srDna-based taxonomic affinities of algal symbionts from a planktonic foraminifer and a solitary radiolarian

Planktonic sarcodines (acantharia, radiolaria, and planktonic foraminifera) are oceanic amoeboid protozoa that often harbor a variety of microalgae as intracellular symbionts. The identity and function of these endosymbiotic algae have intrigued and perplexed biologists for more than a century. The most conspicuous and well‐studied symbiotic algae of planktonic foraminifera and radiolaria are dinoflagellates, but a variety of nondinoflagellate taxa have also been reported. Ultrastructural features have been used to characterize some of these nondinoflagellate algae, but rarely has this led to clear taxonomic affiliations. We analyzed the nuclear small subunit ribosomal DNA (srDNA) isolated from the symbionts of the spinose planktonic foraminiferan Globigerinella siphonifera d'Orbigny (=Globigerinella aequilateralis Brady) and a solitary radiolarian (Spongodrymus sp. Haeckel) in order to determine the identity of these symbionts. The small coccoid algae isolated from G. siphonifera correspond to the Type I symbionts described by Faber et al. (1988) . Phylogenetic analysis of the srDNA sequences places these symbionts within the prymnesiophyte (haptophyte) lineage, closer to Prymnesium Conrad than to Phaeocystis Lagerheim. To our knowledge, this is the first confirmed case of a symbiotic prymnesiophyte. In addition, we were able to examine the level of sequence heterogeneity between symbionts isolated from different individuals of a single host species. The three isolates in this study had srDNA sequences that were almost identical, indicating that the three were all of the same species. Very green symbiotic algae were isolated from three solitary radiolaria identified as species of Spongodrymus. The symbiont srDNA sequences from the three individual hosts were identical to each other, again implicating a single species of algae in that symbiotic association. These symbionts are prasinophytes most closely related to the clade containing Tetaselmis convolutae Norris, Hori et Chihara. Tetraselmis convolutae is the algal symbiont of the marine flatworm, Convolutae roscoffensis Graff.     

Phylogenetic incongruence between dinoflagellate endosymbionts (Symbiodinium) and their host foraminifera (Sorites): small-subunit ribosomal RNA gene sequence evidence

Phototrophic dinoflagellate zooxanthellae commonly occur as endosymbionts in many planktic and certain benthic foraminifera (soritids). Many taxonomic issues and specific identities of foraminiferal dinoflagellates are not yet resolved. To assess taxonomic affinities among other dinoflagellates, we have determined the complete nucleotide sequence of the small-subunit rRNA coding region from Symbiodinium sp., an endosymbiotic dinoflagellate of the larger foraminifer Sorites orbiculus. The poly merase chain reaction was adopted for the in vitro amplification of ribosomal DNA, utilizing primers complementary to conserved regions. PCR-amplified DNA was directly sequenced and the sequence was aligned to all complete 18S-rDNA dinoflagellate sequences currently available through GenBank. Apicomplexan, ciliate, chromistacean, and rhodophycean sequences were added to infer across-kingdom phylogenetic relationships. Phylogenetic analysis of aligned nucleotide sequences produced a single most parsimonious tree (generated by the branch and bound method of PAUP). The inferred phylogeny indicates that the dinoflagellate extracted from the foraminifer Sorites orbiculus is a sister taxon to the symbiont present in the larger foraminifera Marginopora kudakajimaensis, but only distantly related to the dinoflagellate isolated from the soritid Amphisorus hemprichii. The sequence heterogeneity demonstrates a high degree of genetic diversity among Symbiodinium-like zooxanthellae and re-emphasizes that they are a variety of distinct entities.The inferred molecular phylogenetic relationships among symbiotic dinoflagellates are not congruent with the foraminiferal phylogeny based on cladistic methodology. The lack of correlation between the evolutionary history of dinoflagellate symbionts and their foraminiferal hosts argues against co-evolution. This lack of co-evolution implies that flexible recombinations among hosts and symbionts are evolutionarily favorable over permanently associated lineages, at least in these benthic foraminifera.     

Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA

Symbiodinium-like dinoflagellates have been shown to be a diverse group of endosymbionts that associate mutualistically with many kinds of coral reef dwellers, including cnidarians, molluscs, and protists. A high number of genetically ITS types of symbionts have been reported to date. However, whether these recently identified Symbiodinium ITS types indeed represent independent evolutionary lineages is still unsettled. Here I tested the null hypothesis that certain group of symbionts sampled from different geographical locations are derived from a single evolutionary lineage using a nested clade analysis (NCA). I analyzed a total of 174 ITS1 sequences from GenBank and pooled them into 74 ITS1 distinct haplotypes. Using these haplotypes, the statistical parsimony criterion produced 23 independent network trees, each one corresponding to a genetically independent evolving lineage. Some of these lineages revealed certain degree of specificity with some host groups at least at the phylum level. Within the previously described 28S-rDNA phylotype A, five ITS1 lineages were resolved. Phylotypes B and C resolved each in two ITS1 lineages. The highest ITS1 symbiont diversity was observed within the phylotype F, in which 11 lineages were resolved. Moreover, most of these lineages were associated uniquely with protist hosts from the group of foraminiferans. Here it is suggested that this high genetic diversity of endosymbionts associated with foraminiferans is linked with the evolution of soritacean foraminifera, which seems to have been driven by endosymbiosis. Lastly, the absence of genetic recombination presented in this study, suggest a lack of hybridisation at least among the major 28S-rDNA phylotypes within Symbiodinium-like dinoflagellates. This supports highly the idea that these phylotypes are indeed independent evolutionary units, which should be considered at least as different species. Whether they belong to the same genus or to different higher taxa still needs to be revised.     

Brandtodinium gen. nov. and B. nutricula comb. Nov. (Dinophyceae), a dinoflagellate commonly found in symbiosis with polycystine radiolarians

Symbiotic interactions between pelagic hosts and microalgae have received little attention, although they are widespread in the photic layer of the world ocean, where they play a fundamental role in the ecology of the planktonic ecosystem. Polycystine radiolarians (including the orders Spumellaria, Collodaria and Nassellaria) are planktonic heterotrophic protists that are widely distributed and often abundant in the ocean. Many polycystines host symbiotic microalgae within their cytoplasm, mostly thought to be the dinoflagellate Scrippsiella nutricula, a species originally described by Karl Brandt in the late nineteenth century as Zooxanthella nutricula. The free‐living stage of this dinoflagellate has never been characterized in terms of morphology and thecal plate tabulation. We examined morphological characters and sequenced conservative ribosomal markers of clonal cultures of the free‐living stage of symbiotic dinoflagellates isolated from radiolarian hosts from the three polycystine orders. In addition, we sequenced symbiont genes directly from several polycystine‐symbiont holobiont specimens from different oceanic regions. Thecal plate arrangement of the free‐living stage does not match that of Scrippsiella or related genera, and LSU and SSU rDNA‐based molecular phylogenies place these symbionts in a distinct clade within the Peridiniales. Both phylogenetic analyses and the comparison of morphological features of culture strains with those reported for other closely related species support the erection of a new genus that we name Brandtodinium gen. nov. and the recombination of S. nutricula as B. nutricula comb. nov.     

Molecular evidence for host-symbiont specificity in soritid foraminifera

Symbiosis between the dinoflagellate genus Symbiodinium and various invertebrates and protists is an ubiquitous phenomenon in shallow tropical and subtropical waters. Molecular studies undertaken on cnidarian symbionts revealed the presence of several distinctive lineages or subgeneric clades of Symbiodinium whose taxonomic level provides limited information about the specificity between invertebrate hosts and their symbionts. This contrasts with the finding of several Symbiodinium clades being present almost exclusively in foraminifera and belonging to the subfamily Soritinae. To test whether such specificity also exists at a lower taxonomic level within Soritinae, we obtained the SSU rDNA sequences from 159 soritid individuals collected in nine localities worldwide and representing all known morphospecies of this subfamily. For each individual, the symbionts were determined either by sequencing or by RFLP analysis. We distinguished 22 phylotypes of Soritinae in relation with a number of symbiont "groups" corresponding to 3 clades and 5 subclades of Symbiodinium. Among the 22 soritid phylotypes, 14 show strict symbiont specificity and only one was found to be a host for more than two "groups" of Symbiodinium. It is suggested that the strong host-symbiont specificity observed in Soritinae is a combined effect of a selective recognition mechanism, vertical transmission of symbionts, and biogeographical isolation.     

