The congruence between phylogenies of tightly associated groups of organisms (cophylogeny) reflects evolutionary links between ecologically important interactions. However, despite being a classic ...example of an obligate symbiosis, tests of cophylogeny between scleractinian corals and their photosynthetic algal symbionts have been hampered in the past because both corals and algae contain genetically unresolved and morphologically cryptic species. Here, we studied co‐occurring, cryptic Pocillopora species from Mo′orea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the host Pocillopora (using complete mitochondrial genomes, genomic loci, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbAncr markers) and tested for cophylogeny. The analysis supported the presence of five Pocillopora species on the fore reef at Mo′orea that mostly hosted either Cladocopium latusorum or C. pacificum. Only Pocillopora species hosting C. latusorum also hosted taxa from Symbiodinium and Durusdinium. In general, the Cladocopium phylogeny mirrored the Pocillopora phylogeny. Within Cladocopium species, lineages also differed in their associations with Pocillopora haplotypes, except those showing evidence of nuclear introgression, and with depth in the two most common Pocillopora species. We also found evidence for a new Pocillopora species (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of these Pocillopora and Cladocopium species and lineages suggest that symbiont speciation is driven by niche diversification in the host, but there is still evidence for symbiont flexibility in some cases.
The extent to which populations persist under environmental stress depends on the reproductive output of individuals that survive the stress. In coral systems, corals bleach in response to stress ...from elevated water temperature. However, little is known of the extent to which thermal stress impairs the reproductive capacity of the survivors over the following years, limiting the capacity to predict how populations will persist in the Anthropocene.
Using histology to quantify the abundance and size of oocytes and spermaries per polyp, we tested how bleaching impairs the reproductive response of the coral Pocillopora meandrina over two reproductive seasons following the 2015 mass bleaching event in the Hawaiian Islands.
We found that smaller colonies not only had a greater probability of bleaching but also suffered greater reproductive impacts over a longer time. In contrast, larger colonies generated comparable reproductive output regardless of bleaching severity, although bleached colonies generated smaller oocytes the year after bleaching.
These results show that reproductive impacts of bleaching are more complex and size‐specific than commonly assumed. Therefore, estimates of bleaching mortality may underestimate the true impact of thermal stress on populations, especially as populations lose larger individuals from repeated and co‐occurring stressors.
A free Plain Language Summary can be found within the Supporting Information of this article.
A free Plain Language Summary can be found within the Supporting Information of this article.
Response diversity in corals Burgess, Scott C.; Johnston, Erika C.; Wyatt, Alex S. J. ...
Ecology (Durham),
06/2021, Volume:
102, Issue:
6
Journal Article
Peer reviewed
Open access
Variation among functionally similar species in their response to environmental stress buffers ecosystems from changing states. Functionally similar species may often be cryptic species representing ...evolutionarily distinct genetic lineages that are morphologically indistinguishable. However, the extent to which cryptic species differ in their response to stress, and could therefore provide a source of response diversity, remains unclear because they are often not identified or are assumed to be ecologically equivalent. Here, we uncover differences in the bleaching response between sympatric cryptic species of the common Indo-Pacific coral, Pocillopora. In April 2019, prolonged ocean heating occurred at Moorea, French Polynesia. 72% of pocilloporid colonies bleached after 22 d of severe heating (>8°C-days) at 10 m depth on the north shore fore reef. Colony mortality ranged from 11% to 42% around the island four months after heating subsided. The majority (86%) of pocilloporids that died from bleaching belonged to a single haplotype, despite twelve haplotypes, representing at least five species, being sampled. Mitochondrial (open reading frame) sequence variation was greater between the haplotypes that experienced mortality versus haplotypes that all survived than it was between nominal species that all survived. Colonies > 30 cm in diameter were identified as the haplotype experiencing the most mortality, and in 1125 colonies that were not genetically identified, bleaching and mortality increased with colony size. Mortality did not increase with colony size within the haplotype suffering the highest mortality, suggesting that size-dependent bleaching and mortality at the genus level was caused instead by differences among cryptic species. The relative abundance of haplotypes shifted between February and August, driven by declines in the same common haplotype for which mortality was estimated directly, at sites where heat accumulation was greatest, and where larger colony sizes occurred. The identification of morphologically indistinguishable species that differ in their response to thermal stress, but share a similar ecological function in terms of maintaining a coral-dominated state, has important consequences for uncovering response diversity that drives resilience, especially in systems with low or declining functional diversity.
