Biology subjects

Putnam, H. M.

Publications and source records attributed to Putnam, H. M..

At least 19 recordsLinked to original sources

bioRxiv2026

Cross-talk among miRNAs, lncRNAs, and DNA methylation in three coral species reveal conserved epigenetic regulatory architecture

Epigenetic mechanisms support phenotypic plasticity across metazoans, enabling dynamic response to environmental change. DNA methylation and non-coding RNAs, including microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), regulate gene expression through distinct but interconnected mechanisms. In vertebrate systems, these layers form integrated networks in which specific miRNAs directly target the protein machinery of other epigenetic processes ("epi-miRNAs") and specialized lncRNAs act as competing endogenous RNAs (ceRNAs), sequestering miRNAs from their mRNA targets. Whether equivalent cross-layer regulatory architectures exist in cnidarians, whose methylomes are invertebrate-characteristic and whose miRNAs function mechanistically like those of plants, is unknown. Here we integrate matched RNA-seq, small RNA-seq, and whole-genome bisulfite sequencing across three species of reef-building coral (Acropora pulchra, Porites evermanni, and Pocillopora tuahiniensis) to characterize the landscape and regulatory interactions of microRNAs (miRNAs), long non-coding RNAs (lncRNAs) and DNA methylation, including the first description of epi-miRNAs and ceRNA networks in cnidarian taxa. Across the study species, miRNAs putatively targeted transcripts encoding a suite of epigenetic processes, including DNA methylation regulators (TET3, MBD, PRDM14), ubiquitin-signaling and histone-modifying machinery, and components of the miRNA pathway itself (e.g., AGO, TNRC6). The conserved miRNA miR-100 also exhibited species-divergent target coexpression, suggesting lineage-specific regulatory roles for deeply conserved miRNAs. Candidate ceRNA networks were also recovered, including predicted derepression of epimachinery transcripts, indicating that lncRNA-mediated buffering operates alongside direct miRNA control. Recovery of these regulatory interactions across three evolutionarily divergent species, despite few orthologous miRNA or lncRNA, suggests that multi-layered epigenetic regulation is a conserved feature of cnidarian biology. These results establish direct miRNA and lncRNA control of epigenetic machinery as an active component of coral gene regulation, and provide foundational resources for studying how multilayered epigenetic interactions contribute to coral resilience to environmental change. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=140 SRC="FIGDIR/small/739451v1_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@7e07dforg.highwire.dtl.DTLVardef@36cf0forg.highwire.dtl.DTLVardef@5406d3org.highwire.dtl.DTLVardef@8c09e3_HPS_FORMAT_FIGEXP M_FIG C_FIG

molecular biology↗

bioRxiv2026

Contrasting defensive strategies underlie differential susceptibility of corals to crown-of-thorns sea star (CoTS; Acanthaster cf. solaris) predation

Crown-of-thorns sea star (CoTS), Acanthaster cf. solaris, outbreaks are a major cause of hard coral cover decline across the west Pacific, threatening coral reefs. Coral taxa vary in susceptibility to CoTS predation from preferred (Acropora spp.) to non-preferred (Porites spp.), yet the mechanisms underlying these differences are poorly understood. We investigated coral defenses during an ongoing CoTS outbreak in Moorea, French Polynesia by examining gene expression (including putative toxin genes) in healthy and actively predated colonies of a preferred (Acropora hyacinthus) and a non-preferred (Porites sp.) coral prey species. During predation, A. hyacinthus exhibited molecular signatures of cellular stress responses involving oxidative stress signalling, inflammation, and tissue proteolysis. In contrast, Porites sp. showed enrichment of genes involved in mitochondrial metabolic adjustment and aerobic metabolism, suggesting metabolic compensation to maintain cellular function. Furthermore, A. hyacinthus demonstrated a reactive defense behaviour by differentially expressing toxins (e.g., kunitz-type neurotoxins) while Porites sp. employed constitutive expression of all putative toxins regardless of active predation, suggesting a proactive defense strategy. Together, these findings suggest that preferred and non-preferred coral prey exhibit fundamentally different molecular and defensive strategies during CoTS predation, shedding light on the evolutionary arms race between corals and their predators.

