Exploring mechanisms that affect coral cooperation: symbiont transmission mode, cell density and community composition

The coral symbiosis is the linchpin of the reef ecosystem, yet the mechanisms that promote and maintain cooperation between hosts and symbionts have not been fully resolved. We used a phylogenetically controlled design to investigate the role of vertical symbiont transmission, an evolutionary mechanism in which symbionts are inherited directly from parents, predicted to enhance cooperation and holobiont fitness. Six species of coral, three vertical transmitters and their closest horizontally transmitting relatives, which exhibit environmental acquisition of symbionts, were fragmented and subjected to a 2-week thermal stress experiment. Symbiont cell density, photosynthetic function and translocation of photosynthetically fixed carbon between symbionts and hosts were quantified to assess changes in physiological performance and cooperation. All species exhibited similar decreases in symbiont cell density and net photosynthesis in response to elevated temperature, consistent with the onset of bleaching. Yet baseline cooperation, or translocation of photosynthate, in ambient conditions and the reduction in cooperation in response to elevated temperature differed among species. Although Porites lobata and Galaxea acrhelia did exhibit the highest levels of baseline cooperation, we did not observe universally higher levels of cooperation in vertically transmitting species. Post hoc sequencing of the Symbiodinium ITS-2 locus was used to investigate the potential role of differences in symbiont community composition. Interestingly, reductions in cooperation at the onset of bleaching tended to be associated with increased symbiont community diversity among coral species. The theoretical benefits of evolving vertical transmission are based on the underlying assumption that the host-symbiont relationship becomes genetically uniform, thereby reducing competition among symbionts. Taken together, our results suggest that it may not be vertical transmission per se that influences host-symbiont cooperation, but genetic uniformity of the symbiont community, although additional work is needed to test this hypothesis

Intraspecific Differences in Molecular Stress Responses and Coral Pathobiome Contribute to Mortality Under Bacterial Challenge in \u3ci\u3eAcropora millepora\u3c/i\u3e

Disease causes significant coral mortality worldwide; however, factors responsible for intraspecific variation in disease resistance remain unclear. We exposed fragments of eight Acropora millepora colonies (genotypes) to putatively pathogenic bacteria (Vibrio spp.). Genotypes varied from zero to \u3e90% mortality, with bacterial challenge increasing average mortality rates 4-6 fold and shifting the microbiome in favor of stress-associated taxa. Constitutive immunity and subsequent immune and transcriptomic responses to the challenge were more prominent in high-mortality individuals, whereas low-mortality corals remained largely unaffected and maintained expression signatures of a healthier condition (i.e., did not launch a large stress response). Our results suggest that lesions appeared due to changes in the coral pathobiome (multiple bacterial species associated with disease) and general health deterioration after the biotic disturbance, rather than the direct activity of any specific pathogen. If diseases in nature arise because of weaknesses in holobiont physiology, instead of the virulence of any single etiological agent, environmental stressors compromising coral condition might play a larger role in disease outbreaks than is currently thought. To facilitate the diagnosis of compromised individuals, we developed and independently cross-validated a biomarker assay to predict mortality based on genes whose expression in asymptomatic individuals coincides with mortality rates

Divergent transcriptional response to thermal stress among life stages could constrain coral adaptation to climate change

The ability for adaptation to track environmental change depends on how efficiently selection can act on heritable genetic variation. Complex life cycles may promote or constrain adaptation depending on the integration or independence of fitness-related traits over development. Reef-building corals exhibit life cycle complexity and are sensitive to increasing temperatures, highlighting the need to understand heritable potential of the thermal stress response and its developmental regulation. We used tag-based RNA-seq to profile holobiont gene expression of inshore and offshore Porites astreoides adults and recruit offspring in response to a 16-day heat stress, and larvae in response to a 4-day heat stress. Host developmental stage affected both broad patterns of host and symbiont expression, and modulated the stress response in both partners, suggesting that symbiotic interactions could vary between host developmental stages and influence the thermal stress response. Populations also exhibited origin-specific treatment responses, but response magnitude differed among life-stages. Inshore parents and recruit offspring exhibited a more robust stress response, exhibiting greater expression profile divergence and differentially expressing more genes compared to offshore-origin corals. This suggests genetic or epigenetic inheritance of regulatory mechanisms giving rise to expression plasticity, although ontogenetic plasticity as a result of the local reef environment during larval development could also explain the origin effect. However, larval populations exhibited the opposite response, with offshore larvae exhibiting a more robust stress response, possibly due to stage-specific effects or exposure duration. Overall, these results show that putatively adaptive regulatory variation persists in thermally naïve life stages, but thermally responsive genes are stage-specific, which could complicate the evolutionary response of corals to climate change

Symbiont Community Diversity is More Variable in Corals That Respond Poorly to Stress

