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Genomic repeatability and predictability of climate (mal)adaptation in a reef-building coral

Zoe MeziereiD, Iva PopoviciD, Andreas BachleriD, Chris W. CoppiniD, Katrina McGuiganiD, Jennifer K. McWhorteriD, Yves‐Marie BozeciD, Cynthia RiginosiD

Abstract

Climate change is a growing threat to biodiversity, and the persistence of populations largely depends on their capacity to adapt to changing environmental conditions. Although there is an urgent need to forecast local adaptive potential, it is unclear how such predictions are affected by the genomic architectures underlying local adaptation across a species range. In this study, we examine the genomic basis of local adaptation of the short-distance dispersing coral Stylophora pistillata, sampled at forty-six sites across eight reefs of the Great Barrier Reef, Australia. Our results show that thermal adaptation for this species involves hundreds of genomic loci with combinations that differ across geographic regions. Although adaptive loci were largely region-specific, genotype-environment relationships estimated across the entire range could predict regional-level adaptive patterns. This shows that genome-wide sequence data combined with geographically broad sampling can support reliable evolutionary forecasting. Under climate change projections, predicted shifts in genotype-environment associations were highly spatially variable, both between and within geographic regions. While some populations might be sufficiently adapted for moderate (SSP1-2.6 and SSP2-4.5) climate warming by 2050, up to 30% may face severe maladaptation risk by 2100 under a high-emission (SSP5-8.5) scenario. Collectively, these findings offer new insights into the spatial distribution of coral adaptive potential and how it might shape corals resilience in a warming ocean.

02 /Specification & Classification

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In-depth summary

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Claude Opus 5.5 · xhigh effort · 8 Nov 2026 · from the full text of version 3 (20 Aug 2026) · CC BY 4.0

Thermal adaptation in coral Stylophora pistillata is polygenic and largely population-specific across the Great Barrier Reef, yet range-wide models predict regional genotype-environment patterns and future maladaptation.

Genomic offset forecasts assume genotype-environment associations apply range-wide, an assumption rarely tested and little examined in marine taxa such as corals compared with terrestrial plants. Using a dispersal-limited coral with strong regional genetic structure, this work tests locus-level and functional repeatability of thermal adaptation and whether range-wide models still predict regional adaptive patterns and future maladaptation.

Key results

  1. ShownAdaptation to mean temperature is polygenic and mostly population-specific. Only a small set of 10-kb genomic windows was repeatedly associated with temperature across the five S. pistillata populations.

    Weighted-Z analysis over 31,828 10-kb windows flagged 814 to 1,359 candidate windows per population (empirical p 0.05). PicMin found eleven windows repeated at FDR q<0.1 (one in three, three in four, seven in all five populations), against a permutation null mean of zero. 188 windows passed at q<0.5. · Genomic architecture of thermal local adaptation…; Genomic signatures of temperature adaptation…; Repeatability of thermal local adaptation across…

  2. ShownRepeatability at the functional level was also limited. GO enrichment of top candidate windows differed among populations, although it included temperature response and protein refolding. The repeated windows overlap genes linked to metabolism, protein turnover, apoptosis and cell adhesion.

    Using the top 1% of windows (319 per population), only 7% (14/192) of enriched Biological Process GO terms were shared by two or three populations. The eleven repeated windows overlap 15 genes (13 protein-coding, 2 non-coding RNAs), including peroxidasins and sulfotransferase family proteins. · Functional annotations of candidate adaptive…; Discussion; Functional enrichment in candidate windows under…

  3. ShownEnvironment explains a small but significant share of genome-wide variation, and 38% of the explainable signal overlaps with geography. The unique environmental component that remains is modest, and the thermal and shore-distance axis captures 45% of it.

    GBR-wide variance partitioning: environment 3.0% and geography 2.8% adjusted R². The partial RDA conditioned on geography kept 1.4%, with 38% of the full model's explainable variance confounded with geography. Env-PC1 (shore distance, thermal metrics) captured 45% of the partial model's explainable variation. All models were significant (permutation p<0.05). · Predictability of local adaptation across the…; Multivariate genotype-environment associations…

  4. ShownGenotype-environment relationships learned across the GBR, with the test population left out, closely predicted genome-wide adaptive genotype scores in held-out populations. Models trained on any single reef population predicted poorly.

    Out-of-sample Euclidean distances between observed and predicted scores on the first two RDA axes were smaller for GBR-wide training than for single-population training. The geography-conditioned partial RDA was the most accurate of three GBR-wide models. Heron Reef-trained models were worst; Central Reefs-trained models were generally better. · Predictability of local adaptation across the…; Discussion; Multivariate genotype-environment associations…; Figure legends

  5. SuggestedProjected genomic offsets vary within and among regions and are highest at northern and inshore reefs by mid-century. Late in the century they become broadly high under high emissions, partly in thermal conditions outside the historical training range.

