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Muller, E. M.

Publications and source records attributed to Muller, E. M..

9 recordsLinked to original sources

Limited neutral and adaptive genomic divergence suggests Acropora cervicornis can be managed as a single conservation unit across its range

Genomic signatures can provide key insight into the evolutionary history and remaining adaptive potential of threatened populations. As demographic decline erodes both diversity and the processes maintaining it, understanding how remaining variation is distributed becomes increasingly important for conserving species like the staghorn coral, Acropora cervicornis, a foundational but critically endangered Caribbean reef-builder. We analyzed 46 high-coverage A. cervicornis genomes from 10 locations across the tropical western Atlantic to evaluate neutral and adaptive structure, genomic diversity, demographic history, inbreeding, and connectivity, and generated a regional haplotype reference panel for future genomic monitoring. Genome-wide analyses recovered recurring regional substructure, but differentiation was modest and partly explained by isolation-by-distance and spatial variation in effective migration. Subpopulations had similar levels of genomic diversity, shared demographic history, and limited evidence of local adaptation. These patterns support interpreting sampled Caribbean populations as a single evolutionarily significant unit (ESU) containing multiple regional management units (MUs), rather than as deeply divergent evolutionary lineages. Despite substantial retained variation and low current inbreeding, estimated contemporary effective population size was small, suggesting an increased vulnerability to the effects of drift as demographic collapse continues, especially if structure is reinforced by isolated management. Together, our findings emphasize the urgent need for interventions that preserve and enhance genomic diversity, including risk-managed assisted gene flow. Supported by the haplotype reference panel developed here, these strategies will require coordinated efforts across regional entities to conserve and restore A. cervicornis as a jointly managed, single ESU.

genomics↗

Genomic variation associated with endosymbiont shuffling and areal growth in the endangered elkhorn coral, Acropora palmata

Biodiversity losses continue to outpace traditional management, underscoring the need to understand adaptive capacity and the potential for interventions to increase fitness under climate change. We undertook a genome-wide association study on 156 Acropora palmata genets to investigate the genomic basis of areal growth, endosymbiont association, and thermal tolerance. Seven peaks on chromosomes 1, 3 and 14 were associated with endosymbiont shuffling and two peaks on chromosome 4 were associated with areal growth. As variants were located in non-coding regions we incorporated additional data from an independent field-transplant experiment to investigate their relationship with patterns of gene expression. Intersection of these datasets implicated melanocortin-like receptor activity and Ran GTPase activating protein 1 in endosymbiont composition and surface area growth, respectively. Results indicate that growth and endosymbiont associations may represent more viable intervention targets than temperature tolerance and highlight the need to better understand the role of non-coding variation in basic biology and development of restoration interventions.

genomics↗

High relatedness in sexually produced restoration cohorts of the endangered elkhorn coral, Acropora palmata

Climate change is driving the decline of coral populations around the world such that many are unlikely to recover without human intervention. Assisted sexual reproduction is one intervention proposed to enhance genetic diversity and support population recovery, yet its genetic outcomes remain poorly quantified. We evaluated genome-wide relatedness and genetic diversity in 168 restoration genets of the endangered Caribbean coral Acropora palmata, including 153 sexually produced offspring derived from multi-parent batch and biparental crosses. We detected high relatedness within multi-parent batch cross cohorts, with many genets comprising only one or a few full-sibling groups, indicating highly unequal parental contributions. Nucleotide diversity was lower in one batch cross cohort relative to founder populations, but the absolute difference was small and runs of homozygosity were relatively short indicating that inbreeding depression is not yet a concern. These patterns suggest that common larval propagation approaches can successfully generate large numbers of new genets but underscore the need to manage inbreeding risk, especially in small breeding stocks such as the Caribbean Acropora spp. Specifically, our results highlight the need for comprehensive genetic management to integrate assisted sexual reproduction into coral restoration, including parentage tracking, broodstock rotation, and relatedness-informed outplanting designs.

genomics↗

A dominant coral parasite, Candidatus Aquirickettsia rohweri, resists antibiotic exposure and thermal challenge below the bleaching threshold in disease-susceptible Acropora cervicornis

