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Genomic and eco-evolutionary drivers of adaptive potential to climate warming in Western Pacific reef-building corals (Abstract and Citation only)
Thesis

Genomic and eco-evolutionary drivers of adaptive potential to climate warming in Western Pacific reef-building corals (Abstract and Citation only)

Hugo Denis
Southern Cross University
Doctor of Philosophy (PhD), Southern Cross University
2025
DOI:
https://doi.org/10.25918/thesis.560

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Abstract

Coral reefs Climate warming Coral bleaching Western Pacific Acute heat stress Population genomics Symbiodiniaceae Holobiont Gene flow GWAS GEAs Seascape genomics
The biodiversity and ecosystem services of coral reefs are threatened by ocean warming and recurrent marine heatwaves, causing widespread bleaching and mortality of reef-building corals. To persist into the future, corals must adapt to rising sea temperatures, and this will largely depend on natural selection acting on heritable variation in heat tolerance. Limited empirical data exist, however, on the variation in heat tolerance traits across spatial scales, their genomic architecture, and interactions with environmental and evolutionary factors. These knowledge gaps cause substantial uncertainty regarding fundamental questions such as where and how quickly adaptation in corals can occur. As a result, it remains challenging to incorporate evolutionary adaptive potential into conservation and restoration strategies. This thesis addresses these research gaps through the study of the widespread coral Acropora spathulata from the Great Barrier Reef, New Caledonia and the Coral Sea. To study the multifactorial components of adaptive potential, whole genome sequencing of >1,100 coral colonies and their dinoflagellate symbionts was combined with environmental data, measurements of individual heat tolerance from acute stress assays and field observations during marine heatwaves. These data reveal that the acute tolerance of corals aligns with the typical temperatures of their environments. However, heat tolerance varies more widely than previously thought across small spatial scales within reefs, providing the raw material for natural selection. Despite this standing variation, recent marine heatwaves exerted pervasive detrimental effects on the tolerance of corals, and low-latitude populations may be more vulnerable to climate warming as they live closer to their upper thermal limits. These potential limits to adaptation were corroborated by our observations of widespread mortality at several reefs on the Great Barrier Reef during the 2023–2024 marine heatwave. Population genetic analyses highlighted contrasting spatial patterns of genetic variation between coral hosts and their microalgal symbionts. Local adaptation of symbioses to environmental factors drives the association of A. spathulata with five distinct taxa of Cladocopium, including across short spatial scales. Conversely, considerable coral larval dispersal, estimated at ~100 km per generation, results in weak genetic structure across vast spatial scales. This high dispersal also contributes to large breeding population sizes that have safeguarded genetic diversity until now. Using demographic inference, I further report the first evidence of occasional long-distance dispersal and ongoing connectivity between Australian and New Caledonian broadcast-spawning coral populations. Host genomic associations with thermal environments and heat stress responses demonstrate that despite low overall genetic structure, genetic variants within and nearby specific genes drive polygenic heat adaptation. These signals of adaptation appear mostly non-parallel across reef systems, but point to several key genes repeatedly involved in thermal tolerance. My results also indicate a complex genetic basis of heat tolerance that may partly differ across types of thermal exposure, from acute stress to prolonged heatwaves and long-term climate adaptation. Nevertheless, polygenic scores derived from climate-associated variants substantially improved predictions of individual bleaching and mortality responses during a natural marine heatwave. This finding supports the utility of genetic markers in identifying individuals and populations with elevated heat tolerance. Overall, my findings reveal that some acroporid corals harbour a wealth of adaptive potential and may be at lower immediate risk of extinction than other coral taxa, but climate action and coordinated conservation networks across Western Pacific countries are necessary to safeguard their future.

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