molecular biology↗

bioRxiv2026

A Genetic Method for Distinguishing Cryptic Pocillopora Species in French Polynesia without Sequencing

Pocillopora is a widespread, dominant reef-building coral genus in the Indo-Pacific that exhibits high morphological similarity and plasticity. Given this, genetic tools are needed to robustly identify Pocillopora individuals to the species level. Quick and accurate identification approaches for Pocillopora species are critical to estimating biodiversity patterns under current and future environmental challenges. In recent years, the mitochondrial open reading frame (mtORF) and a histone region (PocHistone) have been validated using genome-wide data to become the most widely used species-level markers for Pocillopora. However, Sanger sequencing of a large number of samples can be prohibitively expensive and sequencing facilities are not always readily available. Therefore, we present restriction fragment length polymorphism (RFLP) digests here that identify the six species of Pocillopora (P. acuta, P. cf. effusa, P. grandis, P. meandrina, P. tuahiniensis, and P. verrucosa) found in French Polynesia, without sequencing. In uninformed validation tests (in silico and in vitro), our protocol identified each Pocillopora species with 100% accuracy. Given their cost-effective, rapid nature, the tailoring of additional RFLP digest protocols to identify cryptic coral species in reef regions around the world will support foundational reef science, conservation and restoration initiatives.

molecular biology↗

bioRxiv2026

Spatially resolved gene expression analysis illuminates location-specific functions in the reef-building coral Pocillopora acuta

Reef-building coral polyps contain multiple specialized tissue types with distinct functions, from feeding and defense to symbiosis and skeleton formation. While these cell types have been characterized microscopically and more recently via single-cell RNA sequencing, spatially resolved high-throughput gene expression profiling remains limited in corals. Here we combine Laser Capture Microdissection with RNA sequencing to characterize tissue-specific gene expression in the reef building coral Pocillopora acuta. Oral tissues, adjacent to the seawater, exhibited 1,253 upregulated genes enriched for amino acid synthesis, transmembrane transport, signaling, environmental sensing, and secretion. These tissues showed high expression of immune and microbial-recognition genes consistent with their interface with seawater microbiota: mucins, lectins, toll-like receptors (TLRs), and MyD88 that connects TLRs to the NF-{kappa}B pathway. Aboral tissues, which build the corals skeleton, exhibited 552 upregulated genes enriched for developmental processes, cell adhesion, and stimulus response. We identified strong differential expression of biomineralization- associated genes, including Chitin Synthase and Wnt pathway members, suggesting previously underdescribed roles in skeleton formation. Critically, many genes implicated in specialized functions were expressed in multiple tissues. This lack of location specificity suggests functional biomarkers will likely entail multi-gene expression patterns rather than single genes. Collectively, we highlight the need for greater spatial resolution (e.g., single cell/nuclei and spatial transcriptomics) to fully resolve coral responses within their native tissue complexity. As anthropogenic climate change increasingly threatens coral reefs, spatially resolved molecular insight into coral biology will be critical for interpreting stress response mechanisms, forecasting their limits, and applying human interventions.

molecular biology↗

bioRxiv2026

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↗

bioRxiv2025

Contrasting temperature-induced gene network rewiring and isoform switching underlie relative thermal tolerance of coral species

