Genetic and environmental basis for Symbiodinium specificity in the coral-dinoflagellate symbiosis

Quigley, Kate M. (2016) Genetic and environmental basis for Symbiodinium specificity in the coral-dinoflagellate symbiosis. PhD thesis, James Cook University.

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The mutualism between scleractinian corals and the dinoflagellate genus Symbiodinium forms the nutritional basis for coral reef structure and growth, and contributes significantly to the physiology and resilience of the coral holobiont. Although the composition and diversity of in hospite Symbiodinium communities are known to vary among coral taxa, it is not yet clear what drives the formation of these communities. In particular, little is known about the full diversity of Symbiodinium communities in the early life stages of corals, their dynamics through time or the genetic contributions of coral hosts to these communities. Quantifying the diversity of Symbiodinium communities and the contribution of host genetics to their structure has broad implications for the capacity of these communities to undergo selection and therefore their adaptive potential. This thesis aims to deeply describe Symbiodinium communities in egg, larval, juvenile and adult life stages across a range of coral species, with a focus on quantifying this community as a continuous quantitative genetic trait to estimate host-symbiont heritabilities in corals with contrasting reproductive and symbiont transmission modes. Such knowledge is essential to evaluate the potential for adaptation and ecological rescue of coral populations though intervention strategies targeted at coral microbial communities, which have garnered substantial interest in recent years.

In order to more fully characterize Symbiodinium communities in corals, I used next-generation sequencing (NGS) and adapted bioinformatics tools to construct a novel pipeline that identifies and quantifies these symbionts. To convert high dimensional data into a quantitative genetic (QG) trait for heritability analysis, I adopted tools developed from mathematical ecology theory that incorporate presence/absence, abundance, sequence divergence and rarity into a single metric. Unlike conventional methods for genotyping Symbiodinium, this NGS method is able to detect community members at very low abundance to the type or intra-type level, which has previously only been done on a limited number of coral species and never in their early life-history stages. These methodologies were used to calculate Bayesian heritability (h²) estimates for three coral species that represent vertical (maternal transfer) and horizontal (environmental acquisition) symbiont transmission strategies (Chapters 2 and 3).

Vertical transmission of Symbiodinium communities is widely assumed to have high fidelity in brooding coral species that transmit Symbiodinium directly from parent to offspring. However, using brooded larvae with known parentage, I show that planulae of a vertically-transmitting, cryptic species of Seriatopora hystrix harbour novel diversity not found in adult colonies (Chapter 2). Moreover, the Symbiodinium community was found to be only 33% heritable (h², Bayesian narrow-sense heritability). I also found significant micro-scale spatial variation in the diversity of Symbiodinium communities associated with adult corals, further suggesting that substantial symbiont flexibility exists in vertically-transmitting, brooding corals across multiple life stages. These results overturn the paradigm that Symbiodinium communities in brooding corals are exclusively vertically transmitted, and instead suggest a new mixed-mode transmission strategy that is more in line with symbiosis models in other invertebrate groups. Results also highlight the potential for selection and adaptation of the symbiont community in corals sharing this transmission strategy, and their potential amenability to microbial intervention strategies, such as assisted evolution.

In contrast to brooding corals, Symbiodinium communities associated with the majority of broadcast spawning corals are acquired horizontally from the environment and are assumed to have low fidelity. However, QG heritability estimates calculated for juveniles of the broadcast spawning coral Acropora tenuis were greater (h² = 0.36) than expected for a horizontally transmitting corals using two methods: 1) regression-based estimation, and 2) Bayesian linear mixed model estimation (Chapter 3). In comparison, heritability of Symbiodinium communities in the broadcast spawning coral Montipora digitata, which transmits Symbiodinium from maternal parent to eggs, was higher (h² = 0.57), although still not as high as expected for a vertically-transmitting coral. Both A. tenuis and M. digitata contained novel core, common and rare Symbiodinium types not previously documented in these species. These findings suggest that coral species with contrasting Symbiodinium transmission strategies influence the uptake of their symbiont communities through the transmission of specific genetic architecture from one generation to the next. At the same time, the presence of novel types in juveniles and eggs underscores a degree of flexibility in symbiotic associations for these species.

The presence of novel Symbiodinium diversity in the three coral species studied here does not necessarily imply that they are functionally relevant to the host. To assess the ecological significance of novel community structures found in preceding chapters and test if variability among Symbiodinium communities translates to differences in fitness outcomes, as would be expected from a heritable trait, the fates of A. tenuis juveniles were monitored and compared among families. Symbiodinium communities hosted by juveniles differed significantly between high- and low-surviving families for all three measures quantified: symbiont taxonomic richness, identity and relative abundance (Chapter 4). Results suggest a selective advantage associated with harbouring a specific Symbiodinium community, and highlight Symbiodinium type A3 as a potentially key symbiont partner for this early life stage in A. tenuis. Parental identity also significantly affected larval weight, settlement success and juvenile survival. These results link substantial heritability estimates to differential fitness outcomes in juveniles, indicating that maternal colony identity can be an important driver of population demographic processes in coral populations.

Marine sediments are one of the most important reservoirs of Symbiodinium diversity for uptake by immature corals, and their importance is further implicated by the substantial contributions that environmental influence had on QG heritability estimates in the three study species. However, little is known about the biogeography of free-living Symbiodinium across environmental gradients. Deep sequencing of symbiont communities in marine sediments collected from eight sites along a temperature and water-quality gradient revealed substantial diversity and biogeographical partitioning of Symbiodinium types (Chapter 5). Juveniles of Acropora tenuis and Acropora millepora exposed to sediments took up distinct communities, compared both to each other and to symbiont availability within sediments. Significant differences in photochemical efficiency, growth and survival of juveniles were also attributed to symbionts acquired over the 145 days of sediment exposure. Variability in Symbiodinium type distributions among these reef habitats could be attributed to significant differences in sediment size classes, total organic nitrogen, and trace metals (al and fe) among sites. Results highlight spatial variability in the distribution of Symbiodinium types, and demonstrate that juvenile corals are selecting a relatively small and specific community from a large diversity of available types, whilst also supporting flexibility in the relationship dependent on external environmental conditions.

In summary, this thesis presents the first comprehensive appraisal of genetic and environmental influences governing Symbiodinium communities across all major reproductive and symbiont transmission modes in corals. A new mixed mode model of transmission in vertically transmitting corals was discovered, as well as novel diversity across eggs, planulae, juveniles and adults in three important coral species, and also across a range of sediment habitats. Results highlight the substantial adaptive potential of the symbiont community to rescue reefs from adverse climatic changes.

Item ID: 51572
Item Type: Thesis (PhD)
Keywords: Acropora millepora, Acropora tenuis, coral reef, geographic variation, heritability, juvenile, maternal effects, settlement, spawning corals, survivorship, Symbiodinium, temperature, water quality
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 4: Quigley, Kate M., Willis, Bette L., and Bay, Line K. (2016) Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis. Royal Society Open Science, 3. pp. 1-17.

Date Deposited: 17 Nov 2017 04:47
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 25%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060412 Quantitative Genetics (incl Disease and Trait Mapping Genetics) @ 40%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 35%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 50%
96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 50%
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