Carly B. Scott

Flexibility in the coral-algal symbiosis has been proposed as a mechanism by which coral colonies may acclimatize to shifting environmental conditions, yet the rules governing when and why switching occurs remain unresolved. Here, I compile longitudinal data spanning 59 coral species, 26 years, and 95 globally distributed reefs to estimate switching probability at the colony-level across directional environmental change and thermal variability. Switching was neither universal nor random: the identity of the resident symbiont was the strongest predictor of switching, with Cladocopium -dominated and mixed communities showing the greatest flexibility. Transition probabilities were asymmetrical, with shifts toward Durusdinium consistently more probable than shifts away, regardless of starting genus. Among host species- level effects, morphological traits best explained switching propensity along changing environmental conditions, while both traits and phylogenetic history explained sensitivity to thermal variability, suggesting that these two dimensions of abiotic environments impose distinct selective pressures on the symbiosis. Most switching was ultimately transient; colonies had a 78% chance of reverting back to their original symbiont in the following year. Together, these results challenge the assumption that increased environmental variability and rising temperatures universally correlate with higher switching rates, and suggest instead that host traits, phylogeny, and resident symbiont identity may help identify the subset of taxa for which flexibility represents a viable acclimatization strategy under climate stress.

Forecasting disease epidemics may require considering both abiotic and biotic conditions. Abiotic conditions can influence pathogen dispersal, survival, and infection, while prior infection by one pathogen species can alter host susceptibility to subsequent pathogens, creating historical contingencies. Yet, the relative importance of environmental conditions, within-host pathogen interactions, and their potential interplay in predicting seasonal disease dynamics remain underexplored. To better understand these interactions and improve ecological forecasts of disease risk, we analyzed more than 41,000 plant-level observations of three foliar fungal diseases on the grass species tall fescue in North Carolina, collected from 2017–2024. We built temporally explicit random forest models which for two of the three focal diseases accurately (>80%) predicted future disease dynamics from a complex abiotic and biotic predictor space. From these models, we identified key environmental thresholds that intensified annual epidemics. We then supplemented those machine-learning models with Bayesian hierarchical models and survival analyses, finding that pathogen-pathogen interactions can be as important as environmental conditions in predicting disease risk. Furthermore, for two of the three focal diseases, prior infection by a different pathogen facilitated the subsequent infection and the strength of this facilitation was modulated by environmental context. From this study we draw two major conclusions, one ecological and one methodological. First, knowledge of a host’s current disease state may be as important as local environmental conditions for predicting disease dynamics. Second, by integrating complementary modeling approaches, we can develop both predictive forecasts and mechanistic insight into the biotic and abiotic drivers of infectious disease. Open Research Statement: All data and code used to generate the results contained in this paper are available on GitHub ( https://github.com/cb-scott/WidenerLongTermAnalysis ). Upon publication the final version of all scripts and datafiles will be archived on Zenodo with a permanent DOI.

The coral microbiome is a critical component of coral health and resilience, yet it is unclear what factors drive coral microbiome composition, especially within the context of coral bleaching. Here, we use whole genome sequencing data combined with a machine learning approach (RDAforest) to assess predictors of the microbiome in 208 colonies of Acropora millepora from 12 reef sites in the Central Great Barrier Reef during a 2016 bleaching event. We characterized microbiome variation using k-mers. While some environmental variables, such as chlorophyll seasonal range and maximum degree heating weeks, were associated with microbiome composition, we find that host genetics and dominant photosymbionts were more powerful predictors. In contrast, bleaching score had negligible predictive power. The coral’s microbiome therefore correlates with dominant photosymbiont identity even during a bleaching event. The association of the microbiome with the environment suggests that the coral microbiome can serve as a proxy for environmental variation when environment cannot be measured directly, which may be especially useful in ancient DNA studies.

