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Biology subjects

Elder, H.

Publications and source records attributed to Elder, H..

7 recordsLinked to original sources

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↗

Genome assemblies and genetic maps highlight chromosome-scale macrosynteny in Atlantic acroporids

BackgroundCorals belong to the Cnidaria, an early branching phylum of metazoans. Over the course of their long evolutionary history, they have adapted to changing environments, such as rising sea levels and increasing ocean temperatures. While their history speaks to their evolutionary capacity, it is less clear how quickly they may respond to rapid changes. A critical aspect of adaptive capacity is the structure of their genome and the genetic diversity contained within. FindingsHere, we present chromosome-scale genome assemblies and genetic linkage maps of two critically endangered coral species, Acropora palmata and A. cervicornis, the two extant Atlantic acroporid corals. Genomes of both species were resolved into 14 chromosomes with comparable assembly sizes (A. palmata, 287Mb; A. cervicornis, 305Mb). Gene content, repeat content, gene collinearity and macrosynteny were largely preserved between the Atlantic acroporids but a 2.5 Mb inversion and 1.4 Mb translocation were detected between two of the chromosome pairs. Macrosynteny and gene collinearity decreased when comparing Atlantic with Pacific acroporids. Paracentric inversions of whole chromosome arms characterized A. hyacinthus, specifically. In the larger context of cnidarian evolution, the four acroporids and another scleractinian coral with chromosome-resolved genome assemblies retained six of 21 cnidarian ancestral linkage groups, while also privately sharing numerous ALG fission and fusion events compared to other distantly related cnidarians. Genetic linkage maps were built using a 30K genotyping array with 105 offspring in one family for A. palmata and 154 offspring across 16 families for A. cervicornis. The A. palmata consensus linkage map spans 1,013.42 cM and includes 2,114 informative markers. The A. cervicornis consensus map spans 927.36 cM across 4,859 markers. A. palmata and A. cervicornis exhibited similarly high sex-averaged genome-wide recombination rates (3.53 cM/Mb and 3.04 cM/Mb, respectively) relative to other animals. In our gamete-specific maps, we found pronounced sex-based differences in recombination, known as heterochiasmy, in this simultaneous hermaphrodite, with both species showing recombination rates 2-2.5X higher in eggs compared to sperm. ConclusionsThe genomic resources presented here are the first of their kind available for Atlantic coral species. These data sets revealed that adaptive capacity of endangered Atlantic corals is not limited by their recombination rates, with both species exhibiting high recombination rates and heterochiasmy. Nevertheless, the two sister species maintain high levels of macrosynteny and gene collinearity between them. The few large-scale rearrangements detected deserve further study as a potential cause of fertilization barriers between the species. Together, the assemblies and genetic maps presented here now enable genome-wide association studies and discovery of quantitative trait loci; tools that can aid in the conservation of these endangered corals.

evolutionary biology↗

Performance of Orbicella faveolata larval cohorts does not align with previously observed thermal tolerance of adult source populations

Orbicella faveolata, commonly known as the mountainous star coral, is a dominant reef-building species in the Caribbean, but populations have suffered sharp declines since the 1980s due to repeated bleaching and disease-driven mortality. Prior research has shown that inshore adult O. faveolata populations in the Florida Keys are able to maintain high coral cover and recover from bleaching faster than their offshore counterparts. However, whether this origin-specific variation in thermal resistance is heritable remains unclear. To address this knowledge gap, we produced purebred and hybrid larval crosses from O. faveolata gametes collected at two distinct reefs in the Upper Florida Keys, a nearshore site (Cheeca Rocks, CR) and an offshore site (Horseshoe Reef, HR), in two different years (2019, 2021). We then subjected these aposymbiotic larvae to severe (36 {degrees}C) and moderate (32 {degrees}C) heat challenges to quantify their thermal tolerance. Contrary to our expectation based on patterns of adult thermal tolerance, HR purebred larvae survived better and exhibited gene expression profiles that were less driven by stress response under elevated temperature compared to purebred CR and hybrid larvae. One potential explanation could be compromised reproductive output of CR adult colonies due to repeated summer bleaching events in 2018 and 2019, as gametes originating from CR in 2019 contained less storage lipids than those from HR. These findings provide an important counter-example to the current selective breeding paradigm, that more tolerant parents will yield more tolerant offspring, and highlight the importance of adopting a holistic approach when evaluating larval quality for conservation and restoration purposes.

physiology↗

Long term maintenance of heterologous symbiont association in Acropora palmata on natural reefs

The sensitivity of reef-building coral to elevated temperature is a function of their symbiosis with dinoflagellate algae in the family Symbiodiniaceae. Changes in the composition of the endosymbiont community in response to thermal stress can increase coral thermal tolerance. Consequently, this mechanism is being investigated as a human-assisted intervention for rapid acclimation of coral in the face of climate change. Successful establishment of novel symbioses that increase coral thermal tolerance have been demonstrated in laboratory conditions; however, it is unclear how long these heterologous relationships persist in nature. Here, we show that Acropora palmata can form a novel symbiosis with Durusdinium spp. when reared in land-based aquaria. We tested the stability of this heterologous relationship by outplanting clonal replicates (ramets) of five A. palmata host genotypes to natural reefs in the lower Florida Keys. Amplicon sequencing analysis of ITS2-type profiles revealed that the majority of surviving ramets remained dominated by Durusdinium spp. two years after transplantation. However, 15% of ramets, including representatives of all genotypes, did exhibit some degree of symbiont shuffling or switching at six of eight sites, including complete takeover by site-specific strains of the native symbiont, Symbiodinium fitti. The predominant long-term stability of the novel symbiosis supports the potential effectiveness of symbiont modification as a management tool. However, the finding that 6-7 year-old coral can alter symbiont community composition in the absence of bleaching indicates that Symbiodiniaceae communities are indeed capable of greater flexibility under ambient conditions.

microbiology↗

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↗

Heritable variation in bleaching responses and its functional genomic basis in reef-building corals (Orbicella faveolata)

Reef-building corals are highly sensitive to rising ocean temperatures, and substantial adaptation will be required for animals and the ecosystems they support to persist in changing ocean conditions. Genetic variation that might support adaptive responses has been measured in larval stages of some corals, but these estimates remain unavailable for adult corals and the functional basis of this variation remains unclear. In this study, we focused on the potential for adaptation in Orbicella faveolata, a dominant reef-builder in the Caribbean. We conducted thermal stress experiments using corals collected from natural populations in Bocas del Toro, Panama, and used multilocus SNP genotypes to estimate genetic relatedness among samples. This allowed us to estimate narrow-sense heritability of variation in bleaching responses, revealing that this variation was highly heritable (h2=0.91). This estimate suggests substantial potential for adaptive responses to warming by natural populations of O. faveolata in this region. To investigate the functional basis for this variation, we applied genomic and transcriptomic approaches enabled by expanding sequence resources for this species. We used a genetic linkage map we have recently developed to map associations between SNP genotypes and bleaching responses, and identified four genetic markers associated with bleaching. We also profiled gene expression in corals with contrasting bleaching phenotypes, uncovering substantial variation in responses to thermal stress between heat-tolerant and heat-susceptible corals. Integrating these genomic and transcriptomic data with quantitative genetic analysis provides a new perspective on the mechanistic basis for thermal tolerance phenotypes and the potential for adaptation to rising ocean temperatures.

evolutionary biology↗