Estimating the Potential for Adaptation of Corals to Climate Warming

Abstract

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.

Heritable differences in fitness-related traits among populations of the mustard hill coral, Porites astreoides

“…A later study on the same species reports a similar estimate, with additive parental effects explaining 47% of the variance in larval settlement (Kenkel et al, 2011). Csaszar et al (2010) estimated broad-sense heritabilities of symbiont, host and holobiont traits in adult A. millepora. Contrary to the results of Meyer et al (2009), they report primarily nonsignificant heritabilities for host antioxidant gene expression (Csaszar et al, 2010).…”

“…Although this metric is a good approximation of adaptive potential in long-lived, clonal organisms, such as corals (Csaszar et al, 2010), it is a fraction of phenotypic variance attributable to additive genetic effects (termed narrow-sense heritability, h 2 ) that determines the immediate response to selection (Falconer and Mackay, 1996). Since h 2 is part of H 2 , our estimates of broad-sense heritability for growth and survival in two populations of P. astreoides (Figure 4) overemphasize the true adaptive potential in these traits.…”

“…Csaszar et al (2010) estimated broad-sense heritabilities of symbiont, host and holobiont traits in adult A. millepora. Contrary to the results of Meyer et al (2009), they report primarily nonsignificant heritabilities for host antioxidant gene expression (Csaszar et al, 2010). However, reported heritabilities for symbiont and holobiont traits are almost all significant and H 2 estimates for growth range from 0.19 to 0.59 (Csaszar et al, 2010).…”

“…Substantial variation exists in thermotolerance among genotypes of Symbiodinium (Robinson and Warner, 2006;Howells et al, 2011) that affects holobiont growth (Little et al, 2004;Jones and Berkelmans, 2010) and bleaching thresholds (Oliver and Palumbi, 2011). In addition, high broad-sense heritability estimates for functional traits in Symbiodinium suggests that thermal adaptation of symbionts will have an important role in coral response to climate change (Csaszar et al, 2010), although it must be noted that this heritability was measured in hospite and some of it could have been attributable to the host. Coral thermotolerance limits are affected by host genetic background (Ulstrup et al, 2006;Abrego et al, 2008;Baird et al, 2009;Kenkel et al, 2013a) and holobiont thermal history (Brown et al, 2000(Brown et al, , 2002a(Brown et al, , 2002b.…”

“…Therefore, it is the adaptive potential of the coral holobiont that will truly determine the ability of coral populations to respond to climate change (Iglesias-Prieto and Trench, 1997;LaJeunesse et al, 2010). Csaszar et al (2010) report significant broad-sense heritabilities for coral growth based on variation among groups of clonal fragments sampled from two natural populations; however, these values must include a sizeable component attributable to prior environmental history of the sampled corals rather than genetic factors.…”