Nature or nurture? Testing the correlation between stress tolerance and genotype in the coral Acropora millepora on the Great Barrier Reef

Jin, Young Koo (2015) Nature or nurture? Testing the correlation between stress tolerance and genotype in the coral Acropora millepora on the Great Barrier Reef. PhD thesis, James Cook University.

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Corals are known to have both high phenotypic plasticity and significant capacity for acclimatisation, either through physiological, biochemical and behavioural responses to environmental stochasticity, or through contributions of symbiotic Symbiodinium to the physiological tolerance of the coral holobiont. Local adaptation is suggested by the fact that populations along environmental gradients maintain differences in environmental tolerance after acclimatisation to the same condition, as well as by the existence of correlations between the genetic diversity of coral hosts and environmental gradients in natural coral populations. However, no study has yet identified genetic markers underlying stress tolerance variation in corals.

The research presented here aims to improve knowledge of the adaptive importance of genetic diversity within coral populations by: (1) developing a cost- and time-efficient single nucleotide polymorphism (SNP) genotyping method that accurately estimates allele frequencies from pooled samples (Chapter 2); (2) investigating correlations between allele frequencies at candidate loci and temperature and water quality gradients along the Great Barrier Reef (Chapter 3); (3) validating genotypeenvironment correlations at candidate loci for phenotypes associated with bleaching tolerance in both field and laboratory settings (Chapter 4); and, (4) predicting the spatial distribution of allele frequencies at the anti-oxidant capacity loci identified in Chapter 4 through Bayesian belief network modelling (Chapter 5).

SNPs are the most common type of genetic variation and are present at both functional and neutral loci, making them ideal markers to study adaptive molecular variation. SNP allele frequency distributions can be used to identify coral populations that show signatures of adaptation to local environmental conditions, because the frequency of genetic variants (i.e., alleles) will vary with selection for or against these mutations and any other linked loci that affect fitness of the organism. Examination of genomic signatures of environmental change at the population level provides information about the resilience of coral populations at broad geographical scales. Genotyping of pooled DNA for estimating allelic proportions provides a time- and costeffective method for large sample sets. In Chapter 2, I introduce two quantitative High Resolution Melting (qHRM) methods for measuring allele frequencies at known SNP loci in pooled DNA samples: the "peaks" method, which can be applied to large numbers of SNPs, and the "curves" method, which is more labour intensive but also more accurate.

In Chapter 3, the distributions of SNP allele frequencies at five functional loci were investigated in 25 populations of Acropora millepora along the Great Barrier Reef using the curves genotyping method. Significant correlations between allele frequencies and gradients in both water quality and temperature were detected at two functional loci.

In Chapter 4, I validated the two genetic markers as true quantitative trait loci for anti-oxidant capacity in the common coral, A. millepora. Field surveys revealed that colonies carrying G and T alleles, respectively, at the two loci were significantly less affected by two bleaching events. These results were corroborated in an aquariumbased experiment showing constitutively higher anti-oxidant capacity of colonies with these alleles, particularly in the homozygous state. These genetic markers are located on different chromosomes and closely linked to a range of genes involved in bleachingassociated processes, such as thermal, hypoxic and oxidative stress, suggesting they are indicative of tolerance to a multitude of environmental perturbations.

Markers such as the ones identified in this study provide an opportunity to use environmental mapping to identify populations that are resistant to a range of environmental stressors. In Chapter 5, a spatial Bayesian belief network (BBN) model was developed to predict GBR-wide spatial distributions of allele frequencies at the antioxidant capacity locus C29226S281. A combination of long-term environmental monitoring data, allele frequency data, expert input and statistical evaluation was used to build the model, with the goal of refining prior beliefs and examining dependencies among environmental variables that are proxy indicators of selective forces on allele frequencies at locus C29226S281. The model predicts that a high allele frequency is correlated with poor water quality and large fluctuations in sea temperatures. The Bayesian simulation approach demonstrates that the synergism between highly fluctuating sea temperatures and high nitrate concentrations may be the primary driver in selecting alleles at this locus. High temperature fluctuation in isolation does not increase the probability of finding high allele frequencies. Consistent with this, spatial mapping of predicted allele frequencies reveals that increased anti-oxidant capacity alleles are most likely to be concentrated near the mouths of the Burdekin and Fitzroy Rivers, where nutrient levels are chronically high. Coupling GIS and BBN enables visualisation of the model output, specifically qualitative measurements of allele frequencies, enabling non-experts to explore and interpret complex interactions between environmental and genetic factors.

This thesis provides compelling evidence that the two loci identified are true QTLs associated with responses to bleaching-associated stressors. Correlations between the spatial distribution of allele frequencies and genotypic variation associated with bleaching tolerance at the loci indicate the existence of adaptive genetic diversity in current coral populations. These findings open up opportunities for novel coral reef management approaches, such as spatial mapping of stress tolerance for use in Marine Protected Area design, the identification of stress tolerant colonies for assisted migration and marker-assisted selective breeding to create more tolerant genotypes for restoration of denuded reefs.

Item ID: 46290
Item Type: Thesis (PhD)
Keywords: Acropora millepora, adaptation, allele frequency, alleles, climate change, coral bleaching tolerance, genetic variation, genetics, Great Barrier Reef, high resolution melting, pooled genotyping, population, resilience, single nucleotide polymorphism, SNP
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Capper, Roxana L., Jin, Young K., Lundgren, Petra B., Peplow, Lesa M., Matz, Mikhail V., and van Oppen, Madeleine J.H. (2015) Quantitative high resolution melting: two methods to determine SNP allele frequencies from pooled samples. BMC Genetics, 16. pp. 1-13.

Date Deposited: 09 Nov 2016 04:55
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060303 Biological Adaptation @ 34%
06 BIOLOGICAL SCIENCES > 0699 Other Biological Sciences > 069902 Global Change Biology @ 33%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 50%
96 ENVIRONMENT > 9603 Climate and Climate Change > 960399 Climate and Climate Change not elsewhere classified @ 50%
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