    For 2040-2050 the three SSPs gave similar offset distributions. For 2090-2100, northern offsets rose under SSP2-4.5 vs SSP1-2.6 and rose range-wide under SSP5-8.5 (Tukey post-hoc p<0.05), where Far North temperatures reach +2.3°C above the historical maximum. The abstract cites up to 30% at severe risk by 2100 under SSP5-8.5. · Abstract; Genomic predictions of local (mal)adaptation…; Discussion; Figure legends

Methods, data and reproducibility

Whole-genome resequencing of GBR colonies. Per-population Kendall's tau tests of allele frequency vs temperature were combined into 10-kb windows by weighted-Z analysis, with PicMin for cross-population repeatability. Redundancy analysis on environmental principal components gave out-of-sample predictions; a separate RDA on mean temperature, temperature range and shore distance gave climate genomic offsets.

  • S. pistillata Taxon1 colonies sequenced by short-read WGS (mean 9.7x) at eight GBR reefs, shallow (4-7 m) and deeper (12-15 m) sites; 2.4 million filtered bi-allelic SNPs · Stylophora pistillata (Taxon1) · n = 237 sampled; 230 individuals retained; 46 sites · NCBI BioProject PRJNA1404865
  • S. pistillata reference assemblies: contig-level genome from a GBR specimen used for mapping, scaffolded onto a chromosome-level assembly · Stylophora pistillata · GCA_032172095.1; GCA_964205215.1
  • RNA-Seq datasets used as transcript evidence for Egapx structural annotation of the reference genome · n = 41 RNA-Seq datasets
  • eReefs GBR1/GBR4 hydrodynamic model outputs (monthly, 2015-2023) plus SWAN-derived wave exposure, reduced to six uncorrelated site-level variables · n = 108 months; six retained variables
  • NOAA Coral Reef Watch satellite temperature records (5 km resolution), annual means 1985-2024, for sampling sites and all GBR reefs
  • CMIP6 ensemble of AOGCMs under SSP1-2.6, SSP2-4.5 and SSP5-8.5, downscaled to 10 km; decadal means for 2040-2050 and 2090-2100 · n = ten AOGCMs
Methods & tools
Trimmomatic, BWA-MEM, Samtools v1.10, picard (read processing and mapping), GATK HaplotypeCaller, GenomicsDBImport, GenotypeGVCFs (joint SNP calling), VCFtools v0.1.16 and PLINK v2.0 (filtering, LD pruning, genomic PCA), BEAGLE 5.3 (phasing and imputation), Weighted-Z Analysis (WZA) with Kendall's tau, PicMin (order-statistic test of repeated selection), Redundancy analysis and partial RDA (vegan R package), RagTag v2.1.0 and D-GENIES (scaffolding and alignment visualisation), Egapx v.0.5.2, BUSCO, OMark (structural annotation and assessment), eggNOG-mapper (DIAMOND), InterProScan v5.75-106.0, AnnotationForge, topGO elim Fisher, AlphaFold3 and Foldseek (structural homology for uncharacterised proteins), eReefs, SWAN wave model, NOAA Coral Reef Watch, CMIP6 AOGCM ensemble
Software & environment
Samtools v1.10, VCFtools v0.1.16, PLINK v2.0, BEAGLE 5.3, RagTag v2.1.0, Egapx v.0.5.2, InterProScan v5.75-106.0, eggNOG database released 31 March 2025; R packages vegan and topGO without stated versions.
Reproducibility gaps
No hardware or runtime reported. Processed environmental covariates and downscaled climate projections are not listed as deposited. Permutation, WZA and prediction details are deferred to Supplementary Information.
Limitations (6)
  • Site temperatures came from coarse-resolution hydrodynamic models rather than in situ loggers, so fine-scale thermal contrasts among sites may be missed and the number of adaptive loci underestimated. · stated by the authors
  • The genomic offset RDA was deliberately not conditioned on geography. The authors acknowledge this may inflate offset estimates through confounded isolation-by-distance signal. · stated by the authors
  • Offsets are likely inaccurate under environmental novelty: under SSP5-8.5 in 2090-2100, northern GBR mean annual temperature exceeds 30°C against a range-wide historical maximum of 27.7°C, outside the training range. · stated by the authors
  • The offset models ignore effective population size, migration and other processes shaping adaptive variation, and they assume no adaptive gene flow. Small-effect loci may be missed by genome scans, and the correlative predictions still need experimental or heatwave-based validation. · stated by the authors
  • Cross-population validation used a six-variable environmental PCA and favoured the geography-conditioned partial RDA. Offsets instead used an unconditioned three-variable model extrapolated in time, so the spatial validation does not directly cover the forecasting model. · noted in this summary
  • The abstract's figure of up to 30% facing severe maladaptation by 2100 is not tied to a stated offset threshold or calculation in the main text, and prediction accuracy is reported only graphically, without numeric summaries. · noted in this summary

Who should read:Read this if you use genotype-environment associations or genomic offsets to forecast climate adaptation, especially in genetically structured, dispersal-limited marine species such as corals.

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