The critically endangered Caribbean staghorn coral Acropora cervicornis hosts microbiomes frequently dominated by the putatively parasitic intracellular bacterium Candidatus Aquirickettsia rohweri, which is associated with reduced coral growth and heightened disease susceptibility. Whether this dominance can be disrupted through antibiotic treatment and a sequential disturbance of thermal stress, remains unknown. In this study, we exposed disease-susceptible A. cervicornis fragments to broad-spectrum antibiotics, sub-bleaching thermal stress, or the combination of an antibiotic pre-treatment followed by thermal stress, and tracked changes in microbiome composition and diversity across all experimental phases using 16S rRNA amplicon sequencing and quantitative PCR (qPCR). We find that while the minor microbial fraction exhibits sustained compositional shifts in response to treatment, Ca. Aquirickettsia rohweri is resilient to antibiotic and thermal perturbation and may in fact increase in abundance following antibiotic exposure, suggesting that its dominance is actively maintained and not readily displaced by current disease mitigation strategies.These results indicate that antibiotic intervention is unlikely to be a viable strategy for disrupting Ca. A. rohweri dominance in disease-susceptible A. cervicornis, underscoring the urgency of understanding its transmission routes to inform microbiome rescue efforts.

microbiology↗

Morphological plasticity in a reef-building coral is context-dependent and trades off with resistance to thermal stress

In sessile, long-lived organisms, such as reef-building corals, phenotypic plasticity may play a key role in mitigating the impacts of climate change. Plasticity is often context-dependent and has costs and limits, ultimately resulting in adaptive, neutral, or maladaptive effects. However, our understanding of the mechanisms that maintain variation in, and therefore drive the evolution of, plasticity is still limited. We use a field-based transplant experiment to show context-dependent tradeoffs to morphological plasticity in Acropora cervicornis under real-world conditions driven by climate change. We find that while morphological plasticity is neutral under some conditions, it trades off with thermal tolerance during moderate temperature stress during a marine heatwave. Additionally, we find that plasticity changes over time, underlining the importance of its temporal dynamics in long-lived organisms. Our results demonstrate a key role for environmental change in the eco-evolutionary dynamics of plasticity by demonstrating context-dependent costs under real-world thermal stress.

evolutionary biology↗

A quick and reliable menthol-induced bleaching protocol for the Caribbean staghorn coral, Acropora cervicornis

Corals and dinoflagellate algae form a unique mutualistic symbiosis that provides the energetic and structural foundation for shallow coral reef ecosystems. Despite the long success of this partnership in oligotrophic seas, coral reefs are in decline due to increasing threats from rising seawater temperatures and disease, both of which can lead to bleaching and mortality. In order to better understand the mechanisms that underpin this mutualism, it may be necessary to dismantle the coral-algal symbiosis. Previous studies have experimentally bleached corals using thermal stress, photosynthetic inhibitors (DCMU), and menthol. We compared lab-induced bleaching of staghorn coral Acropora cervicornis by menthol treatment to traditional thermal stress. The larger aim was to adapt existing bleaching protocols to this important coral species used in restoration as a guide for future studies. Bleaching in corals treated with menthol or exposed to elevated temperature stress (31{degrees}C) was monitored by measuring photosynthetic activity determined by Fv/Fm using pulse-amplitude modulated (PAM) fluorescence. Corals were also monitored for symbiont density and overall health using the CoralWatch Coral Health Chart card throughout the experiment. We found that A. cervicornis bleached in response to both menthol treatment and thermal stress, but menthol treatment was more effective at reducing algal symbiont photosynthetic capacity (Fv/Fm) without negatively affecting the health of the coral. Our results indicate that menthol treatment at 0.38 mM rendered staghorn coral aposymbiotic within fourteen days without any visual or physiological damage to the coral. This study provides a simple and effective menthol-bleaching treatment protocol for future studies on staghorn coral.

physiology↗

Assisted gene flow yields Acropora palmata corals with robust physiological performance under warmer water temperatures in a land-based nursery

Assisted gene flow (AGF) is a conservation approach that facilitates the spread of alleles and may accelerate the recovery of genetically depauperate cohorts. The threatened Caribbean coral Acropora palmata is approaching regional extinction within the western Atlantic partly due to increasing water temperatures associated with global climate change. Previously, AGF was conducted by crossing gametes collected from three regions (Curacao - CU, Florida - FL, and Puerto Rico - PR) characterized by contrasting temperature regimes and low gene flow between them. Here, we tested the thermal tolerance of these AGF cohorts in comparison to purebred Florida and Curacao cohorts. Exposure to high temperatures resulted in few physiological changes, likely because the corals hosted the thermally tolerant algal symbiont, Durusdinium trenchii. However, the FL x FL cohort was the most sensitive to the high temperatures with a significant reduction in net photosynthesis and maximum electron transport rate under this treatment. Like the phenotypic responses, gene expression changes in response to heat stress were muted overall. Consequently, there was little power to detect correlations between genotype and phenotype. Relative to mid-parent values, CUxFL AGF cohorts showed 26 overexpressed and 48 underexpressed genes. Differentially expressed genes included known stress responders. Importantly, hybrid crosses harbored 879 private alleles that were previously not recovered in representative genets from Florida and thus carry important conservation value. These findings suggest that AGF corals not only carry novel alleles but also represent novel gene expression patterns.

