Bathymetric patterns of genetic variation in the coral-algal symbiosis

Local and global anthropogenic stressors on coral reefs are projected to increase over the next few decades. The extent to which reefs are affected by these stressors, however, is not uniform and may vary across reef environments. Deep reef areas, for example, have been hypothesized to be less susceptible to certain major disturbances (e.g., thermal bleaching events), which led to the proposition of the ‘deep reef refugia’ hypothesis (DRRH). The premise of the DRRH is that deep reef areas: (1) are protected (to some extent) from disturbances that affect shallow reef areas and (2) can provide a viable reproductive source for shallow reef areas following disturbance. This thesis critically evaluated these assumptions through careful examination of published literature and three molecular case studies that assessed the genetic diversity and structuring of corals and their associated algal endosymbionts (Symbiodinium) between distinct reef habitats on the Great Barrier Reef (GBR). The assumptions underlying the DRRH were first critically evaluated by reviewing the available data from Caribbean reefs due to the fact that there is considerably more information from this region compared to the Indo-Pacific. Although there is evidence that deep reefs (>30 m) can escape the direct effects of storm-induced waves and thermal bleaching events, deep reefs are not immune from disturbance and the notion that deep reef areas are generally protected from disturbances is not supported. Furthermore, the potential of deep reefs to provide a viable reproductive source for shallow reef areas following disturbance is only partly supported in that it is necessarily limited to ‘depth-generalist’ coral species (~25% of the total coral biodiversity), and larval connectivity may be limited by genetic structuring of host and symbiont populations over large depth ranges. Although Symbiodinium communities associated with shallow reef environments have been relatively well studied, little is known about symbiont diversity in deep reef areas of the Indo- Pacific. Symbiodinium diversity was therefore assessed in 10 coral genera from 45 to 70 m depth on the GBR using ITS2-DGGE. The deep-water Symbiodinium community consisted largely of pandemic host generalists, such as C1 and C3, which are also commonly found in shallow water corals across the Pacific and Caribbean. Several coral genera (e.g., Seriatopora, Montipora and Porites) harbored the same symbiont types (respectively C3n, C17 and C15) that were reported previously for these genera in shallow areas of the GBR, however most of the symbiont types identified here were previously found in association with other coral species or genera than those assessed in this study. This preliminary survey indicates that the bathymetric and physiological ranges of known Symbiodinium types may extend further than presently known, and that association with ‘depth-specialist’ Symbiodinium types is not necessarily an obligate strategy of corals with broad depth distributions. A mitochondrial (putative control region) and nuclear (three microsatellites) genetic assessment of the ubiquitous brooding coral (Seriatopora hystrix) coupled with an ITS2 assessment of its associated Symbiodinium across three adjacent reef habitats (spanning ~30 m depth) at three locations on the GBR revealed strong genetic structuring between host populations from adjacent habitats/depths (microsatellites: FST = 0.201-0.275; mtDNA: ! HAB- TOT = 0.832). However, high levels of genetic similarity (e.g., FST = 0.012) were evident between similar habitats/depths from different locations. A concordant habitat partitioning of both the coral host and its symbionts was observed, with four mitochondrial haplotypes (corresponding to four genetic clusters based on microsatellite analyses) and three Symbiodinium types occurring predominantly in particular habitats. The observed association of host and symbiont lineages with specific habitats, replicated across all loci and at two different locations, is consistent distinct sympatric gene pools that are maintained through ecologically-based selection. Furthermore, the strong genetic structuring of S. hystrix host and its symbiont populations across a depth gradient suggest that vertical connectivity (along the reef slope) may be limited in this species and opposes the assumption that deep reef populations can act as a viable reproductive source for shallow reef areas following disturbance. The role of functional differences and divergent selection in the zonation of S. hystrix host- symbiont associations (i.e., ecotypes) was explored through a 14-month reciprocal transplantation across habitats. Survival was generally higher for fragments transplanted back to their habitat of origin (~ 60%) compared to fragments transplanted to a different habitat (~ 20%), suggesting that partitioning may be due to differential selective pressures across habitats. There was only limited evidence for Symbiodinium 'shuffling' (<10% of fragments) during the experiment, and there were no observations of host-symbiont recombination between shallow and deep genotypes. Respirometry and pigment quantification assays revealed photo-physiological differences between shallow and deep ecotypes (after 14 months in the same habitat), with an increased heterotrophic capacity in deep ecotypes. Similar photo- acclimatisation potential was observed between the two shallow ecotypes, highlighting the importance of other potential (non-photo-physiological) traits under selection. These data further corroborate the notion that the observed divergence in S. hystrix is the result of divergent selection and adaptation of ecotypes to distinct reef habitats, and highlight the potential role of ecological speciation processes in the diversification of S. hystrix. In undertaking this thesis, it became clear that the assumptions of the DRRH are not rigorously defensible and that coral connectivity over large depth ranges may be more limited than previously thought due to processes of local adaptation. Nonetheless, the unique cryptic diversity in deep reef habitats and the potential to provide a refuge for local biodiversity (rather than a source of reproductive output) remains a promising aspect of coral reef biology as reefs enter a century of human and climate driven change.