Organismal thermal tolerance will shape future coral reef diversity and abundance, as ocean warming drives extensive bleaching and mortality through increasingly frequent marine heatwaves. Coral thermal tolerance varies markedly among species, reflecting differences in physiology underpinned by molecular regulatory mechanisms. Gene expression plasticity enables transcriptional adjustments to environmental stress, while alternative splicing and isoform switching further expand molecular adaptability by altering transcript diversity and abundance. Because genes function within combinatorial networks, changes in these network members and in the identity of highly influential hub genes can reveal higher-order biological reorganization under stress. Yet, the contribution of isoform switching to gene network dynamics remains unknown in corals. Here we integrate physiology, gene network topology, hub genes dynamics, and isoform switching across three Hawaiian corals, Porites compressa, Montipora capitata, and Pocillopora acuta, to identify molecular processes shaping thermal performance. We show that the interplay between expression plasticity, hub gene rearrangement, and isoform switching drives species-specific thermal tolerance. Network analysis uncovered extensive rewiring and temperature-responsive hub genes turnover regulated by switches in isoform usage. The most thermally tolerant species, P. compressa, shows high energy reserves, stable constitutive gene expression and continuous isoform adjustments across temperatures, while fine-tuning thermal response through dedicated hub genes. In contrast, the most thermally sensitive species, P. acuta, shows lowest energy reserves, with broad transcriptomic shifts and isoform switching controlling the reorganization of network leadership at high temperatures. Together, these findings identify isoform switching as a newly recognized regulatory mechanism contributing to coral thermal resilience and species persistence in warming oceans.

ecology↗

bioRxiv2025

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↗

bioRxiv2025

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↗

bioRxiv2025

Non-coding RNA Repertoire in Reef-Building Corals

Non-coding RNAs (ncRNAs) play critical regulatory roles in gene expression regulation that influences diverse biological processes in response to environmental change. Yet their characterization in non-model organisms, particularly sessile, benthic ecosystem engineers such as reef-building corals that are sensitive to climate change, remains limited. This study provides the first comprehensive analysis of the ncRNA repertoire of species from three ecologically important coral genera from Moorea, French Polynesia: Acropora pulchra, Pocillopora tuahiniensis, and Porites evermanni. These species demonstrate differing symbiotic partners, life history strategies, and physiological traits, offering a broad framework for documenting ncRNA variation in corals. We identified homologs for ncRNA biogenesis and functional machinery, characterized long ncRNAs (lncRNAs), microRNAs (miRNAs), and piwiRNAs (piRNAs), and assessed their genomic context and potential targets. Our findings reveal the presence of conserved ncRNA machinery across these coral species, indicating their capability to generate and utilize ncRNAs for the regulation of gene expression. We identified only a single miRNA conserved with corals and Eumetazoans (miR-100), four miRNAs shared across all three species, previously identified in other cnidarian taxa (miR-100, miR-2023, miR-2025, miR-2036), as well as several species-specific miRNAs. Predicted gene targets of the characterized miRNAs included immune response regulation in A. pulchra and P. tuahiniensis and signal transduction pathways in P. evermanni and P. tuahiniensis. Proximity analysis indicated >71-99% of piRNAs overlapped with genes, with genomic maintenance and stability identified as the primary functional enrichment of those genes. Our characterization of lncRNAs found little sequence overlap across each species (<2%), although lncRNAs in all three species were often in proximity to immune-related genes. This study lays the groundwork for the repertoire and regulatory roles of ncRNAs in reef-building corals, thereby expanding our understanding of epigenetic regulation in environmentally sensitive marine invertebrates and its potential implications in acclimatization and adaptation to environmental change.

