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Biology subjects

Bay, L. K.

Publications and source records attributed to Bay, L. K..

16 recordsLinked to original sources

CRISPR/Cas9-mutagenesis reveals that varying dependence on HSF1 is associated with differences in coral heat tolerance

Coral reefs face declines due to increasing water temperatures associated with climate change. Major research efforts have focused on determining the mechanisms corals can use to adapt to heat stress and identifying molecular indicators for this adaptation. CRISPR/Cas9-based genomic editing promises a new avenue to study gene function in corals; however, these methods are limited by the annual spawning of corals in the wild. Here, we shifted spawning of the reef-building coral Galaxea fascicularis to access gametes multiple times a year in the lab. We discovered the remarkable plasticity and programmability in coral spawning, which enabled the development of a genetically tractable model coral. To investigate the molecular responses of corals to heat stress, we profiled transcriptional changes in heat-tolerant G. fascicularis and heat-sensitive Acropora millepora during acute heat stress. Comparison of the transcriptional responses to heat stress in larvae of the two species revealed that A. millepora has a stronger magnitude of the early heat stress response than G. fascicularis. This increased response in A. millepora included the upregulation of the conserved transcriptional regulator of heat stress response, Heat Shock Transcription Factor 1 (HSF1), and its predicted targets. CRISPR/Cas9 mutagenesis of HSF1 in both species showed that the heat-tolerant G. fascicularis is less dependent on HSF1 than A. millepora for survival during acute heat stress. These results suggest that differences in HSF1 expression after heat exposure contribute to variation in coral heat tolerance and may be used as biomarkers to predict heat tolerance in wild corals.

genetics↗

Localised admixture triggers parallel adaptation in a coral species trio on the Great Barrier Reef

Hybridisation can shape evolutionary trajectories and fuel rapid adaptation. Yet, whether adaptive introgression repeatedly reconfigures genomes in predictable ways remains largely unknown. Here, we show that three-way admixture drives repeatable parallel differentiation in reef-building corals in the Acropora hyacinthus species complex. Adaptive introgression is confined to the southern Great Barrier Reef, where admixture timing coincides with a recent breakdown in species barriers despite limited historical gene flow. Genome-wide introgression is characterised by numerous shared minor-parent ancestry peaks that are enriched for stress-response genes and under positive selection for parallel adaptive admixture. Our results demonstrate that introgressive hybridisation can be geographically restricted between sympatric marine species and can promote repeated rapid adaptation that transcends species boundaries.

evolutionary biology↗

Long-distance gene flow and contrasting population structures of reef-building corals and their algal symbionts inform adaptive potential across the Western Pacific

The genetic diversity and connectivity of reef-building coral populations are key to their survival in warming oceans. Yet our understanding of corals demographic resilience and adaptive potential is complicated by cryptic species diversity, wide geographic distributions, and complex coral-algal symbioses. To address these challenges, we investigated genetic connectivity and diversity of the broadcast-spawning coral Acropora spathulata and its associated Symbiodiniaceae across 29 reefs spanning the Great Barrier Reef, the Coral Sea, and New Caledonia, using whole-genome sequencing of 1,088 colonies. We identified four genetically distinct coral populations that diverged between 0.27 and 0.65 million years ago, likely due to geographic isolation across thousands of kilometers. These populations maintained asymmetrical gene flow along major ocean currents despite demographic isolation, and sustained large local effective population sizes ([~]2,900), supported by a high dispersal range of [~]100 km per generation. In contrast, their Symbiodiniaceae partners varied over finer spatial scales, with five distinct Cladocopium taxa distributed along latitudinal and cross-shore gradients, likely driven by local environmental conditions. These results suggest that high dispersal capacity and large local population size promote demographic resilience within reef systems, while environment-specific symbioses and long-distance gene flow across reef-systems support adaptation and evolutionary rescue.

molecular biology↗

Multigenerational Tracking of Reef-Building Corals Using CRISPR-Cas9induced Genetic Barcodes and eDNA Metabarcoding

