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.2023 Jul 28;14(1):4475.
doi: 10.1038/s41467-023-39651-7.

The role and risks of selective adaptation in extreme coral habitats

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The role and risks of selective adaptation in extreme coral habitats

Federica Scucchia et al. Nat Commun..

Erratum in

Abstract

The alarming rate of climate change demands new management strategies to protect coral reefs. Environments such as mangrove lagoons, characterized by extreme variations in multiple abiotic factors, are viewed as potential sources of stress-tolerant corals for strategies such as assisted evolution and coral propagation. However, biological trade-offs for adaptation to such extremes are poorly known. Here, we investigate the reef-building coral Porites lutea thriving in both mangrove and reef sites and show that stress-tolerance comes with compromises in genetic and energetic mechanisms and skeletal characteristics. We observe reduced genetic diversity and gene expression variability in mangrove corals, a disadvantage under future harsher selective pressure. We find reduced density, thickness and higher porosity in coral skeletons from mangroves, symptoms of metabolic energy redirection to stress response functions. These findings demonstrate the need for caution when utilizing stress-tolerant corals in human interventions, as current survival in extremes may compromise future competitive fitness.

© 2023. The Author(s).

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Genetic differentiation and gene expression patterns between habitats.
a Hierarchical clustering dendrogram based on proportions of shared alleles shows genetic differentiation between reef and mangrove corals. Branch height represents dissimilarity scores on the left and the coancestry coefficient on the right, based on pairwise identity-by-state distances among samples.b Habitat of origin explains most of the variations between the gene expression profiles of reef and mangrove corals (PC1). The Principal Component Analysis is based on variation in mean log2 fold-change across differentially expressed genes.
Fig. 2
Fig. 2. Gene expression profiles and enriched biological processes between reef and mangrove corals.
a Differentially expressed genes with similar expression profiles grouped into two distinct k-means clusters. Clustering is based on expression (log2 fold-change) relative to the row mean in the gene count matrix.b Biological functions enriched within each gene expression cluster. Each Gene Ontology (GO) slim category summarizes a group of significantly (Wallenius test,p < 0.05) enriched GO terms (list available in Supplemental Data 1). Dot colors represent the number of GO terms enriched within each GO slim. For graphical purposes, only GO slims with more than three enriched GO terms were plotted. C1 cluster 1, C2 cluster 2.
Fig. 3
Fig. 3. Changes in skeletal morphometrics among locations.
a,b Cross-sectional tomography slices providing an overview of the internal skeleton architecture, which was characterized in terms of (c,d) single-polyp volumetric thickness, (e) hardness (shore hardness value, higher values indicate a harder material), density, and porosity (ratio of the pore volume connected to the external skeleton surface to bulk volume of the skeleton). Boxplots ine show first and third quartiles, median line, and whiskers at ±1.5 interquartile range. Asterisks represent significant differences computed with two-sided unpairedt test (polyp volume thickness,n = 9,F = 1.542,p < 0.05) or two-sided Mann–Whitney test (density,n = 15–21,p < 0.01; porosity,n = 15–21,p < 0.01). No significant difference in hardness was found between mangroves and reef corals (two-sided Mann–Whitney test,n = 120,p > 0.05). Source data are provided as a Source Data file.
Fig. 4
Fig. 4. Differences in micro-skeletal features ofPorites lutea.
a,c Surface morphology by electron microscopy.b Polyps of reef corals have larger calyxes compared to mangrove corals. Boxplots inb show first and third quartiles, median line and whiskers at ±1.5 interquartile range, asterisk represents a significant difference computed with two-sided unpairedt test (n = 12,F = 2.287,p < 0.0001).d,e Within each single calyx, spines are arranged in a downward configuration in mangrove corals which differs from the shallower arrangement of reef corals (indicated by the red arrows).f,g Enlargements of the spines showing granulated surface composed byh,i bundles of fibers with a less compact and less rounded texture in mangrove corals compared to reef corals. Spines arrangement and surface texture observations were repeated independently forn = 12 polyps per each habitat. Source data are provided as a Source Data file.
Fig. 5
Fig. 5. Conceptual diagram of coral trade-offs across organismal to ecological scales associated with living in an extreme multi-stressor environment.
Common dynamics in biological traits observed in corals living in mangrove environments, characterized of higher temperatures (red color in the scheme), higher or lower salinity levels (red and blue color together), and lower oxygen, light, and pH levels (blue color) compared to neighboring reef sites–,–,,,, (see Supplemental Table 1). To cope with such climate change like fluctuations in abiotic environmental features, corals put in place trade-offs spanning between different scales of biological organization (organismal to population levels). For example, higher metabolic rates, e.g. coral host respiration rates, and energy expenditure (upward arrows) leads to reduction in calcification rates and skeleton density (downward arrows). Such environmental setting also drives strong selective pressure which tends to reduce intra-population genetic diversity. At higher levels of biological hierarchy, both increases and decreases in species abundance and richness have been observed between different coral species (indicated by a slash).
Fig. 6
Fig. 6. Study sites.
Overview of the reef (left image) and mangrove (right image) sites on the Great Barrier Reef adjacent to Low Isles and Woody Isles, respectively, whereP. lutea corals were collected. Pictures provide a typical view ofP. lutea found in these two environments. The red dot off the coast of Australia indicates the location of the study area.
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References

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