Coral reefs are declining globally as climate change and local water quality press environmental conditions beyond the physiological tolerances of holobionts—the collective of the host and its microbial symbionts. To assess the relationship between symbiont composition and holobiont stress tolerance, community diversity metrics were quantified for dinoflagellate endosymbionts (Family: Symbiodiniaceae) from eight Acropora millepora genets that thrived under or responded poorly to various stressors. These eight selected genets represent the upper and lower tails of the response distribution of 40 coral genets that were exposed to four stress treatments (and control conditions) in a 10-day experiment. Specifically, four ‘best performer’ coral genets were analyzed at the end of the experiment because they survived high temperature, high pCO2, bacterial exposure, or combined stressors, whereas four ‘worst performer’ genets were characterized because they experienced substantial mortality under these stressors. At the end of the experiment, seven of eight coral genets mainly hosted Cladocopium symbionts, whereas the eighth genet was dominated by both Cladocopium and Durusdinium symbionts. Symbiodiniaceae alpha and beta diversity were higher in worst performing genets than in best performing genets. Symbiont communities in worst performers also differed more after stress exposure relative to their controls (based on normalized proportional differences in beta diversity), than did best performers. A generalized joint attribute model estimated the influence of host genet and treatment on Symbiodiniaceae community composition and identified strong associations among particular symbionts and host genet performance, as well as weaker associations with treatment. Although dominant symbiont physiology and function contribute to host performance, these findings emphasize the importance of symbiont community diversity and stochasticity as components of host performance. Our findings also suggest that symbiont community diversity metrics may function as indicators of resilience and have potential applications in diverse disciplines from climate change adaptation to agriculture and medicine

Signatures of Adaptation and Acclimatization to Reef Flat and Slope Habitats in the Coral Pocillopora damicornis

Strong population-by-habitat interactions across environmental gradients arise from genetic adaptation or acclimatization and represents phenotypic variation required for populations to respond to changing environmental conditions. As such, patterns of adaptation and acclimatization of reef-building corals are integral to predictions of the future of coral reefs under climate warming. The common brooding coral, Pocillopora damicornis, exhibits extensive differences in host genetic and microbial symbiont community composition between depth habitats at Heron Island in the southern Great Barrier Reef, Australia. An 18-month reciprocal field transplant experiment was undertaken to examine the environmental and genetic drivers behind variation in survival, weight gain, heat tolerance and algal symbiont community between the reef flat and slope habitats. We observed population-by-habitat interactions for in situ partial mortality and weight gain, where trait-related fitness of natives was greater than transplants in most cases, consistent with local adaptation. On average, flat colonies transplanted to the slope had a relatively low partial mortality but minimal weight gain, whereas slope colonies transplanted to the flat had relatively high partial mortality and average weight gain. Experimental heat tolerance was always higher in colonies sourced from the flat, but increased when slope colonies were transplanted to the flat, providing evidence of acclimatization in these colonies. The performance of certain slope to flat transplants may have been driven by each colony’s algal symbiont (Symbiodiniaceae) community, and flat variants were observed in a small number of slope colonies that either had a fixed flat composition before transplantation or shuffled after transplantation. Host genotypes of previously identified genetic outlier loci could not predict survival following transplantation, possibly because of low sample size and/or polygenic basis to the traits examined. Local environmental conditions and Symbiodiniaceae composition may provide insight into the adaptive potential to changing environmental conditions

Rebuild the Academy: Supporting academic mothers during COVID-19 and beyond

The issues facing academic mothers have been discussed for decades. Coronavirus Disease 2019 (COVID-19) is further exposing these inequalities as womxn scientists who are parenting while also engaging in a combination of academic related duties are falling behind. These inequities can be solved by investing strategically in solutions. Here we describe strategies that would ensure a more equitable academy for working mothers now and in the future. While the data are clear that mothers are being disproportionately impacted by COVID-19, many groups could benefit from these strategies. Rather than rebuilding what we once knew, let us be the architects of a new world

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.journal articl

Development of Gene Expression Markers of Acute Heat-Light Stress in Reef-Building Corals of the Genus Porites

Coral reefs are declining worldwide due to increased incidence of climate-induced coral bleaching, which will have widespread biodiversity and economic impacts. A simple method to measure the sub-bleaching level of heat-light stress experienced by corals would greatly inform reef management practices by making it possible to assess the distribution of bleaching risks among individual reef sites. Gene expression analysis based on quantitative PCR (qPCR) can be used as a diagnostic tool to determine coral condition in situ. We evaluated the expression of 13 candidate genes during heat-light stress in a common Caribbean coral Porites astreoides, and observed strong and consistent changes in gene expression in two independent experiments. Furthermore, we found that the apparent return to baseline expression levels during a recovery phase was rapid, despite visible signs of colony bleaching. We show that the response to acute heat-light stress in P. astreoides can be monitored by measuring the difference in expression of only two genes: Hsp16 and actin. We demonstrate that this assay discriminates between corals sampled from two field sites experiencing different temperatures. We also show that the assay is applicable to an Indo-Pacific congener, P. lobata, and therefore could potentially be used to diagnose acute heat-light stress on coral reefs worldwide

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships

Phenotypic Data

This file contains .csv files of raw trait measurements described in the paper (growth, bleaching, PAM) in addition to processed symbiont genotyping counts data (percent mapped reads and haplotype files). The accompanying R command file opens specific trait files and calls out columns in each to perform statistical analyses and generate figures as in the accompanying paper