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Understanding connectivity between populations is key to identifying hotspots of diversity, dispersal sinks and sources, and effective management units for natural resources. Multi-species connectivity seeks to overcome species-specific idiosyncrasies to identify shared patterns that are most critical to spatial management. The linear Hawaiian archipelago provides an excellent platform to assess multi-species connectivity patterns, with shared boundaries to gene flow identified across a majority of the 41 coral reef species surveyed to date. Here, we evaluate genome-scale data by comparing consistency and resolution to previous connectivity studies using far fewer loci. We used pool-seq to genotype 22,503–232,730 single nucleotide polymorphisms per species (625,215 SNPs total) from the same individuals published in previous studies of two fishes, two corals, and two lobsters. Additionally, one coral species (Pocillopora meandrina) without previous archipelago-wide population genetic data was included. With greater statistical power, most genetic differences between pairwise comparisons of islands were significant (250 of 308), consistent with the most recent larval dispersal models for the Hawaiian Archipelago. These data reveal significant differentiation at a finer scale than previously reported using single-marker studies, yet did not overturn any of the conclusions or management implications drawn from previous studies. We confirm that population genomic datasets are consistent with previously reported patterns of multispecies connectivity but add a finer layer of population resolution that is pertinent to management. 

Abstract Cryptic species (evolutionarily distinct lineages that do not align with morphologically defined species) are being increasingly discovered but are poorly integrated into ecological theory. In particular, we still lack a useful understanding of if and how cryptic species differ in ways that affect community recovery from disturbances and responses to anthropogenic stressors, such as the removal of consumers and pollution from nutrients. On coral reefs, nutrient pollution increases the growth of macroalgae that displace corals. Reductions in herbivorous fishes reduce the suppression of macroalgae, while reductions in coralivorous fishes reduce predation on corals. An unresolved question is if and how cryptic coral species respond differently to these impacts, thereby differing in their ability to influence coral community dynamics and maintain coral dominance. Therefore, we assessed how the response of crypticPocilloporaspecies over a period of three years following a simulated disturbance from a cyclone depended on the experimental reduction of fish consumer pressure and nutrient addition. After three years, five morphologically cryptic, but genetically distinct,Pocilloporaspecies recruited to the reef. However, recruitment was dominated by two species:Pocillopora tuahiniensis(46%) andPocillopora meandrina(43%). Under ambient conditions, recruitment ofP. tuahiniensisandP. meandrinawas similar, but experimentally reducing consumer pressure increased recruitment ofP. tuahiniensisby up to 73% and reduced recruitment ofP. meandrinaby up to 49%. In both species, nutrient enrichment increased recruitment and colony growth rates equally, but colonies ofP. tuahiniensisgrew faster and were up to 25% larger after three years than those ofP. meandrina,and growth was unaffected by reduced consumer pressure. Predation by excavating corallivorous fish was higher forP. meandrinathan forP. tuahiniensis, especially under nutrient enrichment. In contrast, polyp extension (an indicator of elevated heterotrophic feeding as well as susceptibility and attractiveness to corallivores) was lower forP. meandrinathan forP. tuahiniensis, especially under low to medium consumer pressure. Overall, we uncovered ecological differences in the response of morphologically cryptic foundation species to two pervasive stressors on coral reefs. Our results demonstrate how cryptic species respond differently to key anthropogenic stressors, which may contribute to response diversity that can support ecological resilience or increase extinction risk. 

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 724Pocilloporacorals 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 ofPocillopora, 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%), andP.cf.effusa(2.76%). For 423 colonies (58% of the genetically identified hosts), we also usedpsbA^ncror ITS2 markers to identify symbiont species (Symbiodiniaceae). The relative abundance ofPocilloporaspecies differed across habitats within the reef. Sister taxaP. verrucosaandP. tuahiniensishad similar niche breadths and hosted the same specialist symbiont species (mostlyCladocopium pacificum) but the former was more common in the back reef and the latter more common deeper on the fore reef. In contrast, sister taxaP. meandrinaandP. grandishad the highest niche breadths and overlaps and tended to host the same specialist symbiont species (mostlyC. latusorum).Pocillopora acutahad 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—Pocilloporaspecies 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. 

Abstract The susceptibility of corals to environmental stress is determined by complex interactions between host genetic variation and the Symbiodiniaceae family community. We exposed genotypes of Montipora capitata hosting primarily Cladocopium or Durusdinium symbionts to ambient conditions and an 8-day heat stress. Symbionts’ cell surface glycan composition differed between genera and was significantly affected by temperature and oxidative stress. The metabolic profile of coral holobionts was primarily shaped by symbionts identity, but was also strongly responsive to oxidative stress. At peak temperature stress, betaine lipids in Cladocopium were remodeled to more closely resemble the abundance and saturation state of Durusdinium symbionts, which paralleled a larger metabolic shift in Cladocopium. Exploring how Symbiodiniaceae members regulate stress and host-symbiont affinity helps identify the traits contributing to coral resilience under climate change. 

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 Mo’orea. 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; Gélin et al. 2017; Mayfield et al. 2015; Oury et al. 2021; Voolstra et al. 2023). On the fore reefs of Mo’orea, 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.  

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 days 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. 

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.