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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, crypticPocilloporaspecies from Mo′orea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the hostPocillopora(using complete mitochondrial genomes, genomic loci, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbA^ncrmarkers) and tested for cophylogeny. The analysis supported the presence of fivePocilloporaspecies on the fore reef at Mo′orea that mostly hosted eitherCladocopium latusorumorC. pacificum.OnlyPocilloporaspecies hostingC. latusorumalso hosted taxa fromSymbiodiniumandDurusdinium. In general, theCladocopiumphylogeny mirrored thePocilloporaphylogeny. WithinCladocopiumspecies, lineages also differed in their associations withPocilloporahaplotypes, except those showing evidence of nuclear introgression, and with depth in the two most commonPocilloporaspecies. We also found evidence for a newPocilloporaspecies (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of thesePocilloporaandCladocopiumspecies 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.

 

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^oC‐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.

 

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 coralPocillopora meandrinaover 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 freePlain Language Summarycan be found within the Supporting Information of this article.

 

For nearly 50 years, analyses of coral physiology have used small coral fragments (nubbins) to make inferences about larger colonies. However, scaling in corals shows that linear extrapolations from nubbins to whole colonies can be misleading, because polyps in nubbins are divorced of their morphologically complex and physiologically integrated corallum. We tested for the effects of integration among branches in determining size-dependent calcification of the coral Pocillopora spp. under elevated P CO 2 . Area-normalized net calcification was compared between branches (nubbins), aggregates of nubbins (complex morphologies without integration) and whole colonies (physiologically integrated) at 400 versus approximately 1000 µatm P CO 2 . Net calcification was unaffected by P CO 2 , but differed among colony types. Single nubbins grew faster than whole colonies, but when aggregated, nubbins changed calcification to match whole colonies even though they lacked integration among branches. Corallum morphology causes the phenotype of branching corals to differ from the summation of their branches. 

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 towards 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.