The fate of coral reefs in response to climate change depends on their ability to adapt to new environments. The coral animal is buffered from environmental stress by its algal endosymbionts and microbial partners (together, the “holobiont”). However, the flexibility of holobiont community assembly is not well understood, making it difficult to estimate its contribution to coral adaptation. To clarify these processes, we genetically profiled holobiont components (coral, algal symbiont, and microbiome) of massive Porites sampled across two size classes (small, < 30 cm and large, > 2 m) and ecologically distinct reef sites near Orpheus and Pelorus Islands, Australia. We recovered five major genetic clusters in the coral host. We estimated the relative contributions of the host genetic structure, site, and size class to holobiont community composition. Host genetic structure was the primary driver of both Symbiodiniaceae and microbial communities, indicating strong holobiont specificity in genetic clusters. In addition, the microbial community was associated with reef site and size class, unlike Symbiodiniaceae that were not significantly affected by either factor. As environmentally segregated, cryptic genetic lineages emerge as a common feature of scleractinian corals, these results emphasize that failure to assess cryptic genetic structure of the coral host may lead to dramatic overestimation of holobiont flexibility.

Understanding the stability of microbial community assembly on coral reefs is crucial for determining their response to changing environments. Here, we evaluate how the marine sediment, water column, and mountainous star coral ( Orbicella faveolata ) metagenomic communities shift over temporal, spatial, and genetic gradients, centered on the annual coral spawning event on St. Croix, USVI. Using low-coverage shotgun sequencing and a reference-free approach, we characterized metagenomic communities and additionally report 15 metagenome-assembled genomes from environmental samples. We show that diel time can be as important as kilometer-scale distance in structuring the coral-associated and marine sediment community structure, albeit with other highly local factors (genotype, within-reef location) driving most variation. Through multivariate machine learning methods, we find several taxa and metabolic pathways enriched over time, where broad metagenomic community shifts may be linked with concurrent temperature increase or the annual coral spawning event. As understanding the coral microbiome in the context of its environment becomes increasingly important, our research underscores the importance of small-scale variation, both spatially and temporally, in structuring coral reef metagenomic communities.

Sex-differential selection (SDS), which occurs when the fitness effects of alleles differ between males and females, can have profound impacts on the maintenance of genetic variation, disease risk, and other key aspects of natural populations. Because the sexes mix their autosomal genomes each generation, quantifying SDS is not possible using conventional population genetic approaches. Here, we introduce a method that exploits subtle sex differences in haplotype frequencies resulting from SDS acting in the current generation. Using data from 300K individuals in the UK Biobank, we estimate the strength of SDS throughout the genome. While only a handful of loci under SDS are individually significant, we uncover highly polygenic signals of genome-wide SDS for both viability and fecundity. Selection coefficients of s = 10 - 3 may be typical. Despite its ubiquity, SDS may impose a mortality load of less than 1%. An interesting life-history tradeoff emerges: Alleles that increase viability more strongly in females than males tend to increase fecundity more strongly in males than in females. Finally, we find marginal evidence of SDS on fecundity acting on alleles affecting arm fat-free mass. Taken together, our findings connect the long-standing evidence of SDS acting on human phenotypes with its impact on the genome.

Sex-differential selection (SDS), which occurs when the fitness effects of alleles differ between males and females, can have profound impacts on the maintenance of genetic variation, disease risk, and other key aspects of natural populations. Because the sexes mix their autosomal genomes each generation, quantifying SDS is not possible using conventional population genetic approaches. Here, we introduce a novel method that exploits subtle sex differences in haplotype frequencies resulting from SDS acting in the current generation. Using data from 300K individuals in the UK Biobank, we estimate the strength of SDS throughout the genome. While only a handful of loci under SDS are individually significant, we uncover polygenic signals of genome-wide SDS for both viability and fecundity. An interesting life-history tradeoff emerges: alleles that increase viability more in one sex increase fecundity more in the other sex. Lastly, we find evidence of SDS on fecundity acting on alleles affecting arm fat-free mass. Taken together, our findings connect the long-standing evidence of SDS acting on human phenotypes with its impact on the genome. Significance statement Selection often acts differently on females and males, as evidenced by the striking sexual dimorphism found in many taxa. As a result, alleles can have different fitness effects in each sex. Consequences can include higher levels of genetic variation and higher disease burdens in populations. This study introduces a novel method to quantify this sex-differential selection (SDS) and reveals that it acts throughout the human genome. We discovered a life history tradeoff between survival and fecundity in females and males and that SDS on fecundity acts on alleles affecting arm fat-free mass.