Widespread biodiversity loss driven by human activity has intensified global efforts to restore degraded ecosystems. Yet a key challenge remains: how to track restored individuals and their offspring over time and space to assess the true impact of restoration? This is especially pressing for coral reefs, which support a quarter of all marine species, are in severe decline globally, and are now the focus of growing restoration initiatives worldwide. Here, we demonstrate a novel approach that combines genome editing and environmental DNA (eDNA) monitoring to enable scalable, non-invasive tracking of individual corals and their offspring. Using CRISPR-Cas9, we introduced unique genetic barcodes into non-coding regions of the Acropora millepora genome. These barcodes - stable, heritable, and distributed across the genome - will allow for individual-level identification over multiple generations. We show that these barcodes can be reliably detected in surrounding seawater using eDNA metabarcoding, offering a powerful, non-destructive tool for tracking corals in situ. Together, this approach provides a proof-of-concept for precision monitoring of restoration outcomes, with broad applicability across species and ecosystems.

genetics↗

Metaproteome analysis of the coral holobiont demonstrates algal symbiont dampening under thermal stress

The accelerating loss of coral reefs worldwide due to anthropogenic climate change has led to a myriad of studies aimed at understanding the basis of coral resilience to support reef conservation. Here, we integrate physiological measurements with proteomic and metabolomic profiles to examine species-specific responses to increased temperature in three sympatric reef-building corals from the Great Barrier Reef: Acropora hyacinthus, Porites lobata, and Stylophora pistillata. We find species-specific stress response strategies with A. hyacinthus, a thermally sensitive species, exhibiting rapid decline in endosymbiont physiology, coupled with a one-third reduction in protein abundance. In contrast, P. lobata displayed a delayed physiological response to stress and a muted proteome response, suggesting greater resilience. S. pistillata initially showed minor shifts in the proteome followed by colony "bail-out". Overall, we observed markedly different responses in most biochemical pathways in the three coral species. Nonetheless, some known biomarkers of stress, including heat-shock proteins, showed conserved responses to thermal stress with differences in temporal abundance reflecting bleaching resistance. Our results underscore the species-specific nature of coral responses to thermal stress and highlight proteomic signatures associated with symbiosis breakdown, offering mechanistic insights into coral bleaching susceptibility and resilience.

microbiology↗

Heat-responsive dynamic shifts in alternative splicing of the coral Acropora cervicornis

Climate change has caused drastic declines in corals. As sessile organisms, response to shifting environmental conditions may include changes in gene expression, epigenetic modifications, or the microbiome, but as of yet, a common mechanism of stress response, alternative splicing (AS), has been underexplored in corals. Using short-term acute thermal stress assays, we investigated patterns of AS in the scleractinian coral Acropora cervicornis during response to and a subsequent overnight recovery phase from low (33), medium (35), and high (37) levels of heat stress. We find that 40% of the genomic gene set is subject to AS. Our findings demonstrate conserved and dynamic shifts in splicing profiles during the heat treatment and subsequent recovery phase. AS increased in response to heat stress and was primarily dominated by intron retention in specific classes of transcripts, including those related to splicing regulation itself. While AS returned to baseline levels post-exposure to low heat, AS persisted even after reprieve from higher levels of heat stress. Partial overlap of AS transcripts with differentially expressed genes suggests that AS may represent a distinct and previously underappreciated regulatory mechanism for thermal stress response in corals.

genomics↗

Environmental, host, and symbiont drivers of heat tolerance in a species complex of reef-building corals

