Coral symbionts in warming seas: population dynamics, adaptation and acclimatisation of Symbiodinium

Howells, Emily (2011) Coral symbionts in warming seas: population dynamics, adaptation and acclimatisation of Symbiodinium. PhD thesis, James Cook University.

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Abstract

Endosymbiotic photosymbionts, belonging to the dinoflagellate genus Symbiodinium, enable corals to succeed as dominant reef builders under ambient conditions, yet are also sensitive to anomalous changes in their thermal environment. Stressful temperatures cause photosynthetic damage to Symbiodinium, which can initiate lethal or sub-lethal coral bleaching. The capacity of Symbiodinium to resist and respond to stress (i.e. resilience) is crucial for the future persistence of corals. The aim of research presented in this thesis was to evaluate the influence of Symbiodinium population traits on the resilience of corals to warming seas. For within-type populations of Symbiodinium, spatial and temporal patterns of genetic diversity were investigated along with the potential for genetic adaptation and physiological acclimatisation to different thermal environments. Populations of the generalist Symbiodinium types C1, C2 and D (ITS1 rDNA) were used as a model system in the bleaching sensitive coral, Acropora millepora, on inshore reefs of the Great Barrier Reef (GBR).

Genetic diversity and connectivity were estimated for Symbiodinium C2 populations using eight polymorphic microsatellite DNA markers. At the central GBR, Symbiodinium C2 assemblages were genotyped in more than 400 colonies of A. millepora sampled at 7 sites (0.4 to 13 km apart) across a 12 year period. Within-host and within-reef assemblages were genetically diverse (up to 7 alleles per microsatellite locus per coral colony), with significant structure observed at all spatial and temporal scales investigated. Differentiation among sites accounted for 19-27% of the total genetic variation and was consistent with restricted hydrodynamic dispersal of Symbiodinium and the nature of local disturbance regimes. Differentiation among sampling years accounted for a lesser 7% of the total genetic variation and was associated with significant coral mortality during bleaching and cyclone events. Bleached corals hosted less diverse Symbiodinium C2 assemblages than healthy corals, indicating that genotypes may be lost during bleaching-induced reductions in Symbiodinium densities. Such population bottlenecks were investigated in more detail by following changes in Symbiodinium C2 assemblages before and after a severe bleaching episode at sites in the southern GBR. A 10 % decline in reef-wide genetic diversity of Symbiodinium C2, including the loss of 16 alleles, was observed after the bleaching episode. The appearance of a few novel alleles after bleaching, combined with the high density of Symbiodinium on coral reefs, suggests that recovery of genetic diversity lost through bleaching is possible. However, if bleaching events become more frequent and severe, the genetic diversity of Symbiodinium populations could become eroded, especially as lost diversity is unlikely to be readily replenished by re-seeding from adjacent reefs.

Conversely, limited genetic connectivity between reefs may have positive implications for populations by promoting adaptation to local environmental conditions. Adaptation of Symbiodinium populations was examined by comparing the thermal tolerance of Symbiodinium type C1 from two central GBR reefs that differ in summer maximum temperatures by ~2°C. Following acclimation to a common thermal environment, Symbiodinium C1 populations displayed heat stress responses that correlated with their native thermal environment, both in symbiosis with a cohort of A. millepora juveniles and in cell cultures. In symbiosis, Symbiodinium C1 from the cooler reef underwent chronic photoinhibition at an elevated temperature of 32°C, causing severe bleaching and partial mortality of juvenile coral hosts. In contrast, Symbiodinium C1 from the warmer reef thrived at 32°C, with high rates of photochemical efficiency and rapid growth of juvenile coral hosts. A second heat stress experiment demonstrated that adaptive variation in the thermal tolerance of Symbiodinium C1 populations was maintained after more than 30 asexual generations in culture. Pigment profiles of Symbiodinium C1 showed that levels of photoprotective pigment (β-carotene relative to chlorophyll a) were more than twofold greater in the population native to the warmer reef indicating a functional basis for variation in thermal tolerance. These results demonstrate that Symbiodinium types can adapt to local thermal environments and that this adaptation shapes the fitness of coral hosts.

The contribution of physiological acclimatisation to adaptive variation in thermal tolerance was investigated during reciprocal transplantation of adult coral symbioses between the warm central and cool southern regions of the GBR. Throughout a year of transplantation, A. millepora-Symbiodinium D associations from the central GBR were exposed to gradually cooling temperatures and A. millepora-Symbiodinium C2 associations from the southern GBR were exposed to gradually warming temperatures.

In both locations, native corals remained healthy and transplanted corals were healthy over initial months when temperatures remained within native thermal regimes. However, during winter, A. millepora-Symbiodinium D associations transplanted to the southern GBR bleached and the majority suffered whole or partial mortality at temperatures <1°C below their native minimum. Similarly, during summer, A. millepora-Symbiodinium C2 associations transplanted to the central GBR bleached and suffered whole or partial mortality at temperatures 1-2°C above their native maximum. At the central GBR during summer bleaching, mortality was preceded by a change in the dominant Symbiodinium type from C2 to D within transplanted corals. The strong interaction between genotype and environment observed for bleaching and mortality (as well as for parameters of growth and reproduction) re-affirm the importance of genetic adaptation in defining the thermal limits of A. millepora- Symbiodinium partnerships. These results likely reflect differences in the thermal tolerance among Symbiodinium types and populations, however variation between coral host populations may also exist.

Findings presented in this thesis demonstrate that coral symbioses are adapted to their current thermal environments. Increases in thermal tolerance required for A. millepora symbioses to persist under warmer seas are dependent on continued genetic adaptation, as there is little potential for acclimatisation beyond current thermal regimes. Critical next steps to determine whether adaptation keeps pace with future warming include the application of functional genetic approaches to population genotyping and quantifying rates of adaptation for both Symbiodinium and coral hosts.

Item ID: 34422
Item Type: Thesis (PhD)
Keywords: acclimatization; adaptation; coral growth; coral; GBR; genetic diversity; genetic structure; genetic variation; Great Barrier Reef; population ecology; reef building; rising ocean temperatures; Symbiodinium; symbiosis; thermal tolerance; warming seas; zooxanthellae
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Howells, Emily J., Willis, Bette L., Bay, Line K., and van Oppen, Madeleine J.H. (2013) Spatial and temporal genetic structure of Symbiodinium populations within a common reef-building coral on the Great Barrier Reef. Molecular Ecology, 22 (14). pp. 3693-3708.

Chapter 4: Howells, E. J., Beltran, V. H., Bay, L. K., Willis, B. L., Van Oppen, M. J. H., and Larsen, N. W. (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change, 2 (2). pp. 116-120.

Chapter 5: Howells, Emily J., Berkelmans, Ray, van Oppen, Madeleine J.H., Willis, Bette L., and Bay, Line K. (2013) Historical thermal regimes define limits to coral acclimatization. Ecology, 94 (5). pp. 1078-1088.

Appendix 1: Bay, Line, Howells, Emily J., and van Oppen, Madeleine J.H. (2009) Isolation, characterisation and cross amplification of thirteen microsatellite loci for coral endo-symbiotic dinoflagellates (Symbiodinium clade C). Conservation Genetics Resources, 1 (1). pp. 199-203.

Appendix 2: Van Oppen, Madeleine J.H., Souter, Petra, Howells, Emily J., Heyward, Andrew, and Berkelmans, Ray (2011) Novel genetic diversity through somatic mutations: fuel for adaptation of reef corals? Diversity, 3 (3). pp. 405-423.

Date Deposited: 20 Nov 2014 01:10
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060207 Population Ecology @ 100%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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