Interspecific Hybridization As a Tool for Enhancing Climate Resilience of Reef
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Interspecific hybridization as a tool for enhancing climate resilience of reef- building corals Wing Yan Chan ORCID: 0000-0001-9875-6903 Submitted in total fulfilment of the requirements of the degree of Doctor of Philosophy Dec 2018 School of BioSciences The University of Melbourne & The Australian Institute of Marine Science Declaration This is to confirm that: 1. this thesis comprises only of my original work towards the PhD, except where indicated in the preface; 2. due acknowledgement has been made in the text to all other material used; 3. the thesis is under 100,000 words, exclusive of tables, maps, bibliographies and appendices. Signed: Date: 14 Dec 2018 ii Abstract The world’s coral reefs are facing unprecedented changes in temperature and carbonate chemistry caused by the increasing concentration of atmospheric CO2. Recent massive loss of corals across the world suggests that their rate of adaptation and/or acclimatization is unlikely fast enough to keep pace with climate change. This thesis examines interspecific hybridization as a conservation management tool to develop coral stock with enhanced climate resilience and adaptive potential. I start this thesis by discussing the potential benefits and risks of hybridization, and exploring the legal framework associated with hybrids and hybridization (chapter 1). Next, I present the results of interspecific fertilization trials, as well as stress experiments on coral larvae (chapter 2) and recruits (chapter 3) conducted to compare fitness of purebred and hybrid offspring. To understand mechanisms that may have contributed to the observed holobiont fitness differences, bacterial and algal endosymbiont communities associated with these corals were examined using 16S rRNA gene and ITS2 metabarcoding (chapter 4), and coral host gene expression patterns were assessed using RNA sequencing (chapter 5). The following findings and key conclusions have emerged from this thesis. Firstly, all four tested pairs of Acropora species from the Great Barrier Reef were cross-fertile, but the degree of prezygotic barriers varied (chapters 2, 3). In both years in which hybridization was attempted (2015, 2016), the majority of the target species pairs had no or limited temporal isolation (i.e., similar spawning dates and times). The only clear temporal isolation was between the ‘early spawner’ A. tenuis and the ‘late spawner’, A. loripes, although their gametes were still compatible. Gametic incompatibility varied between species pairs and the year of hybridization tests (which involved the same coral species collected from different locations). Levels of cross fertility ranged iii from no prezygotic barriers in both directions (chapter 3), to successful fertilization in one direction only, and in once case, unsuccessful fertilization in both directions (chapter 2). The observed variations in gametic incompatibility may be a consequence of differences in gamete- gamete recognition molecules. Secondly, hybrid corals were generally as fit as or more fit than parental purebred species (chapters 2, 3). At the embryonic stage, hybrid embryos developed normally and at similar rates as purebred embryos (chapter 3). At the larval stage, survival and settlement of hybrid larvae under 10 days exposure to ambient and elevated temperatures were mostly similar to that of purebreds, but higher than purebreds in a small number of cases (chapter 2). Hybrid recruits also had similar algal endosymbiont uptake rates and photochemical efficiency as that of purebred recruits (chapter 3). Under seven months exposure to ambient and elevated temperature and pCO2 conditions, however, some hybrids showed higher survival and grew larger than parental purebred species under both conditions (chapter 3). Overall, maternal effects were observed in hybrids of the A. tenuis x A. loripes cross (i.e., hybrids had similar fitness to the maternal parent species), and over-dominance in hybrids of the A. sarmentosa x A. florida cross (i.e., hybrids had higher fitness than both parental species), with some variations between traits and treatment conditions. While fitness of these hybrids in the field and their reproductive potential are yet to be investigated, these findings provide proof-of concept that interspecific hybridization may enhance coral resilience and this approach may therefore increase the success of coral reef restoration programs. Thirdly, the observed holobiont fitness differences between offspring groups were likely due to host-related factors (chapter 5), but not the microbial communities associated with these corals iv (chapter 4). No differences in the bacterial and microalgal endosymbiont community composition were found between