PLANKTONIC SARCODINES: MICROHABITAT FOR OCEANIC DINOFLAGELLATES1

Two morphologically distinct species of free-swimming dinoflagellates belonging to the genus Gyrodinium utilize the spine and rhizopodial environments of planktonic foraminifera and colonial radiolaria as microhabitats. Up to 84% of the sarcodines examined in a given population were associated with these dinoflagellates at densities up to 20,000 cells per sarcodine in some radiolarian colonies. Both dinoflagellate species possess chloroplasts, indicating they are capable of autotrophy. ¹⁴C-labelling experiments with the radiolarian-associated dinoflagellate demonstrate that it can take up inorganic carbon under both light and dark conditions. Ultrastructural evidence suggests the foraminiferal dinoflagellate may be capable of phagotrophy. Hence, these algae should be considered mixotrophs. An unusual cytoplasmic extension used for attachment and possibly feeding occurs in the foraminiferal-associated Gyrodinium and is documented with electron microscopy. Ultrastructural examination suggests this organelle may be hydrostatically controlled and may be an extension of the sac pusule.     

Molecular Identification of Algal Endosymbionts in Large Miliolid Foraminifera: 2. Dinoflagellates

Large miliolid foraminifers of the subfamily Soritinae bear symbiotic dinoflagellates morphologically similar to the species of the "Symbiodinium" complex, commonly found in corals and other marine invertebrates. Soritid foraminifers are abundant in coral reefs and it has been proposed that they share their symbionts with other dinoflagellate-bearing reef dwellers. In order to test this hypothesis, we have analysed partial large subunit ribosomal DNA sequences from dinoflagellates symbionts obtained from 28 foraminiferal specimens, and compared them to the corresponding sequences of Symbiodinium-like endosymbionts from various groups of invertebrates. Phylogenetic analysis of our data shows that all soritid symbionts belong to the "Symbiodinium" species complex, within which they form seven different molecular types (Frl-Fr7). Only one of these types (Fr1) branches within a group of invertebrate symbionts, previously described as type C. The remaining six types form sister groups to coral symbionts previously designed as types B, C, and D. Our data indicate a high genetic diversity and specificity of Symbiodinium-like symbionts in soritids. Except for type C, we have found no evidence for the transmission of symbionts between foraminifers and other symbiont-bearing invertebrates from the same localities. However, exchanges must have occurred frequently between the different species of Soritinae, as suggested by the lack of host specificity and some biogeographical patterns observed in symbiont distribution. Our data suggest that members of the subfamily Soritinae acquired their symbionts at least three times during their history, each acquisition being followed by a rapid diversification and independent radiation of symbionts within the foraminiferal hosts.     

Molecular Identification of Algal Endosymbionts in Large Miliolid Foraminifera: 1. Chlorophytes

Large miliolid foraminifers bear various types of algal endosymbionts including chlorophytes, dinoflagellates, rhodophytes, and diatoms. Symbiosis plays a key role in the adaptation of large foraminifera to survival and growth in oligotrophic seas. The identity and diversity of foraminiferal symbionts, however, remain largely unknown. In the present work we use ribosomal DNA (rDNA) sequences to identify chlorophyte endosymbionts in large miliolid foraminifera of the superfamily Soritacea. Partial 18S and complete Internal Transcribed Spacer (ITS) rDNA sequences were obtained from symbionts of eight species representing all genera of extant chlorophyte-bearing Soritacea. Phylogenetic analysis of the sequences confirms the previous fine structure-based identification of these endosymbionts as belonging to the genus Chlamydomonas. All foraminiferal symbionts form a monophyletic group closely related to Chlamydomonas noctigama. The group is composed of seven types identified in this study, including one previously morphologically described species, Chlamydomonas hedleyi. Each of these types can be considered as a separate species, based on the comparison of genetic differences observed between other established Chlamydomonas species. Several foraminiferal species share the same symbiont type, but only one species, Archaias angulatus, was found to bear more than one type.     