molecular biology↗

bioRxiv2025

Coral venom and toxins as protection against crown-of-thorns sea star attack

Crown-of-thorns sea star (CoTS) outbreaks are one of the leading causes of hard coral cover decline across the Indo-Pacific, posing a major threat to the health and resilience of coral reefs. However, the drivers underlying feeding on preferred (e.g., Acropora spp.) versus non-preferred (e.g., Porites spp.) are poorly understood. We hypothesised that coral venom may influence CoTS food preferences. We investigated whether coral venom toxin and peptide families may drive CoTS prey preferences by comparing the genomes and transcriptomes of preferred (five Acropora species) and non-preferred (five Porites species and Echinopora lamellosa) prey species of CoTS. We constructed databases of known cnidarian venom toxins, and along with the full UniProtKB/Swiss-Prot Tox-Prot database, used these to identify toxin peptides and investigate function and phylogeny. The most abundant toxins across all coral species included kunitz-type neurotoxins, neurotoxic turripeptides, snake venom lectins, toxic proteases and actinoporins. There were proteins present only in certain Porites species but completely absent from all Acropora species (e.g., tereporin/conoporin, snake venom peptides) and vice versa (e.g., sarafotoxin). Further, Porites species contained a homolog to conkunitzin, a toxin known to disintegrate the tube feet of CoTS, suggesting a potential mechanism for their lower susceptibility to predation. We also observed a greater diversity of jellyfish-like proteins in CoTS-exposed Porites species compared to naive Porites species, suggesting these proteins deter CoTS. These findings have direct applications to assessing reef corals susceptibility to future CoTS outbreaks and active reef management.

bioinformatics↗

bioRxiv2025

Exposure to a gradient of warming and acidification highlights physiological, molecular, and skeletal tolerance thresholds in Pocillopora acuta recruits

Ocean warming and acidification are among the biggest threats to the persistence of coral reefs. Organismal stress tolerance thresholds are life stage specific, can vary across levels of biological organization, and also depend on natural environmental variability. Here, we exposed the early life stages of Pocillopora acuta in K[a]ne ohe Bay, Hawai i, USA, a common reef-building coral throughout the Pacific, to projected ocean warming and acidification scenarios. We measured ecological, physiological, biomineralization, and molecular responses across the critical transition from larvae to newly settled recruits following 6 days of exposure to diel fluctuations in temperature and pH in Control (26.8-27.9{degrees}C, 7.82-7.96 pHTotal), Mid (28.4-29.5{degrees}C, 7.65-7.79 pHTotal) and High conditions (30.2-31.5{degrees}C, 7.44-7.59 pHTotal). We found that P. acuta early life stages are capable of survival, settlement, and calcification under all scenarios. The High conditions, however, caused a significant reduction in survival and settlement capacity, with changes in the skeletal fiber deposition patterns. In contrast to a limited impact on the expression of biomineralization genes, the dominant transcriptomic response to the High conditions relative to the two other treatments included depressed metabolism, reduced ATP production and increased activity of DNA damage-repair processes. Collectively, our findings indicate that corals living in environments with large diurnal fluctuations in seawater temperature and pH, such as K[a]ne ohe Bay, can tolerate exposure to moderate projected increased temperature and reduced pH. However, under more severe environmental conditions significant negative effects on coral cellular metabolism and overall organismal survival jeopardize species fitness and recruitment.

molecular biology↗

bioRxiv2024

Decoding the Functional Interactome of Non-Model Organisms with PHILHARMONIC

Despite the widespread availability of genome sequencing pipelines, many genes remain part of the genome's "dark matter," where existing inference tools cannot even begin to guess the biological function of their proteins from sequence alone. This challenge is especially pronounced in organisms that are highly evolutionarily distant from well-studied models, where homology-based methods break down. Here, we describe PHILHARMONIC, a computational method that combines deep learning-based de novo protein interaction network inference with robust unsupervised spectral clustering and remote homology to illuminate functional organization in any non-model organism. From only a sequenced proteome, we show PHILHARMONIC generates meaningful functional hypothesis for protein functions, functional communities, and higher-order network structure. We validate its performance using experimental gene expression and pathway data in D. melanogaster, and we demonstrate its broad utility by analyzing temperature sensing and stress response pathways in the reef-building coral P. damicornis and its algal symbiont C. goreaui. PHILHARMONIC provides a general-purpose engine for functional discovery and biological hypothesis generation in non-model organisms, enabling systems-level insights across the full diversity of life.

bioinformatics↗

bioRxiv2024

Coral larvae employ nitrogen sequestration mechanisms to stabilize carbon provisioning from algal symbionts under increased temperature

