Complex parental effects impact variation in larval thermal tolerance in a vertically transmitting coral.

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.

Small-scale genetic structure of coral populations in Palau based on whole mitochondrial genomes: Implications for future coral resilience.

The ability of local populations to adapt to future climate conditions is facilitated by a balance between short range dispersal allowing local buildup of adaptively beneficial alleles, and longer dispersal moving these alleles throughout the species range. Reef building corals have relatively low dispersal larvae, but most population genetic studies show differentiation only over 100s of km. Here, we report full mitochondrial genome sequences from 284 tabletop corals (Acropora hyacinthus) from 39 patch reefs in Palau, and show two signals of genetic structure across reef scales from 1 to 55 km. First, divergent mitochondrial DNA haplotypes exist in different proportions from reef to reef, causing PhiST values of 0.02 (p = 0.02). Second, closely related sequences of mitochondrial Haplogroups are more likely to be co-located on the same reefs than expected by chance alone. We also compared these sequences to prior data on 155 colonies from American Samoa. In these comparisons, many Haplogroups in Palau were disproportionately represented or absent in American Samoa, and inter-regional PhiST = 0.259. However, we saw three instances of identical mitochondrial genomes between locations. Together, these data sets suggest two features of coral dispersal revealed by occurrence patterns in highly similar mitochondrial genomes. First, the Palau-American Samoa data suggest that long distance dispersal in corals is rare, as expected, but that it is common enough to deliver identical mitochondrial genomes across the Pacific. Second, higher than expected co-occurrence of Haplogroups on the same Palau reefs suggests greater retention of coral larvae on local reefs than predicted by many current oceanographic models of larval movement. Increased attention to local scales of coral genetic structure, dispersal, and selection may help increase the accuracy of models of future adaptation of corals and of assisted migration as a reef resilience intervention.

Coral bleaching resistance variation is linked to differential mortality and skeletal growth during recovery.

The prevalence of global coral bleaching has focused much attention on the possibility of interventions to increase heat resistance. However, if high heat resistance is linked to fitness tradeoffs that may disadvantage corals in other areas, then a more holistic view of heat resilience may be beneficial. In particular, overall resilience of a species to heat stress is likely to be the product of both resistance to heat and recovery from heat stress. Here, we investigate heat resistance and recovery among individual Acropora hyacinthus colonies in Palau. We divided corals into low, moderate, and high heat resistance categories based on the number of days (4-9) needed to reach significant pigmentation loss due to experimental heat stress. Afterward, we deployed corals back onto a reef in a common garden 6-month recovery experiment that monitored chlorophyll a, mortality, and skeletal growth. Heat resistance was negatively correlated with mortality during early recovery (0-1 month) but not late recovery (4-6 months), and chlorophyll a concentration recovered in heat-stressed corals by 1-month postbleaching. However, moderate-resistance corals had significantly greater skeletal growth than high-resistance corals by 4 months of recovery. High- and low-resistance corals on average did not exhibit skeletal growth within the observed recovery period. These data suggest complex tradeoffs may exist between coral heat resistance and recovery and highlight the importance of incorporating multiple aspects of resilience into future reef management programs.

Persistence of phenotypic responses to short-term heat stress in the tabletop coral Acropora hyacinthus.

Widespread mapping of coral thermal resilience is essential for developing effective management strategies and requires replicable and rapid multi-location assays of heat resistance and recovery. One- or two-day short-term heat stress experiments have been previously employed to assess heat resistance, followed by single assays of bleaching condition. We tested the reliability of short-term heat stress resistance, and linked resistance and recovery assays, by monitoring the phenotypic response of fragments from 101 Acropora hyacinthus colonies located in Palau (Micronesia) to short-term heat stress. Following short-term heat stress, bleaching and mortality were recorded after 16 hours, daily for seven days, and after one and two months of recovery. To follow corals over time, we utilized a qualitative, non-destructive visual bleaching score metric that correlated with standard symbiont retention assays. The bleaching state of coral fragments 16 hours post-heat stress was highly indicative of their state over the next 7 days, suggesting that symbiont population sizes within corals may quickly stabilize post-heat stress. Bleaching 16 hours post-heat stress predicted likelihood of mortality over the subsequent 3-5 days, after which there was little additional mortality. Together, bleaching and mortality suggested that rapid assays of the phenotypic response following short-term heat stress were good metrics of the total heat treatment effect. Additionally, our data confirm geographic patterns of intraspecific variation in Palau and show that bleaching severity among colonies was highly correlated with mortality over the first week post-stress. We found high survival (98%) and visible recovery (100%) two months after heat stress among coral fragments that survived the first week post-stress. These findings help simplify rapid, widespread surveys of heat sensitivity in Acropora hyacinthus by showing that standardized short-term experiments can be confidently assayed after 16 hours, and that bleaching sensitivity may be linked to subsequent survival using experimental assessments.

Widespread variation in heat tolerance and symbiont load are associated with growth tradeoffs in the coral Acropora hyacinthus in Palau.

Climate change is dramatically changing ecosystem composition and productivity, leading scientists to consider the best approaches to map natural resistance and foster ecosystem resilience in the face of these changes. Here, we present results from a large-scale experimental assessment of coral bleaching resistance, a critical trait for coral population persistence as oceans warm, in 221 colonies of the coral Acropora hyacinthus across 37 reefs in Palau. We find that bleaching-resistant individuals inhabit most reefs but are found more often in warmer microhabitats. Our survey also found wide variation in symbiont concentration among colonies, and that colonies with lower symbiont load tended to be more bleaching-resistant. By contrast, our data show that low symbiont load comes at the cost of lower growth rate, a tradeoff that may operate widely among corals across environments. Corals with high bleaching resistance have been suggested as a source for habitat restoration or selective breeding in order to increase coral reef resilience to climate change. Our maps show where these resistant corals can be found, but the existence of tradeoffs with heat resistance may suggest caution in unilateral use of this one trait in restoration.

Differential gene expression during substrate probing in larvae of the Caribbean coral Porites astreoides.

The transition from larva to adult is a critical step in the life history strategy of most marine animals. However, the genetic basis of this life history change remains poorly understood in many taxa, including most coral species. Recent evidence suggests that coral planula larvae undergo significant changes at the physiological and molecular levels throughout the development. To investigate this, we characterized differential gene expression (DGE) during the transition from planula to adult polyp in the abundant Caribbean reef-building coral Porites astreoides, that is from nonprobing to actively substrate-probing larva, a stage required for colony initiation. This period is crucial for the coral, because it demonstrates preparedness to locate appropriate substrata for settlement based on vital environmental cues. Through RNA-Seq, we identified 860 differentially expressed holobiont genes between probing and nonprobing larvae (p ≤ .01), the majority of which were upregulated in probing larvae. Surprisingly, differentially expressed genes of endosymbiotic dinoflagellate origin greatly outnumbered coral genes, compared with a nearly 1:1 ratio of coral-to-dinoflagellate gene representation in the holobiont transcriptome. This unanticipated result suggests that dinoflagellate endosymbionts may play a significant role in the transition from nonprobing to probing behaviour in dinoflagellate-rich larvae. Putative holobiont genes were largely involved in protein and nucleotide binding, metabolism and transport. Genes were also linked to environmental sensing and response and integral signalling pathways. Our results thus provide detailed insight into molecular changes prior to larval settlement and highlight the complex physiological and biochemical changes that occur in early transition stages from pelagic to benthic stages in corals, and perhaps more importantly, in their endosymbionts.