SMALL SUBUNIT rDNA SEQUENCE ANALYSIS OF SYMBIOTIC DINOFLAGELLATES FROM SEVEN SCLERACTINIAN CORALS IN A TAHITIAN LAGOON

The diversity of symbiotic dinoflagellates from reef-building corals collected in the lagoon of Tahiti (South Pacific ocean) was investigated by using a molecular approach. Populations of symbionts (strains or species) of 7 coral species ( Fungia scutaria , F. paumotensis Stutchbury, Pavona cactus Forskål, Leptastrea transversa Kluzinger, Pocillopora verrucosa Ellis and Solender, Montastrea curta Dana, and Acropora formosa Dana) were delimited by phylogenetic analysis of small subunit rDNA sequences. Coral P. verrucosa harbored 2 populations of symbiont SSU rDNA sequences that may correspond to two different Symbiodinium species. Corals F. scutaria and M. curta also seemed to contain two different Symbiodinium species. SSU rDNA dinoflagellate sequences from P. cactus , L. transversa , F. scutaria , F. paumotensis , and P. verrucosa were in the same phylogenetic cluster and showed low variability. For these distantly related coral species, dinoflagellate strains from the same species, rDNA paralogues from the same strain, or closely related Symbiodinium species could not be distinguished because monophyletic subgroups were not observed. SSU rDNA dinoflagellate sequences from A. formosa and M. curta were clearly different from the other Symbiodinium sequences and may represent specific species. This molecular approach highlighted a greater diversity of symbiotic dinoflagellates from corals in South Pacific ( Symbiodinium groups A, B, and C) than that observed in the rest of the Pacific ocean ( Symbiodinium group C). The diversity of symbiotic associations in a restricted area of the lagoon of Tahiti may reflect the complexity of interactions between species of Symbiodinium and corals.     

Molecular phylogeny of a potentially parasitic dinoflagellate isolated from the solitary radiolarian, Thalassicolla nucleata

Thalassicolla nucleata, a solitary radiolarian, has been described as being parasitized by two dinoflagellates, Solenodinium (Syndiniales) and Caryotoma (Blastodiniales). Several T. nucleata were stripped of their extracapsular material and allowed to regenerate their rhizopodial structures without symbionts. Within a week, two were observed to disintegrate, leaving behind non-pigmented swimming dinoflagellate cells. Identical full-length ribosomal sequences were recovered from both samples. Upon alignment and phylogenetic analysis, it was determined that these putative parasite sequences were distinct from Scrippsiella nutricula (the dinoflagellate symbiont of the host), and also from all other dinoflagellate parasites sequenced to date.     

Many corals host thermally resistant symbionts in high-temperature habitat

Physiologically distinct lines of dinoflagellate symbionts, Symbiodinium spp., may confer distinct thermal tolerance thresholds on their host corals. Therefore, if a coral can alternately host distinct symbionts, changes in their Symbiodinium communities might allow corals to better tolerate increasing environmental temperatures. However, researchers are currently debating how commonly coral species can host different symbiont types. We sequenced chloroplast 23 s rDNA from the Symbiodinium communities of nine reef-building coral species across two thermally distinct lagoon pools separated by ~500 m. The hotter of these pools reaches 35°C in the summer months, while the other pool’s maximum temperature is 1.5°C cooler. Across 217 samples from nine species, we found a single haplotype in both Symbiodinium clades A and D, but four haplotypes in Symbiodinium clade C. Eight of nine species hosted a putatively thermally resistant member of clade D Symbiodinium at least once, one of which hosted this clade D symbiont exclusively. Of the remaining seven that hosted multiple Symbiodinium types, six species showed higher proportions of the clade D symbiont in the hotter pool. Average percentage rise in the frequency of the clade D symbiont from the hotter to cooler pool was 52% across these six species. Even though corals hosted members of both the genetically divergent clades D and C Symbiodinium, some showed patterns of host–symbiont specificity within clade C. Both Acropora species that hosted clade C exclusively hosted a member of sub-clade C2, while all three Pocillopora species hosted a member of sub-clade C1 (sensu van Oppen et al. 2001). Our results suggest that coral–algal symbioses often conform to particular temperature environments through changes in the identity of the algal symbiont.     