Rising sea surface temperatures are increasingly causing breakdown in the nutritional relationship between corals and algal endosymbionts (Symbiodiniaceae), threatening the basis of coral reef ecosystems and highlighting the critical role of coral reproduction in reef maintenance. The effects of thermal stress on metabolic exchange (i.e., transfer of fixed carbon photosynthates from symbiont to host) during sensitive early life stages, however, remains understudied. We exposed symbiotic Montipora capitata coral larvae in Hawaii to high temperature (+2.5{degrees}C for 3 days), assessed rates of photosynthesis and respiration, and used stable isotope tracing (4mM 13C sodium bicarbonate; 4.5 h) to quantify metabolite exchange. While larvae did not show any signs of bleaching and did not experience declines in survival and settlement, metabolic depression was significant under high temperature, indicated by a 19% reduction in respiration rates, but with no change in photosynthesis. Larvae exposed to high temperature showed evidence for maintained translocation of a major photosynthate, glucose, from the symbiont, but there was reduced metabolism of glucose through central carbon metabolism (i.e., glycolysis). The larval host invested in nitrogen cycling by increasing ammonium assimilation, urea metabolism, and sequestration of nitrogen into dipeptides, a mechanism that may support the maintenance of glucose translocation under thermal stress. Host nitrogen assimilation via dipeptide synthesis appears to be used for nitrogen limitation to the Symbiodiniaceae, with the outcome of reduced symbiont population growth and retention of fixed carbon, effectively simulating photosynthate translocation to the host. Collectively, our findings indicate that although these larvae are susceptible to metabolic stress under high temperature, they can combat bleaching by diverting energy to nitrogen assimilation to maintain symbiont population density, photosynthesis, and carbon translocation.

cell biology↗

bioRxiv2024

DNA methylation modulates transcriptional noise in response to elevated pCO2 in the eastern oyster (Crassostrea virginica)

Ocean acidification significantly affects marine calcifiers like oysters, warranting the study of molecular mechanisms like DNA methylation that contribute to adaptive plasticity in response to environmental change. However, a consensus has not been reached on the extent to which methylation modules gene expression, and in turn plasticity, in marine invertebrates. In this study, we investigated the impact of pCO2 on gene expression and DNA methylation in the eastern oyster, Crassostrea virginica. After a 30-day exposure to control (572 ppm) or elevated pCO2 (2,827 ppm), whole genome bisulfite sequencing (WGBS) and RNA-Seq data were generated from adult female gonad tissue and male sperm samples. Although differentially methylated loci (DML) were identified in females (89) and males (2,916), there were no differentially expressed genes, and only one differentially expressed transcript in females. However, gene body methylation impacted other forms of gene activity in sperm, such as the maximum number of transcripts expressed per gene and changes in the predominant transcript expressed. Elevated pCO2 exposure increased gene expression variability (transcriptional noise) in males but decreased noise in females, suggesting a sex-specific role of methylation in gene expression regulation. Functional annotation of genes with changes in transcript-level expression or containing DML revealed several enriched biological processes potentially involved in elevated pCO2 response, including apoptotic pathways and signal transduction, as well as reproductive functions. Taken together, these results suggest that DNA methylation may regulate gene expression variability to maintain homeostasis in elevated pCO2 conditions and could play a key role in environmental resilience in marine invertebrates.