Reef-building coral populations are under unprecedented threat from climate warming. Yet, variation in coral heat tolerance exists whereby some colonies can cope with higher sea temperatures than others and thus may hold unique value for conservation and restoration. Here, we quantify variation in heat tolerance of an ecologically important tabular coral species complex across the Great Barrier Reef (GBR) while also measuring genomic variation in the coral host and symbiont partners. Coral bleaching and photochemical traits were measured in 569 colonies within the Acropora hyacinthus species complex from 17 reefs following exposure to standardized acute heat stress assays. We detected substantial variation in heat tolerance, where individual colony thermal thresholds differed by up to 7.3{degrees}C and 5.7{degrees}C among and within reefs, respectively. Sea surface temperature climatology was the strongest predictor of heat tolerance, where colonies from warmer northern and inshore reefs typically exhibited the highest thermal thresholds, while colonies from cooler southern reefs were able to tolerate greater temperature increases relative to their local summer temperatures. Heat tolerance was also positively associated with exposure to thermal stress in the weeks preceding measurements. Assignment of colonies to host genomic clusters revealed four putative species within the A. hyacinthus complex that did not vary in their responses to experimental heat stress. Symbiodiniaceae communities within colonies were comprised primarily of Cladocopium ITS2 variants that differed spatially but had minimal effect on heat tolerance. Between 36 - 80% of heat tolerance variation was explained by environmental, host, and symbiont genomic predictors, leaving 20 - 64% to be explained by additional underlying drivers such as functional genomic variation not measured here. These results may be used to inform conservation and restoration actions, including targeting heat tolerant individuals for selective breeding, and will provide a foundation for evaluating the genomic basis of heat tolerance.

ecology↗

Quantifying the thermal tolerance traits of individual corals reveals widespread variation across the Great Barrier Reef

Adaptation of reef-building corals to global warming depends upon standing heritable variation in tolerance traits upon which selection can act. Yet limited knowledge exists on heat tolerance variation among conspecific individuals separated by meters to hundreds of kilometers. Here, we performed standardized acute heat stress assays to quantify the thermal tolerance traits of 768 colonies of Acropora spathulata from 14 reefs spanning 1060 km (9.5{degrees} latitude) of the Great Barrier Reef. Thermal thresholds for photochemical efficiency and chlorophyll retention varied considerably among individual colonies both among reefs ([~]6 {degrees}C) and within reefs ([~]3 {degrees}C). Although tolerance rankings of colonies varied between traits, the most heat tolerant corals (i.e. top 25% of each trait) were found at virtually all reefs, indicating widespread phenotypic variation. Reef-scale environmental predictors explained 12-62% of trait variation. Corals exposed to high thermal averages and recent thermal stress exhibited the greatest photochemical performance, likely reflecting local adaptation and stress pre-acclimatization, and the lowest chlorophyll retention suggesting stress pre- sensitization. Importantly, heat tolerance relative to local summer temperatures was the greatest on southern reefs suggestive of higher adaptive potential. These results can be used to identify naturally tolerant coral populations and individuals for conservation and restoration applications.

ecology↗

High survival following bleaching highlights the resilience of a highly disturbed region of the Great Barrier Reef

Natural bleaching events provide an opportunity to examine how local scale environmental variation influences bleaching severity and recovery. During the 2020 marine heatwave, we documented widespread and severe coral bleaching (75 - 98% of coral cover) throughout the Keppel Islands in the Southern inshore Great Barrier Reef. Acropora, Pocillopora and Porites were the most severely affected genera, while Montipora was comparatively less susceptible. Site-specific heat-exposure metrics were not correlated with Acropora bleaching severity, but recovery was faster at sites that experienced lower heat exposure. Despite severe bleaching and exposure to accumulated heat that often results in coral mortality (degree heating weeks [~] 4 - 8), cover remained stable. Approximately 94% of fate-tracked Acropora millepora colonies survived, perhaps owing to reduced irradiance stress from high turbidity, heterotrophic feeding, and large tidal flows that can increase mass transfer. Severe bleaching followed by rapid recovery, and the continuing dominance of Acropora populations in the Keppel Islands is indicative of high resilience. These coral communities have survived an 0.8 {degrees}C increase in average temperatures over the last 150 years. However, recovery following the 2020 bleaching was driven by the easing of thermal stress, which may challenge their recovery potential under further warming. Open Research StatementData are not yet provided but are being compiled. Upon acceptance data will be archived on GitHub.