hybrid and purebred corals (chapter 4). Microbial communities of these seven months old recruits were highly diverse and lacked host specificity. Winnowing of the communities occurred over time, resulting in less diverse microbial communities that differed between the two species pair crosses by two years of age. Transcriptome-wide gene expression analysis for the A. tenuis x A. loripes cross showed clear maternal patterns (chapter 5), consistent with the observed fitness results. Hybrids had similar gene expression patterns to their material parents, and only up to 10 differentially expressed genes were observed between them. In contrast, hundreds of genes were found differentially expressed between purebred A. tenuis and A. loripes, as well as between hybrids that had different maternal parents. Due to insufficient material available for the A. sarmentosa x A. florida cross at the end of the seven months aquarium experiment, transcriptome analysis was not conducted for this cross. Findings from this thesis support the notion that interspecific hybridization may improve coral resilience and facilitate adaptation to climate change. Further, as genetic diversity within species is predicted to decline as a consequence of high mortality disturbances such as mass bleaching events, interspecific hybridization can be used to restore losses in genetic diversity. If future studies can demonstrate high fitness of hybrid corals in the field and in advanced generations, hybrid corals may serve as a stock for reef managers for reseeding degraded reefs and/or enhancing resilience of healthy reefs. v Preface Two out of the six chapters of this thesis (chapters 1, 4) have been submitted to peer-review journals and are under review. Chapter 2 and Chapter 3 have been published in a peer-review journal. Details of contribution for each manuscript are outlined below. Chapter 1 Chan WY, Hoffmann AA, van Oppen MJH. (2018). Hybridization as a conservation management tool in the Anthropocene. (Revision submitted to Conservation Letters). All authors contributed to conceptual development and the final edited version of the manuscript. WYC and MvO wrote the manuscript, and WYC and AH designed the decision tree. WYC contributed to about 70% of this work. Chapter 2 Chan WY, Peplow LW, van Oppen MJH. (2019). Interspecific gamete compatibility and hybrid larval fitness in reef-building corals: Implications for coral reef restoration. Scientific Reports 9, 4757. doi:10.1038/s41598-019-41190-5. WYC and MvO designed the experiment. WYC and LP conducted the experiment and collected the data. WYC undertook data analyses. WYC and MvO wrote the manuscript. Approximately 70% of the work was completed by WYC. vi Chapter 3 Chan WY, Peplow LM, Menéndez P, Hoffmann AA, van Oppen MJH. (2018). Interspecific hybridization may provide novel opportunities for coral reef restoration. Frontiers in Marine Science 5. doi:10.3389/fmars.2018.00160. WYC, MvO, LP, AH designed the experiment. MvO developed the concept for this study. WYC and LP conducted the experiment and collected the data. PM, WYC and AH undertook statistical analyses. WYC and MvO wrote the manuscript and all authors contributed to the final edited version of the manuscript. WYC contributed to about 65% of the work. Chapter 4 Chan WY, Peplow LM, Menéndez P, Hoffmann AA, van Oppen MJH. (2018). The roles of age, parentage and environment on bacterial and algal endosymbiont communities in Acropora corals. (Submitted to Molecular Ecology). WYC, MvO, LP, and AH designed the experiment. WYC and LP performed the experiment. LP carried out the laboratory work. PM, WYC and AH undertook statistical analyses. WYC and MvO wrote much of the manuscript and all authors contributed to the final edited version of the manuscript. Approximately 65% of this work was performed by WYC. vii Other relevant publications during candidature Carr H, et. al., Chan WY. (2019). The Aichi Biodiversity Targets: Achievements for marine conservation and priorities beyond 2020. (Submitted to PeerJ). Chan WY, and Eggins SM. (2017). Calcification responses to diurnal variation in seawater carbonate chemistry by the coral Acropora formosa. Coral Reefs 36, 763–772. doi:10.1007/s00338-017-1567-8. van Oppen MJH, et al., Chan WY. (2017). Shifting paradigms in restoration of the world’s coral reefs. Global Change Biology 23, 3437–3448. doi:10.1111/gcb.13647. Froehlich MB, Chan WY, Tims SG, Fallon SJ, and Fifield LK. (2016). Time-resolved record of 236U and 239,240Pu isotopes from a coral growing during the nuclear testing program at Enewetak Atoll (Marshall Islands). J Environ Radioact 165, 197–205. doi:10.1016/j.jenvrad.2016.09.015. viii Acknowledgment I would like to express my heartfelt gratitude to my supervisors, Madeleine van Oppen and Ary Hoffmann, for their guidance and support during my candidature.