Gene expression plasticity facilitates acclimatization of a long-lived Caribbean coral across divergent reef environments.

Local adaptation can increase fitness under stable environmental conditions. However, in rapidly changing environments, compensatory mechanisms enabled through plasticity may better promote fitness. Climate change is causing devastating impacts on coral reefs globally and understanding the potential for adaptive and plastic responses is critical for reef management. We conducted a four-year, three-way reciprocal transplant of the Caribbean coral Siderastrea siderea across forereef, backreef, and nearshore populations in Belize to investigate the potential for environmental specialization versus plasticity in this species. Corals maintained high survival within forereef and backreef environments, but transplantation to nearshore environments resulted in high mortality, suggesting that nearshore environments present strong environmental selection. Only forereef-sourced corals demonstrated evidence of environmental specialization, exhibiting the highest growth in the forereef. Gene expression profiling 3.5 years post-transplantation revealed that transplanted coral hosts exhibited profiles more similar to other corals in the same reef environment, regardless of their source location, suggesting that transcriptome plasticity facilitates acclimatization to environmental change in S. siderea. In contrast, algal symbiont (Cladocopium goreaui) gene expression showcased functional variation between source locations that was maintained post-transplantation. Our findings suggest limited acclimatory capacity of some S. siderea populations under strong environmental selection and highlight the potential limits of coral physiological plasticity in reef restoration.

Global change differentially modulates Caribbean coral physiology.

Global change driven by anthropogenic carbon emissions is altering ecosystems at unprecedented rates, especially coral reefs, whose symbiosis with algal symbionts is particularly vulnerable to increasing ocean temperatures and altered carbonate chemistry. Here, we assess the physiological responses of three Caribbean coral (animal host + algal symbiont) species from an inshore and offshore reef environment after exposure to simulated ocean warming (28, 31°C), acidification (300-3290 µatm), and the combination of stressors for 93 days. We used multidimensional analyses to assess how a variety of coral physiological parameters respond to ocean acidification and warming. Our results demonstrate reductions in coral health in Siderastrea siderea and Porites astreoides in response to projected ocean acidification, while future warming elicited severe declines in Pseudodiploria strigosa. Offshore S. siderea fragments exhibited higher physiological plasticity than inshore counterparts, suggesting that this offshore population was more susceptible to changing conditions. There were no plasticity differences in P. strigosa and P. astreoides between natal reef environments, however, temperature evoked stronger responses in both species. Interestingly, while each species exhibited unique physiological responses to ocean acidification and warming, when data from all three species are modelled together, convergent stress responses to these conditions are observed, highlighting the overall sensitivities of tropical corals to these stressors. Our results demonstrate that while ocean warming is a severe acute stressor that will have dire consequences for coral reefs globally, chronic exposure to acidification may also impact coral physiology to a greater extent in some species than previously assumed. Further, our study identifies S. siderea and P. astreoides as potential 'winners' on future Caribbean coral reefs due to their resilience under projected global change stressors, while P. strigosa will likely be a 'loser' due to their sensitivity to thermal stress events. Together, these species-specific responses to global change we observe will likely manifest in altered Caribbean reef assemblages in the future.

Help Me, Symbionts, You're My Only Hope: Approaches to Accelerate our Understanding of Coral Holobiont Interactions.

Tropical corals construct the three-dimensional framework for one of the most diverse ecosystems on the planet, providing habitat to a plethora of species across taxa. However, these ecosystem engineers are facing unprecedented challenges, such as increasing disease prevalence and marine heatwaves associated with anthropogenic global change. As a result, major declines in coral cover and health are being observed across the world's oceans, often due to the breakdown of coral-associated symbioses. Here, we review the interactions between the major symbiotic partners of the coral holobiont-the cnidarian host, algae in the family Symbiodiniaceae, and the microbiome-that influence trait variation, including the molecular mechanisms that underlie symbiosis and the resulting physiological benefits of different microbial partnerships. In doing so, we highlight the current framework for the formation and maintenance of cnidarian-Symbiodiniaceae symbiosis, and the role that immunity pathways play in this relationship. We emphasize that understanding these complex interactions is challenging when you consider the vast genetic variation of the cnidarian host and algal symbiont, as well as their highly diverse microbiome, which is also an important player in coral holobiont health. Given the complex interactions between and among symbiotic partners, we propose several research directions and approaches focused on symbiosis model systems and emerging technologies that will broaden our understanding of how these partner interactions may facilitate the prediction of coral holobiont phenotype, especially under rapid environmental change.

Genetic divergence and range expansion in a western North Pacific coral.

Coral poleward range expansions have recently been observed in response to warming oceans. Range expansion can lead to reduced genetic diversity and increased frequency of deleterious mutations that were rare in core populations, potentially limiting the ability for adaptation and persistence in novel environments. Successful expansions that overcome these founder effects and colonize new habitat have been attributed to multiple introductions from different sources, hybridization with native populations, or rapid adaptive evolution. Here, we investigate population genomic patterns of the reef-building coral Acropora hyacinthus along a latitudinal cline that includes a well-established range expansion front in Japan using 2b-RAD sequencing. A total of 184 coral samples were collected across seven sites spanning from ~24°N to near its northern range front at ~33°N. We uncover the presence of three cryptic lineages of A. hyacinthus, which occupy discrete reefs within this region. Only one lineage is present along the expansion front and we find evidence for its historical occupation of marginal habitats. Within this lineage we also find evidence of bottleneck pressures associated with expansion events including higher clonality, increased linkage disequilibrium, and lower genetic diversity in range edge populations compared to core populations. Asymmetric migration between populations was also detected with lower migration from edge sites. Lastly, we describe genomic signatures of local adaptation potentially attributed to lower winter temperatures experienced at the more recently expanded northern populations. Together these data illuminate the genomic consequences of range expansion in a coral and highlight how adaptation to discrete environments along expansion fronts may facilitate further range expansion in this temperate coral lineage.

Promoting inclusive metrics of success and impact to dismantle a discriminatory reward system in science.

Success and impact metrics in science are based on a system that perpetuates sexist and racist "rewards" by prioritizing citations and impact factors. These metrics are flawed and biased against already marginalized groups and fail to accurately capture the breadth of individuals' meaningful scientific impacts. We advocate shifting this outdated value system to advance science through principles of justice, equity, diversity, and inclusion. We outline pathways for a paradigm shift in scientific values based on multidimensional mentorship and promoting mentee well-being. These actions will require collective efforts supported by academic leaders and administrators to drive essential systemic change.

Common Caribbean corals exhibit highly variable responses to future acidification and warming.

We conducted a 93-day experiment investigating the independent and combined effects of acidification (280-3300 µatm pCO2) and warming (28°C and 31°C) on calcification and linear extension rates of four key Caribbean coral species ( Siderastrea siderea, Pseudodiploria strigosa, Porites astreoides, Undaria tenuifolia) from inshore and offshore reefs on the Belize Mesoamerican Barrier Reef System. All species exhibited nonlinear declines in calcification rate with increasing pCO2. Warming only reduced calcification in Ps. strigosa. Of the species tested, only S. siderea maintained positive calcification in the aragonite-undersaturated treatment . Temperature and pCO2 had no effect on the linear extension of S. siderea and Po. astreoides, and natal reef environment did not impact any parameter examined. Results suggest that S. siderea is the most resilient of these corals to warming and acidification owing to its ability to maintain positive calcification in all treatments, Ps. strigosa and U. tenuifolia are the least resilient, and Po. astreoides falls in the middle. These results highlight the diversity of calcification responses of Caribbean corals to projected global change.