The traits of corals that survived recent bleaching events
Led by: Dr Line Bay, AIMS
The past two years have seen unprecedented coral bleaching on the GBR but the consequences on biodiversity and genetic diversity are not yet known. This project will address the following questions: 1) Has bleaching resulted in a loss of genetic diversity in three coral species? 2) Do surviving populations contain genetic signatures of adaptation to bleaching temperatures? 3) What is the prevalence of heat tolerant photo-symbionts within surviving corals and in the environmental pool? 4) Are heat tolerant Symbiodinium communities and host genetic variants correlated with ambient environmental and recent bleaching conditions? High throughput genomic sequence variance analysis will identify genes in corals and Symbiodinium types associated with bleaching tolerance. Through correlations with environmental variables we will develop a spatially explicit understanding of the distribution and abundance of stress tolerant coral genes and symbionts (in hospite and free-living) to identify key coral populations for protection, key reefs for resilience management and potential breeding stock for use in reef restoration activities.
The Great Barrier Reef experienced extensive bleaching related coral mortality across the Northern (N) and Central (C) GBR sectors in 2016-2017. Heritable genetic variation associated with tolerance to higher temperatures exists in some populations1, and supports the hypothesis that adaptation to changing environmental conditions is possible2,3. However, the rate and extent of temperature adaptation is unknown, and we currently have a poor understanding of how bleaching events affect the genetics and adaptability of natural coral populations4,5.
Genetic variation underpins the potential scope for adaption of natural populations and maintenance of genetic diversity is a key objective for biodiversity conservation and management6. Functional or adaptive diversity is a subset of total genetic diversity and describes variants of genes that are directly associated with tolerance and survival (i.e., putative adaptive loci PALs). The knowledge on functional genetic variation for thermal tolerance is increasing for corals around the world1,7,8, however, it is not yet clear whether survivors from natural bleaching events possess PALs that enable them to withstand higher temperatures that are fast becoming the norm on our reefs.
The health and stress tolerance of corals is strongly influenced by the genetic identity of the photo-symbionts they host in their tissues (i.e., types of Symbiodinium spp). An increase in the abundance of rare Symbiodinium types following disturbance can rapidly (over weeks to months) promote survival and enhanced temperature tolerance by ~1.5oC9,10,14,15. Types, including those from Symbiodinium clade D, have been identified as important for corals’ temperature tolerance and survival11,12. Extreme environments may select for stress tolerant coral individuals16,17 possibly through associations with more stress tolerant symbionts. As most corals acquire Symbiodinium from an environmental pool anew in each generation14, the environmental pool may thus be an important source of temperature tolerant symbionts. Developing a spatially explicit understanding of the distribution and abundance of stress tolerant coral PALs and symbionts (in hospite and free-living) will help identify key hard coral populations for protection, key reefs for resilience management and as potential breeding stock for use in future coral reef restoration activities.
- Identification of genetic variants (PALs) that underpin bleaching susceptibility
Existing sample collections from the Central GBR 2017 bleaching event will be used to identify functional genetic variation associated with bleaching susceptibility in the branching coral Acropora millepora (Figure 1b). This species displayed extensive variation in bleaching within and among reefs (necessary for this analysis) and was sampled in March at the height of the 2017 event. Gene variants across the coral genome will be associated with acute bleaching severity to identify functional PALs for bleaching/heat tolerance. Combined with published putative tolerance loci for other species and life stages1,7,8 these data will provide a panel of functional genetic diversity for bleaching tolerance that will be applied across species. This approach may extend to alternative species with variable life-history characteristics, including corals with vertical transmission of symbionts (Stylophora pistillata) or different growth morphologies (Porites lutea).
- Estimates of total and adaptive genetic diversity in surviving corals
Surviving colonies from three coral species with different bleaching sensitivities (Acropora millepora, A. hyacinthus and A. tenuis, Figure 1a) from the Central and Northern GBR will be used to test whether the frequency of genetic variants at tolerance loci varies between reefs that experienced different levels of heat exposure and reef wide bleaching. The criteria for reef selection will occur through collaboration among the three proposed NESP projects (see links to other projects section). Coral species selection followed discussions with GBRMPA, the AIMS monitoring team and Prof. Mumby (i.e., ecological importance of branching corals form habitat structure and are fast growing, thus important for recovery of damaged reefs). Also vitally important are the extensive prior sample collections of these three species at AIMS, and the genomic resources for these species currently being published by GBRF’s ReFuGe 2020 project. Comparisons with existing pre-bleaching samples (spanning latitudes and shelf positions collected between 1997 and 2014 – Figure 1b) will identify whether overall genetic diversity has declined and whether the frequency of gene variants at tolerance loci has changed among reefs. This will reveal if surviving corals on temperature stressed reefs have responded adaptively to bleaching through increases in the frequencies of PALs.
