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Cunning, R.

Publications and source records attributed to Cunning, R..

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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↗

Reproductive Trade-offs in Caribbean Corals: Plasticity Accelerates While Fragmentation Delays Reproductive Capacity

In modular organisms, where growth and fragmentation blur the boundaries between individuals, the interplay between asexual and sexual reproduction creates complex fitness trade-offs. Life-history theory predicts that resources allocated to one fitness component necessarily reduce investment in others, yet detecting these trade-offs in wild populations of clonal organisms remains challenging. Phenotypic plasticity can enhance survival, yet its influence on reproductive capacity and life history trade-offs remains poorly understood. Using a fully crossed reciprocal transplant design, we tracked 263 colonies of the branching coral Acropora cervicornis across nine reef sites over 42 months, investigating relationships between fragmentation, morphological plasticity, and the capacity for sexual reproduction. Breakage patterns reflected both environmental and genetic factors. Primary branch breaks created a "double negative" effect--simultaneously more than doubling mortality risk and delaying attainment of a validated reproductive size class by [~]40%. Conversely, higher morphological plasticity in surface area-to-volume ratio accelerated sexual maturation up to 6-fold, counteracting the negative effects of fragmentation. In parallel, a simple demographic model parameterized with published fecundity data estimated that primary breakage reduces expected cumulative reproductive output by [~]58%, a result robust across a wide range of parameter assumptions. These results demonstrate a fundamental reproductive trade-off in which asexual reproduction through fragmentation undermines sexual reproductive potential by reducing colony size. Moreover, our findings reveal that fragmentation susceptibility is broadly heritable and subject to selection, and identify a compensatory mechanism through which plasticity enhances fitness beyond immediate survival.

evolutionary biology↗

Epigenetic Intelligence: How Organisms Track Their Environment Through Molecular Memory

The regulation of gene expression by epigenetic markers is a growing area of focus for researchers who seek to explain rapid phenotypic acclimatization to environmental change. Yet even as empirical datasets accumulate exponentially, the mechanistic underpinnings of epigenetic changes and their role in connecting environmental variation with the regulation of gene function remain unclear. Here, we use a stochastic model of epigenetic change to generate three testable predictions: (1) that organisms require environmental feedback to track their environments through epigenetic responses, (2) that this tracking requires coordination between the addition and removal of epigenetic markers, and (3) that epigenetically driven tracking is only effective under specific subsets of environmental variability. Despite the intuitiveness of these postulates, few to no experimental studies directly test them. We review correlational evidence consistent with the models predictions, describe hypothetical mechanisms by which epigenetic strategies could evolve, and clearly identify knowledge gaps and urgent experimental needs in the field. Overall, the field of environmental epigenetics is poised for major advances, which can be enhanced through the continued synthesis of mathematical frameworks and empirical data.

genetics↗

Seasonal plasticity of symbiotic strategies clarifies coral holobiont resistance and resilience

As coral reefs face unprecedented declines driven by thermal stress and the breakdown of coral symbiosis (i.e., coral bleaching), restoration efforts increasingly rely on coral health and resilience rankings. However, seasonal plasticity in symbiosis and holobiont metabolism, along with the presence of cryptic species, can complicate data interpretation. Therefore, quantifying seasonal plasticity in coral physiology and incorporating genetic identification are essential for accurately interpreting and drawing conclusions from trait-based and fitness-based analyses. To test the effect of seasonal and site variation on physiological plasticity we sampled three ecologically dominant genera, Acropora, Pocillopora, and Porites across three lagoon sites (n=15 tagged colonies genus-1 site-1) on the north shore of Moorea French Polynesia in January, March, September, and December of 2020. We identified coral host and intracellular symbiotic Symbiodiniaceae to the highest taxonomic resolution possible and quantified 13 physiological variables within the holobiont. Genetic analyses identified A. pulchra along with cryptic lineages in Pocillopora (P. meandrina, P. tuahiniensis) and Porites (P. evermanni, P. lobata/lutea). A. pulchra was dominated by Durusdinium trenchii and also contained Symbiodinium microadriaticum. Symbiont communities differed between cryptic congeners, with P. meandrina hosting Cladocopium latusorum and P. tuahiniensis hosting Cladocopium pacificum, whereas P. evermanni and P. lobata/lutea both hosted Cladocopium (C15), but each with unique C15 profiles. Weedy taxa such as Acropora and Pocillopora displayed a cycle of symbiont boom and bust in response to seasonally variable light and temperature, likely contributing to the high stress sensitivity of these taxa. In contrast, despite seasonal environmental variability, Porites displayed greater symbiont stability, with temperature--rather than light--serving as the stronger explanatory variable of seasonal variation in host physiology. Increased host biomass under cooler conditions, which provides energy reserves, may serve as an important stabilizing factor in massive Porites well-documented stress resilience. Collectively, our data provide essential evidence of the need for integrative analyses considering baseline physiological states across seasons along with host and symbiont genetics, particularly in light of the plethora of climate change related stress test assays taking place throughout the year across coral taxa with cryptic lineages.