Scleractinian corals of the genus Pocillopora (Lamarck, 1816) are notoriously difficult to identify morphologically with considerable debate on the degree to which phenotypic plasticity, ...introgressive hybridization and incomplete lineage sorting obscure well-defined taxonomic lineages. Here, we used RAD-seq to resolve the phylogenetic relationships among seven species of Pocillopora represented by 15 coral holobiont metagenomic libraries. We found strong concordance between the coral holobiont datasets, reads that mapped to the Pocillopora damicornis (Linnaeus, 1758) transcriptome, nearly complete mitochondrial genomes, 430 unlinked high-quality SNPs shared across all Pocillopora taxa, and a conspecificity matrix of the holobiont dataset. These datasets also show strong concordance with previously published clustering of the mitochondrial clades based on the mtDNA open reading frame (ORF). We resolve seven clear monophyletic groups, with no evidence for introgressive hybridization among any but the most recently derived sister species. In contrast, ribosomal and histone datasets, which are most commonly used in coral phylogenies to date, were less informative and contradictory to these other datasets. These data indicate that extant Pocillopora species diversified from a common ancestral lineage within the last ~3 million years. Key to this evolutionary success story may be the high phenotypic plasticity exhibited by Pocillopora species.
Cryptic species that are morphologically similar co-occur because either the rate of competitive exclusion is very slow, or because they are not, in fact, ecologically similar. The processes that ...maintain cryptic local diversity may, therefore, be particularly subtle and difficult to identify. Here, we uncover differences among several cryptic species in their relative abundance across a depth gradient within a dominant and ecologically important genus of hard coral,
Pocillopora
. From extensive sampling unbiased toward morphological characters, at multiple depths on the fore reef around the island of Mo’orea, French Polynesia, we genetically identified 673 colonies in the
Pocillopora
species complex. We identified 14 mitochondrial Open Reading Frame haplotypes (mtORFs, a well-studied and informative species marker used for pocilloporids), which included at least six nominal species, and uncovered differences among haplotypes in their relative abundance at 5, 10, and 20 m at four sites around the island. Differences in relative haplotype abundance across depths were greater than differences among sites separated by several kilometers. The four most abundant species are often visibly indistinguishable at the gross colony level, yet they exhibited stark differences in their associations with light irradiance and daily water temperature variance. The pattern of community composition was associated with frequent cooling in deeper versus shallower water more than warmer temperatures in shallow water. Our results indicate that these cryptic species are not all ecologically similar. The differential abundance of
Pocillopora
cryptic species across depth should promote their coexistence at the reef scale, as well as promote resilience through response diversity.
Coral populations must be able to adapt to changing environmental conditions for coral reefs to persist under climate change. The adaptive potential of these organisms is difficult to forecast due to ...complex interactions between the host animal, dinoflagellate symbionts and the environment. Here we created 26 larval families from six Montipora capitata colonies from a single reef, showing significant, heritable variation in thermal tolerance. Our results indicate that 9.1% of larvae are expected to exhibit four times the thermal tolerance of the general population. Differences in larval thermotolerance were driven mainly by maternal contributions, but we found no evidence that these effects were driven by symbiont identity despite vertical transmission from the dam. We also document no evidence of reproductive incompatibility attributable to symbiont identity. These data demonstrate significant genetic variation within this population which provides the raw material upon which natural selection can act.
Pocillopora tuahiniensis sp. nov. is described based on mitochondrial and nuclear genomic data, algal symbiont genetic data, geographic isolation, and its distribution pattern within reefs that is ...distinct from other sympatric Pocillopora species (Johnston et al. 2022a, b). Mitochondrial and nuclear genomic data reveal that P. tuahiniensis sp. nov. is a unique species, sister to P. verrucosa, and in a clade different from that of P. meandrina (Johnston et al. 2022a). However, the gross in situ colony appearance of P. tuahiniensis sp. nov. cannot easily be differentiated from that of P. verrucosa or P. meandrina at Moorea. By sequencing the mtORF region, P. tuahiniensis sp. nov. can be easily distinguished from other Pocillopora species. Pocillopora tuahiniensis sp. nov. has so far been sampled in French Polynesia, Ducie Island, and Rapa Nui (Armstrong et al. 2023; Edmunds et al. 2016; Forsman et al. 2013; Glin et al. 2017; Mayfield et al. 2015; Oury et al. 2021; Voolstra et al. 2023). On the fore reefs of Moorea, P. tuahiniensis sp. nov. is very abundant 10 m and is one of the most common Pocillopora species at these depths (Johnston et al. 2022b). It can also be found at a much lower abundance at shallow depths on the fore reef and back reef lagoon. The holotype is deposited at the Smithsonian Institution as USNM-SI 1522390 and the mtORF Genbank accession number is OP418359.