- In depth analysis of the composition of Symbiodinium communities in corals and the environment
New and existing sample collections of multiple coral species from across the GBR will be used to determine the distribution and abundance of temperature tolerant symbionts. We will use highly sensitive next generation sequencing methods to get a full picture of the Symbiodinium diversity within corals before and after mass bleaching, including highly abundant and background (i.e., rare) symbionts. We will also identify the composition of free-living sediment-associated Symbiodinium communities available for uptake by corals including the distribution and abundance of predicted heat tolerant types. This will identify reservoirs of stress tolerant symbionts available for uptake post-catastrophic bleaching.
- Environmental drivers of the prevalence of coral host genetic heat tolerance loci and stress-tolerant symbionts across the GBR
We will use multivariate analyses (e.g. Bayesian generalized non-linear models) to identify correlations of total and adaptive coral genetic diversity (PALs), with in hospite Symbiodinium communities in pre- and post-bleaching samples and environmental pools of Symbiodinium with over 20 environmental drivers available from eAtlas and other data repositories. The identification of which environmental drivers are important for the discovery of reefs and coral populations with a high abundance of PALs and will assist in the identification of important reefs for protection, connectivity and potential breeding stock for future restoration activities.
1) RAD-seq next generation sequencing of existing acute bleaching samples of A. millepora for the identification of loci associated with heat tolerance. 2) RAD-seq of coral host genetic variation and Amplicon-seq of Symbiodinium communities in 15 – 20 pre – bleaching colonies in of A. millepora, A. tenuis and A. hyacinthus from each of 18 reefs distributed across environmental gradients in the Central and Northern GBR Sectors. The collection of post-bleaching samples of the same species and reefs as above and coral and Symbiodinium genetic analysis of these samples as above. 2) New sediment collections from the Central and Northern GBR (3 samples each from 30 reefs) and Amplicon-seq of Symbiodinium communities in these samples.
Out of scope:
1) New collections from the Southern GBR. 2) Prokaryotic or physiological characterisation of coral samples. The new samples collected here will be stored in a manner that will enable these analyses to be undertaken in the future.
Details of related prior research
Prior data suggests that environmental drivers of dominant coral associated18 and free-living symbiont genetic diversity15 can be detected and that they are distinct among reefs and for coral associated and free-living life stages. Previous investigations of a smaller number of genetic loci for A. millepora and A. tenuis across the GBR suggest that pre-bleaching genetic diversity was high19,20 and sufficient to enable adaptation to increasing temperatures but that bleaching events will erode this diversity potentially impeding future adaptation to temperature5. Existing data from studies on coral reefs from around the world will be incorporated where possible, to enable the genetic tools and outputs to be applied to reefs beyond the GBR.
Links to other research and/or the work of other Hubs
This proposal forms a natural extension and a significant value-add to NESP 3.3.1 that quantified bleaching and sampled Acropora millepora, A. tenuis and four other species in the Central GBR in March and Sep 2017 but does not include the genetic analyses proposed here. The current proposal is completely aligned with NESP 4.2 and 4.5 TWQ in this RPv4. The seamless collaboration among these three new proposals facilitates the comparison of corals on reefs that experienced strong warming to those that did not. Host genetic and symbiont traits for which strong environmental drivers can be identified will be spatially extrapolated and fed into Mumby’s resilience model (Figure 2). This proposal also builds on the results from two projects that examine a) the pre-bleaching genetic structure of A. tenuis across inshore Central GBR (Accelerate Partnerships grant: Ragan, Beeden, …and van Oppen) and b) the utility of (pre-bleaching) gene flow estimates for A. tenuis in resilience mapping (GBRF: Riginos, Bay, Mumby et al). The data from both studies will be used in the pre-bleaching analysis of A. tenuis proposed here. This project is also linked with the GBR Legacy expedition in Nov – Dec 2017 (www.greatbarrierreeflegacy.org). AIMS has scientists on this expedition that will visit up to 18 reefs in the Northern GBR sector. We are directly involved in the reef selection and will use this opportunity to sample Northern GBR corals and sediments proposed here representing a vessel hire saving of 21 days @ $4000 = $84K. This project compliments AIMS internally funded work on assisted gene flow that tests whether cross breeding between northern warm adapted and central cooler adapted corals can produce more temperature tolerant young.
Summary of how it is expected that the research will be applied to inform decision-making and on-ground action.
Host genetic variation, in hospite and environmental Symbiodinium community composition associated with bleaching tolerance are key attributes that affect the resilience of populations on the GBR. It is expected our results will:
- Inform the conservation status of hyacinthus based on current estimates of genetic diversity.