physiology↗

bioRxiv2023

Pocillopora meandrina daytime broadcast spawning in Moorea, French Polynesia

Knowledge of coral gamete release is fundamental to reef ecology and evolution, but cryptic species complicate reproduction studies. In Moorea, French Polynesia, when corals were decimated by crown-of-thorns and a cyclone between 2007-2010, recruitment of six cryptic species of Pocillopora spp. primarily drove decadal reef recovery. Broadcast spawning for these genetically-verified species at Moorea is, however, undocumented in the scientific literature. We conducted in situ surveys over 58 days during September 2022-January 2023, October 2023-January 2024, and October 2024-December 2024. To identify the Pocillopora spp. we used molecular analysis of mtORF and PocHistone markers. P. meandrina and P. grandis spawned 2-3 days following the full moons of October-December. In contrast, P. verrucosa and P. tuahiniensis spawned at the new moons in November-December, with P. verrucosa spawning on lunar days 0-1, and P. tuahiniensis spawning on lunar days 1-3. Diel offset in the timing of spawning following sunrise was present in both moon phases indicating a temporal speciation barrier. P. verrucosa spawned [~]45 min after sunrise, whereas P. tuahiniensis spawned [~]73 min after sunrise. Similarly, P. grandis spawned [~]40 minutes after sunrise, whereas P. meandrina spawned [~]65 minutes after sunrise. Only one colony of P. effusa spawned (lunar day 3 new moon [~]06:30-06:50), requiring further confirmation of the timing for this low abundance species. Collectively, these first spawning reports provide an initial scientific documentation of Pocillopora spawning at the genetically-verified species level in Moorea, increasing capacity to study the essential process of coral reproduction for critical reef building species. Data, Code, Image Archive: https://osf.io/5geqd/ ResumeLa connaissance de la liberation des gametes chez les coraux est fondamentale pour comprendre lecologie et levolution des recifs, mais la presence despeces cryptiques complique les etudes sur la reproduction. A Moorea, en Polynesie francaise, lorsque les coraux ont ete decimes par des etoiles de mer couronne depines et un cyclone entre 2007 et 2010, le recrutement de six especes cryptiques de Pocillopora spp. a principalement contribue a la recuperation des recifs au cours de la decennie suivante. Toutefois, la reproduction par emission synchronisee des gametes (broadcast spawning) de ces especes genetiquement verifiees a Moorea na pas encore ete documentee dans la litterature scientifique. Nous avons mene des observations in situ sur 58 jours entre septembre 2022 et janvier 2023, doctobre 2023 a janvier 2024, puis doctobre a decembre 2024. Pour identifier les especes de Pocillopora spp., nous avons utilise une analyse moleculaire des marqueurs mtORF et PocHistone. P. meandrina et P. grandis ont pondu 2 a 3 jours apres les pleines lunes doctobre a decembre. En revanche, P. verrucosa et P. tuahiniensis ont pondu lors des nouvelles lunes en novembre et decembre, P. verrucosa aux jours lunaires 0 a 1, et P. tuahiniensis aux jours lunaires 1 a 3. Un decalage journalier dans le moment de la ponte apres le lever du soleil a ete observe pour les deux phases lunaires, indiquant une barriere temporelle de speciation. P. verrucosa a pondu environ 45 minutes apres le lever du soleil, tandis que P. tuahiniensis a pondu environ 73 minutes apres. De maniere similaire, P. grandis a pondu environ 40 minutes apres le lever du soleil, alors que P. meandrina a pondu environ 65 minutes apres. Une seule colonie de P. effusa a pondu (jour lunaire 3, nouvelle lune, entre [~]06:30 et 06:50), ce qui necessite une confirmation supplementaire du moment de reproduction pour cette espece peu abondante. Collectivement, ces premieres observations de ponte constituent une premiere documentation scientifique de la reproduction des Pocillopora au niveau des especes genetiquement verifiees a Moorea, augmentant la capacite a etudier ce processus essentiel de reproduction chez des especes cles pour la construction des recifs.

ecology↗

bioRxiv2023

Genomic comparison of the temperate coral Astrangia poculata with tropical corals yields insights into winter quiescence, innate immunity, and sexual reproduction

