetracus and Neohylomys), and a sister-relationship of Atelerix and Erinaceus. As well, we verified that the extremely long branch lengths within the Galericinae are consistent with their fossil records. Not surprisingly, we found significant incongruence between the phylogenetic signals of the genes and the morphological characters, specifically in the case of Hylomys parvus, Mesechinus, and relationships between Hemiechinus and Paraechinus.
Although we discovered new clues to understanding the evolutionary relationships within the Erinaceidae, our results nonetheless, strongly suggest that more robust analyses employing more complete taxon sampling (to include fossils) and multiple unlinked genes would greatly enhance our understanding of the Erinaceidae. Until then, we have left the nomenclature of the taxa unchanged; hence it does not yet precisely reflect their phylogenetic relationships or the depth of their genetic diversity.
PMCID: PMC3380021  PMID: 22745729
24.  The Evolution of the Four Subunits of Voltage-Gated Calcium Channels: Ancient Roots, Increasing Complexity, and Multiple Losses 
Genome Biology and Evolution  2014;6(9):2210-2217.
The alpha subunits of voltage-gated calcium channels (Cavs) are large transmembrane proteins responsible for crucial physiological processes in excitable cells. They are assisted by three auxiliary subunits that can modulate their electrical behavior. Little is known about the evolution and roles of the various subunits of Cavs in nonbilaterian animals and in nonanimal lineages. For this reason, we mapped the phyletic distribution of the four channel subunits and reconstructed their phylogeny. Although alpha subunits have deep evolutionary roots as ancient as the split between plants and opistokonths, beta subunits appeared in the last common ancestor of animals and their close-relatives choanoflagellates, gamma subunits are a bilaterian novelty and alpha2/delta subunits appeared in the lineage of Placozoa, Cnidaria, and Bilateria. We note that gene losses were extremely common in the evolution of Cavs, with noticeable losses in multiple clades of subfamilies and also of whole Cav families. As in vertebrates, but not protostomes, Cav channel genes duplicated in Cnidaria. We characterized by in situ hybridization the tissue distribution of alpha subunits in the sea anemone Nematostella vectensis, a nonbilaterian animal possessing all three Cav subfamilies common to Bilateria. We find that some of the alpha subunit subtypes exhibit distinct spatiotemporal expression patterns. Further, all six sea anemone alpha subunit subtypes are conserved in stony corals, which separated from anemones 500 MA. This unexpected conservation together with the expression patterns strongly supports the notion that these subtypes carry unique functional roles.
PMCID: PMC4202318  PMID: 25146647
voltage-gated calcium channel; ion channel; Cnidaria; Nematostella vectensis; evolution of nervous system
25.  Spatial and Species Variations in Bacterial Communities Associated with Corals from the Red Sea as Revealed by Pyrosequencing 
Applied and Environmental Microbiology  2012;78(20):7173-7184.
Microbial associations with corals are common and are most likely symbiotic, although their diversity and relationships with environmental factors and host species remain unclear. In this study, we adopted a 16S rRNA gene tag-pyrosequencing technique to investigate the bacterial communities associated with three stony Scleractinea and two soft Octocorallia corals from three locations in the Red Sea. Our results revealed highly diverse bacterial communities in the Red Sea corals, with more than 600 ribotypes detected and up to 1,000 species estimated from a single coral species. Altogether, 21 bacterial phyla were recovered from the corals, of which Gammaproteobacteria was the most dominant group, and Chloroflexi, Chlamydiae, and the candidate phylum WS3 were reported in corals for the first time. The associated bacterial communities varied greatly with location, where environmental conditions differed significantly. Corals from disturbed areas appeared to share more similar bacterial communities, but larger variations in community structures were observed between different coral species from pristine waters. Ordination methods identified salinity and depth as the most influential parameters affecting the abundance of Vibrio, Pseudoalteromonas, Serratia, Stenotrophomonas, Pseudomonas, and Achromobacter in the corals. On the other hand, bacteria such as Chloracidobacterium and Endozoicomonas were more sensitive to the coral species, suggesting that the host species type may be influential in the associated bacterial community, as well. The combined influences of the coral host and environmental factors on the associated microbial communities are discussed. This study represents the first comparative study using tag-pyrosequencing technology to investigate the bacterial communities in Red Sea corals.
PMCID: PMC3457102  PMID: 22865078

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