physiology↗

Genome assembly and annotation of Acropora pulchra from Mo'orea French Polynesia

Reef-building corals are integral ecosystem engineers in tropical coral reefs worldwide but are increasingly threatened by climate change and rising ocean temperatures. Consequently, there is an urgency to identify genetic, epigenetic, and environmental factors, and how they interact, for species acclimatization and adaptation. The availability of genomic resources is essential for understanding the biology of these organisms and informing future research needs for management and and conservation. The highly diverse coral genus Acropora boasts the largest number of high-quality coral genomes, but these remain limited to a few geographic regions and highly studied species. Here we present the assembly and annotation of the genome and DNA methylome of Acropora pulchra from Moorea, French Polynesia. The genome assembly was created from a combination of long-read PacBio HiFi data, from which DNA methylation data were also called and quantified, and additional Illumina RNASeq data for ab initio gene predictions. The work presented here resulted in the most complete Acropora genome to date, with a BUSCO completeness of 96.7% metazoan genes. The assembly size is 518 Mbp, with 174 scaffolds, and a scaffold N50 of 17 Mbp. Structural and functional annotation resulted in the prediction of a total of 40,518 protein-coding genes, and 16.74% of the genome in repeats. DNA methylation in the CpG context was 14.6% and predominantly found in flanking and gene body regions (61.7%). This reference assembly of the A. pulchra genome and DNA methylome will provide the capacity for further mechanistic studies of a common coastal coral in French Polynesia of great relevance for restoration and improve our capacity for comparative genomics in Acropora and cnidarians more broadly.

genomics↗

Marine heatwaves threaten cryptic coral diversity and erode associations amongst coevolving partners

Climate change-amplified heatwaves are known to drive extensive mortality in marine foundation species. However, a paucity of longitudinal genomic datasets has impeded understanding of how these rapid selection events alter species genetic structure. Impacts of these events may be exacerbated in species with obligate symbioses, where the genetics of multiple co-evolving species may be affected. Here, we tracked the symbiotic associations and fate of reef-building corals for six years through a prolonged heatwave. Coral genetics strongly predicted survival of the common coral Porites through the event, with strong differential survival (15 to 64%) apparent across morphologically identical -but genetically distinct- lineages. The event also disrupted strong associations between coral lineages and their symbiotic partners, homogenizing symbiotic assemblages across lineages and reducing the specificity of coral-algal symbioses. These results highlight that marine heatwaves threaten cryptic genetic diversity of foundation species and have the potential to decouple tight relationships between co-evolving host-symbiont pairs.

ecology↗

Cophylogeny and specificity between cryptic coral species (Pocillopora spp.) at Moorea and their symbionts (Symbiodiniaceae)

The congruence between phylogenies of tightly associated groups of organisms (cophylogeny) reflects evolutionary links between ecologically important interactions. However, despite being a classic example of an obligate symbiosis, tests of cophylogeny between scleractinian corals and their photosynthetic algal symbionts have been hampered in the past because both corals and algae contain genetically unresolved and morphologically cryptic species. Here, we studied co-occurring, cryptic Pocillopora species from Moorea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the host Pocillopora (using genomic loci, complete mitochondrial genomes, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbAncr markers) and tested for cophylogeny. The analysis supported the presence of five Pocillopora species on the fore-reef at Moorea that mostly hosted either Cladocopium latusorum or C. pacificum. Only Pocillopora species hosting C. latusorum, and that have similar relative abundances across depths, also hosted taxa from Symbiodinium and Durusdinium. In general, the Cladocopium phylogeny mirrored the Pocillopora phylogeny. Within Cladocopium species, lineages also differed in their associations with Pocillopora haplotypes, except those showing evidence of nuclear introgression, and with depth in the two most common Pocillopora species. We also found evidence for a new Pocillopora species (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of these Pocillopora and Cladocopium species and lineages suggest that symbiont speciation is driven by niche diversification in the host, but there is still evidence for symbiont flexibility in rare cases.

evolutionary biology↗

A Dynamic Bioenergetic Model For Coral-Symbiodinium Symbioses And Coral Bleaching As An Alternate Stable State

Coral reef ecosystems owe their ecological success-and vulnerability to climate change-to the symbiotic metabolism of corals and Symbiodinium spp. The urgency to understand and predict the stability and breakdown of these symbioses (i.e., coral bleaching) demands the development and application of theoretical tools. Here, we develop a dynamic bioenergetic model of coral-Symbiodinium symbioses that demonstrates realistic steady-state patterns in coral growth and symbiont abundance across gradients of light, nutrients, and feeding. Furthermore, by including a mechanistic treatment of photo-oxidative stress, the model displays dynamics of bleaching and recovery that can be explained as transitions between alternate stable states. These dynamics reveal that healthy and bleached states correspond broadly to nitrogen- and carbon-limitation in the system, with transitions between them occurring as integrated responses to multiple environmental factors. Indeed, a suite of complex emergent behaviors reproduced by the model (e.g., bleaching is exacerbated by nutrients and attenuated by feeding) suggests it captures many important attributes of the system; meanwhile, its modular framework and open source R code are designed to facilitate further problem-specific development. We see significant potential for this modeling framework to generate testable hypotheses and predict integrated, mechanistic responses of corals to environmental change, with important implications for understanding the performance and maintenance of symbiotic systems.

systems biology↗