Estimating potential for adaption of corals to climate warming

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Climate models predict rapidly warming oceans throughout the 21st century along with increased mortalities in reef-building coral-algal symbioses. Yet the ability of corals to adapt genetically in an evolutionary sense to a warmer climate is unknown. The adaptive potential of corals can be approximated by the extent to which variation in thermal tolerance is caused by genetic factors (i.e. by the broad-sense heritability, H²). This thesis investigated H² in a total of eleven thermal tolerance traits from two populations of the reef-building coral species Acropora millepora in the central Great Barrier Reef, Australia. The first population that was investigated associates with thermo-tolerant algal symbionts of the genus Symbiodinium (clade D), and came from Magnetic Island (MI), while the second population from Orpheus Island (OI) associates with the intermediately tolerant Symbiodinium type C2. Traits investigated were characteristic of the coral host, the algal symbiont, and the holobiont (whole symbiosis). The present thesis revealed extensive genetic variation in algal symbiont traits, which, together with short generation times, allows for rapid symbiont adaptation to climate warming. A significant adaptive potential was also found for coral colony growth rates, defined here as a holobiont trait. This is in stark contrast to the coral host, which did not display heritability for the majority of the traits investigated for either population. The coral host with its long generation time has therefore only a low potential to adapt to rapidly warming oceans. Five of the six thermal tolerance traits yielded significant heritabilities in each of the two symbiont types. In clade D symbionts from MI, the adaptive potential was given for the maximum quantum yield of photosystem II, Fv/Fm, one of the most commonly studied stress parameters in coral biology which indicates the overall health condition of photosystems. The one trait that did not yield a significant heritability in D symbionts was non-photochemical quenching (ФNPQ) of excess excitation energy. The trait ФNPQ can be considered as a switch for xanthophyll cycling, a mechanism that protects photosystems through conversion of the pigment diadinoxanthin (DD) into diatoxanthin (DT). However, D symbionts diverted 50 % of the incoming light energy for the initiation of the xanthophyll cycle (i.e. via ФNPQ), and the xanthophyll cycle mechanism itself showed significant heritability in either symbiont type. Both symbiont types also displayed significant heritability for another measure of photoprotection, the ability to regulate the pool size of photoprotective xanthophyll pigments (XP) relative to total light-harvesting pigments (LH). Although Fv/Fm did not yield a significant heritability in C2 symbionts from OI, both symbiont types again showed heritability for the effective quantum yield of photosystem II (ФPSII), and for unregulated energy dissipation (ФNO). For traits reflecting the function of the coral host, messenger RNA (mRNA) expression levels of four fundamental genes involved in the oxidative stress response were investigated. These genes code for cellular defences which regulate cellular iron homeostasis (i.e. Ferritin), repair denatured proteins (i.e. the heat shock protein Hsp70), detoxify harmful oxygen radicals (i.e. the mitochondrial enzyme manganese superoxide dismutase MnSOD), and might be involved in the dysfunction of coral cell-adhesion proteins during bleaching via a remodelling of surface receptors in the extra-cellular matrix (i.e. a zinc- metalloprotease, Zn²⁺-met). Each coral host population, however, showed heritability for expression of just one of those four genes (i.e. MnSOD in the MI population, and Zn²⁺-met in the OI population), therefore displaying only a limited capacity for evolution of thermal tolerance. Holobiont growth showed a significant heritability in both coral-algal populations, thus providing the basis for evolutionary adaptation. In the long term, however, this trait might be impaired by ocean acidification, which has a negative impact on coral calcification and, therefore, on holobiont growth rates. In summary, algal symbionts have short generation times and considerable genetic variation in functional traits, thus allowing for rapid adaptation to higher temperatures. However, adaptive response estimates based on low heritabilities in coral host traits along with the coral’s mainly sexual reproduction and long generation time raise concerns about the timely adaptation of the holobiont in the face of rapid climate warming.
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