Estimating potential for adaption of corals to climate warming

University of Technology, Sydney. Faculty of Science.Open AccessClimate 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

Estimating the Potential for Adaptation of Corals to Climate Warming

The persistence of tropical coral reefs is threatened by rapidly increasing climate warming, causing a functional breakdown of the obligate symbiosis between corals and their algal photosymbionts (Symbiodinium) through a process known as coral bleaching. Yet the potential of the coral-algal symbiosis to genetically adapt in an evolutionary sense to warming oceans is unknown. Using a quantitative genetics approach, we estimated the proportion of the variance in thermal tolerance traits that has a genetic basis (i.e. heritability) as a proxy for their adaptive potential in the widespread Indo-Pacific reef-building coral Acropora millepora. We chose two physiologically different populations that associate respectively with one thermo-tolerant (Symbiodinium clade D) and one less tolerant symbiont type (Symbiodinium C2). In both symbiont types, pulse amplitude modulated (PAM) fluorometry and high performance liquid chromatography (HPLC) analysis revealed significant heritabilities for traits related to both photosynthesis and photoprotective pigment profile. However, quantitative real-time polymerase chain reaction (qRT-PCR) assays showed a lack of heritability in both coral host populations for their own expression of fundamental stress genes. Coral colony growth, contributed to by both symbiotic partners, displayed heritability. High heritabilities for functional key traits of algal symbionts, along with their short clonal generation time and high population sizes allow for their rapid thermal adaptation. However, the low overall heritability of coral host traits, along with the corals' long generation time, raise concern about the timely adaptation of the coral-algal symbiosis in the face of continued rapid climate warming

Cavitation bubbles generated by the D-Actor 200 and the Swiss DolorClast devices.

<p>The panels show the frames with the highest number of labeled pixels (from the corresponding high-speed imaging film sequences described in the main text) generated by the D-Actor 200 (A-D) operated at 3 bar and 1 Hz (A), 3 bar and 15 Hz (B), (maximum) 5 bar and 1 Hz (C), and 5 bar and 15 Hz (D), as well as with the Swiss DolorClast (E-H) operated at 3 bar and 1 Hz (E), 3 bar and 15 Hz (F), (maximum) 4 bar and 1 Hz (G), and 4 bar and 15 Hz (H). The scale bar represents 5 mm.</p

Devices investigated in the present study and their working principles.

<p>(A) Working principle of radial extracorporeal shock wave therapy (rESWT) devices. Compressed air (1) is used to fire a projectile (2) within a guiding tube (3) that strikes a metal applicator (4) placed on the patient’s skin. The projectile generates stress waves in the applicator that transmit pressure waves (5) non-invasively into tissue. Note that both the Swiss DolorClast (B) and the D-Actor 200 (C) share this construction principle. (B) “Radial” handpiece of the Swiss DolorClast (EMS) with the 15-mm applicator. (C) Handpiece of the D-Actor 200 (Storz Medical) with the 15-mm applicator. (D) Vibracare (G5/General Physiotherapy). The arrow indicates the direction of view into the chamber of the Vibracare head that was opened in (E); the asterisk indicates the backside of the chamber. (E) Working principle of the Vibracare. A flywheel mass (6) rotates around a vertical axis (7) within a chamber (asterisk).</p

Absence of cavitation bubbles when investigating the Vibracare device with high speed imaging.

<p>The arrows point to the surface of the moving head of the device in frames of the high-speed imaging experiments, showing minimum (A) and maximum (B) deflection of the device’s head.</p

Damage of the surface of x-ray film caused by pressure waves generated by the D-Actor 200 and the Swiss DolorClast devices.

<p>The figures show the surface of x-ray film after exposure to 10,000 pressure waves generated by the D-Actor 200 (A) and the Swiss DolorClast (B) at maximum energy settings (i.e., 5 bar for the D-Actor 200 and 4 bar for the Swiss DolorClast). The asterisk in (A) indicates a hole in the x-ray film. The Vibracare device operated at maximum energy settings (50 cycles per second) had no detectable impact on x-ray film (C). The scale bars represent 500 μm.</p

Pressure waves and cavitation bubbles generated by the D-Actor 200 and the Swiss DolorClast devices.

<p>Representative frames of the high-speed imaging experiments described in the main text, showing pressure waves (arrows) emitted from the applicators of the D-Actor 200 operated at (maximum) 5 bar air pressure (on the left) and the Swiss DolorClast operated at (maximum) 4 bar air pressure (on the right). The panels show five consecutive frames each 3.33 μs apart, plus a subsequent frame that was captured 120 μs after the first frame. Asterisks indicate the tip of the applicators lowered from above into the top section of the camera’s field-of-view. Note that the first cavitation bubbles were already detected at 10 μs after occurrence of the pressure wave (arrowheads in frames “+10 μs”). The scale bar represents 5 mm.</p

Exposure of <i>C</i>. <i>elegans</i> worms to radial shock waves and the movements of the Vibracare head.

<p>In (A) the “Radial” handpiece of the Swiss DolorClast (Electro Medical Systems) with the 6-mm applicator was lowered from above into one U-bottom well of a 96-well plate containing <i>C</i>. <i>elegans</i> worms either in S-Medium or PVA (see main text). A fluorinated rubber O-ring (green) was used to seal the U-bottom well. In (B) a 96-well plate containing <i>C</i>. <i>elegans</i> worms, sealed with parafilm and closed with its lid, was fixed with adhesive tape onto the upwards facing massaging head of the Vibracare (G5/General Physiotherapy).</p

Results of the quantitative analysis of the high-speed imaging experiments.

<p>Number of detected pixels as a function of time in the high-speed imaging experiments described in the main text, obtained for the D-Actor 200 (A-D) operated at 3 bar and 1 Hz (A), 3 bar and 15 Hz (B), (maximum) 5 bar and 1 Hz (C), and 5 bar and 15 Hz (D), as well as with the Swiss DolorClast (E-H) operated at 3 bar and 1 Hz (E), 3 bar and 15 Hz (F), (maximum) 4 bar and 1 Hz (G), and 4 bar and 15 Hz (H).</p