ecology↗

Nutrient enrichment alters gene expression in 'Ca.' Aquarickettsia rohweri, promoting parasite expansion and horizontal transmission

Ocean warming, disease, and pollution contributed to global declines in coral abundances and diversity. In the Caribbean, corals previously dominated reefs, providing an architectural framework for diverse ecological habitats, but have significantly declined due to infectious microbial disease. Key species like coral Acropora cervicornis, are now considered critically endangered, prompting researchers to focus on scientific endeavors to identify factors that influence coral disease resistance and resilience. We previously showed that disease susceptibility, growth rates, and bleaching risk were all associated with the abundance of a single bacterial parasite, Ca. Aquarickettsia rohweri which proliferates in vivo under nutrient enrichment. Yet how nutrients influence parasite physiology and life history strategies within its host are unknown. We performed microscopy and transcriptomic analyses of Ca. A. rohweri populations during a 6-week nutrient exposure experiment. Microscopy showed that this parasite was abundant in coral tissue and densely packed in mucocytes prior to nutrient enrichment. Ca. A. rohweri energy scavenging genes and those potentially involved in this habitat transition are significantly upregulated during enrichment. Specifically, transcripts involved in signaling, virulence, two-component systems, and nutrient import genes are elevated under higher nutrients. These data support the predicted role of Ca. A. rohweri as a highly active nutrient-responsive A. cervicornis parasite, and provide a glimpse at the mechanism of induced disease susceptibility while implicating nutrient exposure in its horizontal transmission. SignificanceThe coral disease crisis has contributed to global declines in coral abundance and diversity and is exacerbated by environmental stressors like eutrophication. Thus, identifying factors that influence coral disease resistance and resilience is a top priority. The Rickettsiales-like bacterium, Candidatus Aquarickettsia rohweri is ubiquitous coral symbiont that is strongly linked to coral disease susceptibility in staghorn coral, and is undergoing positive selection across the Caribbean. Although Ca. A. rohweri is a putative parasite, little is known about the activity of this bacterium in coral tissue. This work supports the role of Ca. A. rohweri as a highly active, nutrient-responsive parasite and proposes a mechanism for how Ca. A. rohweri contributes to coral disease susceptibility, parasite expansion, and horizontal transmission.

microbiology↗

A meta-analysis of the stony coral tissue loss disease microbiome finds key bacteria in lesions and unaffected tissue of diseased colonies

Stony coral tissue loss disease (SCTLD) has been causing significant whole colony mortality on reefs in Florida and the Caribbean. The cause of SCTLD remains unknown, with limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of SSU 16S ribosomal RNA gene datasets generated by 16 field and laboratory SCTLD studies to find consistent bacteria associated with SCTLD across disease zones (vulnerable, endemic, and epidemic), coral species, coral compartments (mucus, tissue, and skeleton), and disease states (apparently healthy colony tissue [AH], and unaffected [DU] and lesion [DL] tissue from diseased colonies). We also evaluated bacteria in seawater and sediment, which may be sources of SCTLD transmission. Although AH colonies in endemic and epidemic zones harbor bacteria associated with SCTLD lesions, and aquaria and field samples had distinct microbial compositions, there were still clear differences in the microbial composition among AH, DU, and DL in the combined dataset. Alpha diversity between AH and DL was not different; however, DU showed increased alpha diversity compared to AH, indicating that, prior to lesion formation, corals may undergo a disturbance to the microbiome. This disturbance may be driven by Flavobacteriales, which were especially enriched in DU. While Rhodobacterales and Peptostreptococcales-Tissierellales were prominent in structuring microbial interactions in DL. Peptostreptococcales-Tissierellales specifically may contribute to lesion progression through an alpha-toxin. We provide a consensus of SCTLD-associated bacteria both prior to and during lesion progression and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.

microbiology↗