- Reveal the vulnerability and resilience of coral species based on functional and neutral genetic diversity and their symbiont associations.
- Contribute to identifying reef locations for targeted management actions including spatial protection and potential future restoration activities.
This research will value-add to GBR monitoring programs arising from RIMRep by identifying corals that are heat stress tolerant, and those that aren’t. This will allow monitoring programs to measure the relative contributions of heat tolerant and heat stressed taxa to a given coral assemblage to allow the identification of GBR reefs at risk of future bleaching. The translation of this project into RIMRep will occur through Dr Beeden.
1. Dixon GB, Davies SW, Aglyamova G V, Meyer E, Bay LK, Matz M V (2015) Genomic determinants of coral heat tolerance across latitudes. Science (80- ) 348:1460–1462
2. Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral reefs 8:155–162
3. Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA (2016) Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob Chang Biol
4. van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci 112:2307–2313
5. Matz M V, Treml EA, Aglyamova G V, van Oppen MJH, Bay LK (2017) Adaptive pathways of coral populations on the Great Barrier Reef. bioRxiv 114173
6. Frankham R, Ballou JD, Ralls K, Eldridge M, Dubash MR, Fenster CB, Lacy RC, Sunnucks P (2017) Genetic management of fragmented animal and plant populations.
7. Jin YK, Lundgren P, Lutz A, Raina J-B, Howells EJ, Paley AS, Willis BL, van Oppen MJH (2016) Genetic markers for antioxidant capacity in a reef-building coral. Sci Adv 2:1–7
8. Bay RA, Palumbi SR (2014) Multilocus adaptation associated with heat resistance in reef-building corals. Curr Biol 24:2952–2956
9. Bay LK, Doyle J, Logan M, Berkelmans R (2016) Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. R Soc Open Sci 3:1–10
10. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc R Soc B Biol Sci 273:2305–2312
11. Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT, Warner ME, Ralph PJ (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381
12. Quigley KM, Willis BL, Bay LK. (2016) Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis. R. Soc. open sci. 3: 160471. http://dx.doi.org/10.1098/rsos.160471
13. Quigley KM, Davies SW, Kenkel CD, Willis BL, Matz M V, Bay LK (2014) Deep-sequencing method for quantifying background abundances of Symbiodinium types: exploring the rare Symbiodinium biosphere in reef-building corals. PLoS One 9:e94297
14. Quigley K, Willis B, Bay L (2017) Heritability of the Symbiodinium community in vertically-and horizontally-transmitting broadcast spawning corals. Sci Rep 7:8219
15. Quigley K, Bay LK, Willis B (In Prep) Geographic variation in temperature and water quality drive sediment associated Symbiodinium communities and impacts symbiont uptake and fitness in juvenile acroporid corals
16. Camp EF, Nitschke MR, Rodolfo-Metalpa R, Houlbreque F, Gardner SG, Smith DJ, Zampighi M, Suggett DJ (2017) Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci Rep 7:
17. van Oppen MJH, Bongaerts P, Frade PR, Peplow LM, Boyd SE, Nim HT, Bay LK (in review) Adaptation to reef habitats through selection on the coral animal and its associated microbiome. Science Advances
18. Cooper TF, Berkelmans R, Ulstrup KE, Weeks S, Radford B, Jones AM, Doyle J, Canto M, O’Leary RA, van Oppen MJH (2011) Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLoS One 6:e25536
19. Lukoschek V, Riginos C, van Oppen MJH (2016) Congruent patterns of connectivity can inform management for broadcast spawning corals on the Great Barrier Reef. Molecular Ecology 25:3065–3080
20. van Oppen MJH, Peplow LM, Kininmonth S, Berkelmans R (2011) Historical and contemporary factors shape the population genetic structure of the broadcast spawning coral, Acropora millepora, on the Great Barrier Reef. MolEcol 20:4899-4914
NESP 2017 Research Priority Alignment
NESP Priority Theme 3: Natural resource management improvements based on sound understanding of the status and long-term trends of priority species and systems.
This project will inform the following Research Priorities:
- Identify and trial practical methods to improve reef resilience, such as the transplantation of coral and coral genetics.
- Identify locally or regionally specific management interventions to achieve or maintain realistic desired states for tropical environmental, social, cultural and economic values.
- Develop and implement better tools, including spatial information, to support the prioritisation of on-ground investments and interventions and assess their success.
- Explore the opportunities for citizen science and Indigenous participation to improve coral restoration awareness and outcomes.
Coral bleaching; Genetic diversity; Connectivity; Putatively adaptive loci; Protection.
This project is jointly funded through AIMS and the Australian Government’s National Environmental Science Programme.
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