ecology↗

Genetic variation in heat tolerance of the coral Platygyra daedalea offers the potential for adaptation to ocean warming

Climate change induced increases in global ocean temperature represent the greatest threat to the persistence of reef ecosystems and most coral populations are projected to experience temperatures above their current bleaching thresholds annually by 2050. Adaptation to higher temperatures is necessary if corals are to persist in a warming future. While many aspects of heat stress have been well studied, few data are available for predicting the capacity for adaptive cross-generational responses in corals. Consistent sets of heat tolerant genomic markers that reliably predict thermal tolerance have yet to be identified. To address this knowledge gap, we quantified the heritability and genetic variation associated with heat tolerance in Platygyra daedalea from the Great Barrier Reef. We tracked the survival of quantitative genetic crosses of larvae in a heat tolerance selection experiment. We also identified allelic shifts in heat-selected survivors compared with paired, non-selected controls. The narrow-sense heritability of survival under heat stress was 0.66 and a total of 1,069 single nucleotide polymorphisms (SNPs) were associated with different survival probabilities. While 148 SNPs were shared between several experimental crosses, no common SNPs were identified for all crosses suggesting that specific combinations of many markers are responsible for heat tolerance. However, we found two regions that overlap with previously identified loci associated with heat tolerance in Persian Gulf populations of P. daedalea reinforcing the importance of these markers for heat tolerance. These results illustrate the importance of high heritability and the complexity of the genomic architecture underpinning host heat tolerance. These findings suggest that this P. daedalea population has the genetic prerequisites for adaptation to increasing temperatures. This study also provides knowledge for the development of high throughput genomic tools to screen for variation within and across populations to enhance adaptation through assisted gene flow and assisted migration.

evolutionary biology↗

Global gene expression patterns in response to white patch syndrome: Disentangling symbiont loss from the thermal stress response in reef-building coral

The mechanisms resulting in the breakdown of the coral symbiosis once the process of bleaching has been initiated remain unclear. Distinguishing symbiont loss from the abiotic stress response may shed light on the cellular and molecular pathways involved in each process. This study examined physiological changes and global gene expression patterns associated with white patch syndrome (WPS) in P. lobata, which manifests in localized bleaching independent of thermal stress. In addition, a meta-analysis of global gene expression studies in other corals and anemones was used to contrast differential regulation as a result of abiotic stress from expression patterns correlated with symbiotic state. Symbiont density, chlorophyll a content, holobiont productivity, instant calcification rate, and total host protein content were uniformly reduced in WPS relative to healthy tissue. While expression patterns associated with WPS were secondary to fixed effects of source colony, specific functional enrichments suggest that the viral infection putatively giving rise to this condition affects symbiont rather than host cells. The meta-analysis revealed that expression patterns in WPS-affected tissues were significantly correlated with prior studies examining short-term thermal stress responses. This correlation was independent of symbiotic state, as the strongest correlations were found between WPS adults and both symbiotic adult and aposymbiotic coral larvae experiencing thermal stress, suggesting that the majority of expression changes reflect a non-specific stress response. Across studies, the magnitude and direction of expression change among particular functional enrichments suggests unique responses to stressor duration, and highlights unique responses to bleaching in an anemone model which engages in a non-obligate symbiosis.

ecology↗

Population genetics of the coral Acropora millepora: Towards a genomic predictor of bleaching

Although reef-building corals are rapidly declining worldwide, responses to bleaching vary both within and among species. Because these inter-individual differences are partly heritable, they should in principle be predictable from genomic data. Towards that goal, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We then obtained whole genome sequences for 237 phenotyped samples collected at 12 reefs distributed along the Great Barrier Reef, among which we inferred very little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We further used 213 of the samples to conduct a genome-wide association study of visual bleaching score, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for the use of genomics-based approaches in conservation strategies.

evolutionary biology↗

Positive genetic associations among fitness traits support evolvability of a reef-building coral under multiple stressors

Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for synergistic interactions among stressors and the genetic variance and covariance among fitness-related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef-building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were tradeoffs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive co-variances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals adaptive capacity when predicting the future of coral reefs.

evolutionary biology↗

Symbiont community diversity is more constrained in holobionts that tolerate diverse stressors

Coral reefs are experiencing global declines as climate change and other stressors cause environmental conditions to exceed the physiological tolerances of host organisms and their microbial symbionts (collectively termed the holobiont). To assess the role of symbiont community composition in holobiont stress tolerance, diversity metrics and abundances of obligate dinoflagellate endosymbionts (Family: Symbiodiniaceae) were quantified from eight Acropora millepora coral colonies (hereafter called genets) that thrived under or responded poorly to various stressors. Four best performer coral genets were selected for analysis because they survived 10 days of high temperature, high pCO2, bacterial addition, or combined stressors, whereas four worst performer coral genets were analyzed because they experienced significant mortality under these stressors. At the end of the experimental period, seven of eight coral genets mainly hosted Cladocopium symbionts, but also contained Brevolium, Durusdinium, and/or Gerakladinium symbionts at lower abundances (<0.1% of the total community). After 10 days of stress, symbiont communities varied significantly among host genets, but not stress treatments, based on alpha and beta diversity metrics. A generalized joint attribute model (GJAM) also predicted that symbiont communities were primarily sensitive to host genet at regional scales. Indicator species analysis and the regional GJAM model identified significant associations among particular symbionts and host genet performance. Specifically, Cladocopium 3k contributed to the success of best performer host genets under various stressful conditions, whereas Durusdinium glynnii and Durusdinium trenchii were significantly associated with one worst performer genet. Cladocopium 3k dominance should be more broadly investigated as a potential predictor of stress resistance in Acropora millepora populations across their geographic range. Symbiodiniaceae communities exhibited higher richness and variance (beta diversity) in the worst performing genets. These findings highlight that symbiont community diversity metrics may be important indicators of resilience in hosts central to diverse disciplines, from agriculture to medicine.

ecology↗

Patterns of gene body methylation predict coral fitness in new environments

Despite widespread taxonomic representation, the function of gene body methylation (GBM) remains uncertain. One hypothesis is that GBM mediates phenotypic plasticity. To investigate this hypothesis, we performed whole-genome methylation and transcriptome profiling on reciprocally transplanted colony fragments of the reef-building coral Acropora millepora. GBM was only slightly affected by transplantation but these small changes correlated with coral fitness in the new environment. Specifically, for transplanted corals, similarity in GBM patterns to native corals positively correlated with growth rate, as well as carbohydrate, protein, lipid and endosymbiont content. Between populations, elevated GBM positively correlated with transcription, supporting previous findings that GBM is associated with stable and active transcription. Contrary to expectations however, changes in transcription as a result of transplantation did not correlate with changes in GBM and did not predict fitness. This indicates that on physiological time scales GBM is not directly coupled to transcription, leaving open the question about the mechanism linking GBM to fitness during acclimatization.

ecology↗

Adaptive pathways of coral populations on the Great Barrier Reef

Can genetic adaptation in reef-building corals keep pace with the current rate of sea surface warming? Here we combine population genomic, biophysical modeling, and evolutionary simulations to predict future adaptation of the common coral Acropora millepora on the Great Barrier Reef. Loss of coral cover in recent decades did not yet have detectable effect on genetic diversity in our species. Genomic analysis of migration patterns closely matched the biophysical model of larval dispersal in favoring the spread of existing heat-tolerant alleles from lower to higher latitudes. Given these conditions we find that standing genetic variation could be sufficient to fuel rapid adaptation of A. millepora to warming for the next 100-200 years, although random thermal anomalies would drive increasingly severe mortality episodes. However, this adaptation will inevitably cease unless the warming is slowed down, since no realistic mutation rate could replenish adaptive genetic variation fast enough.

evolutionary biology↗