Facultatively symbiotic corals provide important experimental models to explore the establishment, maintenance, and breakdown of the mutualism between corals and members of the algal family Symbiodiniaceae. The temperate coral Astrangia poculata is one such model as it is not only facultatively symbiotic, but also occurs across a broad temperature and latitudinal gradient. Here, we report the de novo chromosome-scale assembly and annotation of the A. poculata genome. Though widespread segmental/tandem duplications of genomic regions were detected, we did not find strong evidence of a whole genome duplication (WGD) event. Comparison of the gene arrangement between A. poculata and the tropical coral Acropora millepora revealed 56.38% of the orthologous genes were conserved in syntenic blocks despite [~]415 million years of divergence. Gene families related to sperm hyperactivation and innate immunity, including lectins, were found to contain more genes in A. millepora relative to A. poculata. Sperm hyperactivation in A. millepora is expected given the extreme requirements of gamete competition during mass spawning events in tropical corals, while lectins are important in the establishment of coral-algal symbiosis. By contrast, gene families involved in sleep promotion, feeding suppression, and circadian sleep/wake cycle processes were expanded in A. poculata. These expanded gene families may play a role in A. poculatas ability to enter a dormancy-like state ("winter quiescence") to survive freezing temperatures at the northern edges of the species range.

genomics↗

bioRxiv2023

Coral species-specific loss and physiological legacy effects are elicited by extended marine heatwave

Marine heatwaves are increasing in frequency and intensity, with potentially catastrophic consequences for marine ecosystems such as coral reefs. An extended heatwave and recovery time-series that incorporates multiple stressors and is environmentally realistic can provide enhanced predictive capacity for performance under climate change conditions. We exposed common reef-building corals in Hawai i, Montipora capitata and Pocillopora acuta, to a 2-month period of high temperature and high pCO2 conditions or ambient conditions in a factorial design, followed by 2 months of ambient conditions. High temperature, rather than high pCO2, drove multivariate physiology shifts through time in both species, including decreases in respiration rates and endosymbiont densities. Pocillopora acuta exhibited more significantly negatively altered physiology, and substantially higher bleaching and mortality than M. capitata. The sensitivity of P. acuta appears to be driven by higher baseline rates of photosynthesis paired with lower host antioxidant capacity, creating an increased sensitivity to oxidative stress. Thermal tolerance of M. capitata may be partly due to harboring a mixture of Cladocopium and Durusdinium spp., whereas P. acuta was dominated by other distinct Cladocopium spp. Only M. capitata survived the experiment, but physiological state in heatwave exposed M. capitata remained significantly diverged at the end of recovery relative to individuals that experienced ambient conditions. In future climate scenarios, particularly marine heatwaves, our results indicate a species-specific loss of corals that is driven by baseline host and symbiont physiological differences as well as Symbiodiniaceae community compositions, with the surviving species experiencing physiological legacies that are likely to influence future stress responses.

physiology↗

bioRxiv2023

Divergent recovery trajectories in reef-building corals following a decade of successive marine heatwaves

Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme heat stress events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individuals lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawaii, Montipora capitata and Porites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies of P. compressa exhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during and after the third heatwave. In contrast, bleaching-susceptible M. capitata repeatedly bleached during all successive heatwaves and exhibited seasonal bleaching for up to three years following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically, M. capitata displayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 months following the third heatwave. Conversely, P. compressa appeared to recover across most physiological metrics within two years, reverting to predictable seasonal variability. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene. Significance StatementCoral reefs are in jeopardy as climate change has led to increasingly frequent marine heatwaves. Some corals can survive these extreme heat stress events, thus acquiring environmental memory that may prime them for increased resistance and resilience in subsequent heatwaves via beneficial acclimatization. Yet, as the time between heatwaves decreases, the accumulation of stress experienced by some individuals may preclude opportunities for beneficial acclimatization. This nearly decade-long study revealed divergent recovery trajectories within and between species in response to successive marine heatwaves, ranging from costly to beneficial. As the climate continues to change, surviving corals must not only gain heat tolerance, but also rapidly recover to maintain the critically important ecosystem services that humanity relies on.

ecology↗