Abstract While the presence of morphologically cryptic species is increasingly recognized, we still lack a useful understanding of what causes and maintains co‐occurring cryptic species and its ...consequences for the ecology, evolution, and conservation of communities. We sampled 724 Pocillopora corals from five habitat zones (the fringing reef, back reef, and fore reef at 5, 10, and 20 m) at four sites around the island of Moorea, French Polynesia. Using validated genetic markers, we identified six sympatric species of Pocillopora , most of which cannot be reliably identified based on morphology: P. meandrina (42.9%), P. tuahiniensis (25.1%), P. verrucosa (12.2%), P. acuta (10.4%), P. grandis (7.73%), and P. cf. effusa (2.76%). For 423 colonies (58% of the genetically identified hosts), we also used psbA ncr or ITS2 markers to identify symbiont species (Symbiodiniaceae). The relative abundance of Pocillopora species differed across habitats within the reef. Sister taxa P. verrucosa and P. tuahiniensis had similar niche breadths and hosted the same specialist symbiont species (mostly Cladocopium pacificum ) but the former was more common in the back reef and the latter more common deeper on the fore reef. In contrast, sister taxa P. meandrina and P. grandis had the highest niche breadths and overlaps and tended to host the same specialist symbiont species (mostly C. latusorum ). Pocillopora acuta had the narrowest niche breadth and hosted the generalist, and more thermally tolerant, Durusdinium gynnii . Overall, there was a positive correlation between reef habitat niche breadth and symbiont niche breadth— Pocillopora species with a broader habitat niche also had a broader symbiont niche. Our results show how fine‐scale variation within reefs plays an important role in the generation and coexistence of cryptic species. The results also have important implications for how niche differences affect community resilience, and for the success of coral restoration practices, in ways not previously appreciated.
We quantified benthic community structure on shallow (10 m isobath) reefs separated by 3–130 km on four islands in the south Pacific, and evaluated the roles of disturbances vs. coral recruitment as ...causes of spatial heterogeneity. Reefs were surveyed in 2013 on Moorea, Tahiti, Tetiaroa, and Maiao, with community structure sampled at two sites on each island using photoquadrats. The effects of coral recruitment on population structure were evaluated through genetic analyses of Pocillopora on three of the islands. Benthic community structure with functional group resolution differed among islands and generally among sites, but coral community structure (generic resolution) differed among islands, but generally not among sites. Genetic analyses of Pocillopora using the open reading frame of host mtDNA revealed varying relative abundances of Pocillopora meandrina/Pocillopora eydouxi, Pocillopora verrucosa, Pocillopora effuses, and two unnamed haplotypes on each island. These results suggest that corals on each island represent unique samplings of genetically discrete larval assemblages rather than random samplings of a single larval assemblage. Together, our findings emphasize the extent to which coral community structure varies over a scale of <200 km, and suggests that recruitment from spatially discrete pools of coral larvae plays an important role in creating spatial variation in community structure, even where reefs are connected by prevailing currents.
Species within the scleractinian genus
Lamarck 1816 exhibit extreme phenotypic plasticity, making identification based on morphology difficult. However, the mitochondrial open reading frame (mtORF) ...marker provides a useful genetic tool for identification of most species in this genus, with a notable exception of
and
. Based on recent genomic work, we present a quick and simple, gel-based restriction fragment length polymorphism (RFLP) method for the identification of all six
species occurring in Hawai'i by amplifying either the mtORF region, a newly discovered histone region, or both, and then using the restriction enzymes targeting diagnostic sequences we unambiguously identify each species
Using this approach, we documented frequent misidentification of
species based on colony morphology. We found that
colonies are frequently mistakenly identified as
in Kāne'ohe Bay, O'ahu. We also found that
likely has a northern range limit in the Northwest Hawaiian Islands, above which
was regularly mistaken for
.
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