Low genetic diversity of symbiotic dinoflagellates (Symbiodinium) in scleractinian corals from tropical reefs in southern Hainan Island, China

Endosymbiotic dinoflagellates in the genus Symbiodinium are among the most abundant and important group of photosynthetic protists found in coral reef ecosystems.In order to further characterize this diversity and compare with other regions of the Pacific,samples from 44 species of scleractinian corals representing 20 genera and 9 families,were collected from tropical reefs in southern Hainan Island,China.Denaturing gradient gel electrophoresis fingerprinting of the ribosomal internal transcribed spacer 2 identified 11 genetically distinct Symbiodinium types that have been reported previously.The majority of reef-building coral species (88.6％) harbored only one subcladal type of symbiont,dominated by host-generalist C1 and C3,and was influenced little by the host’s apparent mode of symbiont acquisition.Some species harbored more than one clade of Symbiodinium (clades C,D) concurrently.Although geographically isolated from the rest of the Pacific,the symbiont diversity in southern Hainan Island was relatively low and similar to both the Great Barrier Reef and Hawaii symbiont assemblages (dominated by clade C Symbiodinium).These results indicate that a specialist symbiont is not a prerequisite for existence in remote and isolated areas,but additional work in other geographic regions is necessary to test this idea.     

High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii

The Hawaiian Islands represent one of the most geographically remote locations in the Indo-Pacific, and are a refuge for rare, endemic life. The diversity of symbiotic dinoflagellates (Symbiodinium sp.) inhabiting zooxanthellate corals and other symbiotic cnidarians from the High Islands region was surveyed. From the 18 host genera examined, there were 20 genetically distinct symbiont types (17 in clade C, 1 in clade A, 1 in clade B, and 1 in clade D) distinguished by internal transcribed spacer region 2 sequences. Most types were found to associate with a particular host genus or species and nearly half of them have not been identified in surveys of Western and Eastern Pacific hosts. A clear dominant generalist symbiont is lacking among Hawaiian cnidarians. This is in marked contrast with the symbiont community structures of the western Pacific and Caribbean, which are dominated by a few prevalent generalist symbionts inhabiting numerous host taxa. Geographic isolation, low host diversity, and a high proportion of coral species that directly transmit their symbionts from generation to generation are implicated in the formation of a coral reef community exhibiting high symbiont diversity and specificity.Communicated by H.R. Lasker     

The distribution of <Emphasis Type="Italic">Symbiodinium</Emphasis> diversity within individual host foraminifera

While one-to-one specificity between reef-dwelling hosts and symbiotic dinoflagellates of the genus Symbiodinium may occur, detailed examination of some hosts reveals that they contain multiple symbiont types. Individuals of the foraminifer Amphisorus hemprichii living in Papua New Guinea contained mixed communities of Symbiodinium dominated by symbiont types in clades C and F. Moreover, the types showed a distinct pattern in their distribution across the radius of the foraminifer, with clade F Symbiodinium more prevalent in the center of the host cell. The mixed community of symbionts and their pattern of distribution within the foraminifer is likely the result of processes happening both inside the foraminifer and in its external environment. Persistent mixed symbiont communities in foraminifera may be stabilized through benefits conferred by maintaining multiple symbiont lineages for symbiont shuffling. Alternatively they may be stabilized through a heterogeneous internal host environment, partitioning of symbiont functional roles or limitation of symbiont reproduction by the host. Six factors generally determine the presence of any particular symbiont type within a foraminifer: mode of transmission, availability from the environment, recognition by the host, regulation by the host, competition between lineages, and fitness of the holobiont. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Radiolaria associated with large diversity of marine alveolates

We have isolated cells of unculturable radiolarians from marine coastal waters. Individual cells were subjected to single cell whole genome amplification (SCWGA) and gene-targeted PCR. Using this approach we recover a surprisingly large diversity of sequences related to the enigmatic marine alveolate groups 1 and 2 (MALV I and MALV II) that most likely represent intracellular symbionts or parasites of the radiolarian cells. 18S rDNA phylogeny of the MALV sequences reveals 4 distinct clades of radiolarian associates here named Radiolarian Associated Sequences (RAS) 1-4. One clade of both phaeodarian and radiolarian associates and one clade of only phaeodarian associates are also identified. The MALV sequences cluster according to host type, i.e. sequences from associates identified in radiolarians, fish, copepods, ciliates or dinoflagellates are not intermixed but separated into distinct clades. This implies several independent colonizations of host lineages and links a large diversity of MALV to radiolarian-associated species. This demonstrates that radiolarians may be an important reservoir for MALV, making them a key group for understanding the impact of intracellular symbionts on the marine ecosystem. This study shows that applying SCWGA on unculturable cells is a promising approach to study the vast diversity and interactions of intracellular eukaryote organisms.     

Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity

Like other reef-building corals, members of the genus Acropora form obligate endosymbioses with dinoflagellates (zooxanthellae) belonging to the genus Symbiodinium. Both Symbiodinium and its hosts are diverse assemblages, and the relationships between host and algal genotypes are unclear. In this study, we determined phylogenetic relationships between Symbiodinium isolates from a wide range of Acropora species and plotted the algal genotypes onto a molecular phylogeny of 28 Acropora species, using the same samples for the host and symbiont genotyping. In addition, we performed a preliminary survey of zooxanthella distribution in Acropora species from the central Great Barrier Reef. Three of the four known major zooxanthellae clades were represented in the 168 samples examined, and within the major clade C, three distinct subclades were identified. No evidence was found for coevolution, but several clear patterns of specificity were identified. Moreover, composition of the zooxanthella pool varied among locales and in one host species we found light-related patterns of zooxanthella distribution.     

"Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition

Endosymbiotic dinoflagellates, or "zooxanthellae," are required for the survival of a diverse community of invertebrates that construct and dominate shallow, tropical coral reef ecosystems. Molecular systematics applied to this once understudied symbiont partner, Symbiodinium spp., divide the group into divergent lineages or subgeneric "clades." Within each clade, numerous closely related "types," or species, exhibit distinctive host taxon, geographic, and/or environmental distributions. This diversity is greatest in clade C, which dominates the Indo-Pacific host fauna and shares dominance in the Atlantic-Caribbean with clade B. Two "living" ancestors in this group, C1 and C3, are common to both the Indo-Pacific and Atlantic-Caribbean. With these exceptions, each ocean possesses a diverse clade C assemblage that appears to have independently evolved (adaptively radiated) through host specialization and allopatric differentiation. This phylogeographic evidence suggests that a worldwide selective sweep of C1/C3, or their progenitor, must have occurred before both oceans separated. The probable timing of this event corresponds with the major climactic changes and low CO(2) levels of the late Miocene and/or early Pliocene. Subsequent bursts of diversification have proceeded in each ocean since this transition. An ecoevolutionary expansion to numerous and taxonomically diverse hosts by a select host-generalist symbiont followed by the onset of rapid diversification suggests a radical process through which coral-algal symbioses respond and persist through the vicissitudes of planetary climate change.     

Flexible associations between Pocillopora corals and Symbiodinium limit utility of symbiosis ecology in defining species

Corals in the genus Pocillopora are the primary framework builders of eastern tropical Pacific (ETP) reefs. These corals typically associate with algal symbionts (genus Symbiodinium) in clade C and/or D, with clade D associations having greater thermal tolerance and resistance to bleaching. Recently, cryptic "species" delineations within both Pocillopora and Symbiodinium have been suggested, with host–symbiont specificity used as a supporting taxonomic character in both genera. In particular, it has been suggested that three lineages of Pocillopora (types 1–3) exist in the ETP, of which type 1 is the exclusive host of heat-tolerant Symbiodinium D1. This host specificity has been used to support the species name "Symbiodinium glynni" for this symbiont. To validate these host–symbiont relationships and their taxonomic utility, we identified Pocillopora types and their associated Symbiodinium at three sites in the ETP. We found greater flexibility in host–symbiont combinations than previously reported, with both Pocillopora types 1 and 3 able to host and be dominated by Symbiodinium in clade C or D. The prevalence of certain combinations did vary among sites, showing that a gradient of specificity exists which may be mediated by evolutionary relationships and environmental disturbance history. However, these results limit the utility of apparent host–symbiont specificity (which may have been a result of undersampling) in defining species boundaries in either corals or Symbiodinium. They also suggest that a greater diversity of corals may benefit from the thermal tolerance of clade D symbionts, affirming the need to conserve Pocillopora across its entire geographic and environmental range.