Coral bleaching, the stress‐induced breakdown of coral‐algal symbiosis, threatens reefs globally. Paradoxically, despite adverse fitness effects, corals bleach annually, even outside of abnormal temperatures. This generally occurs shortly after the once‐per‐year mass coral spawning. Here, we propose a hypothesis linking annual coral bleaching and the transmission of symbionts to the next generation of coral hosts. We developed a dynamic model with two symbiont growth strategies, and found that high sexual recruitment and low adult coral survivorship and growth favour bleaching susceptibility, while the reverse promotes bleaching resilience. Otherwise, unexplained trends in the Indo‐Pacific align with our hypothesis, where reefs and coral taxa exhibiting higher recruitment are more bleaching susceptible. The results from our model caution against interpreting potential shifts towards more bleaching‐resistant symbionts as evidence of climate adaptation—we predict such a shift could also occur in declining systems experiencing low recruitment rates, a common scenario on today's reefs.

For sessile organisms at high risk from climate change, phenotypic plasticity can be critical to rapid acclimation. Epigenetic markers like DNA methylation are hypothesized as mediators of plasticity; methylation is associated with the regulation of gene expression, can change in response to ecological cues, and is a proposed basis for the inheritance of acquired traits. Within reef-building corals, gene-body methylation (gbM) can change in response to ecological stressors. If coral DNA methylation is transmissible across generations, this could potentially facilitate rapid acclimation to environmental change. We investigated methylation heritability in Acropora, a stony reef-building coral. Two Acropora millepora and two Acropora selago adults were crossed, producing eight offspring crosses (four hybrid, two of each species). We used whole-genome bisulfite sequencing to identify methylated loci and allele-specific alignments to quantify per-locus inheritance. If methylation is heritable, differential methylation (DM) between the parents should equal DM between paired offspring alleles at a given locus. We found a mixture of heritable and nonheritable loci, with heritable portions ranging from 44% to 90% among crosses. gBM was more heritable than intergenic methylation, and most loci had a consistent degree of heritability between crosses (i.e. the deviation between parental and offspring DM were of similar magnitude and direction). Our results provide evidence that coral methylation can be inherited but that heritability is heterogenous throughout the genome. Future investigations into this heterogeneity and its phenotypic implications will be important to understanding the potential capability of intergenerational environmental acclimation in reef building corals.

The fate of coral reefs in response to climate change depends on their ability to adapt to new environments. The coral animal is buffered from environmental stress by its algal endosymbionts and microbial partners (together, the “holobiont”). However, the flexibility of holobiont community assembly in time and space is not well understood, making it difficult to estimate its contribution to coral adaptation. To clarify these processes at a centuries-long time scale, we compared the holobiont of massive Porites adults (>2m) to their juvenile (Porites compounded by cryptic genetic structure. Within the largest of these clusters, we additionally found significant genetic separation between adult and juvenile corals. Host genetic structure was the primary driver of both Symbiodiniaceae (84% of variance explained) and microbial (60% of variance explained) community composition, indicating strong holobiont specificity in cryptic lineages. The relative role of environment and age was over two-fold higher for the microbial community compared to the Symbiodiniaceae community. Our results indicate local environmental factors and time influence the microbial community at a meaningful scale, but genetics trumps all for the vertically-transmitted Symbiodiniaceae community.