Advertisement

Coral Reefs

pp 1–12 | Cite as

Predicting the spatial distribution of allele frequencies for a gene associated with tolerance to eutrophication and high temperature in the reef-building coral, Acropora millepora, on the Great Barrier Reef

  • Young K. JinEmail author
  • Stuart Kininmonth
  • Petra B. Lundgren
  • Madeleine J. H. van Oppen
  • Bette L. Willis
Report

Abstract

In the face of unprecedented rates of environmental alterations, the necessity to predict the capacity of corals to respond adaptively in a complex ecological system is becoming increasingly urgent. Recent findings that bleaching-resistant Acropora millepora coral populations have high frequencies of specific alleles provide an opportunity to use spatial mapping of alleles to identify resistant populations. In this study, a Bayesian belief network (BBN) model was developed to predict the spatial distribution of allele frequencies for a specific locus associated with bleaching resistance in response to acute eutrophication during the summertime in A. millepora in the Palm Islands (Great Barrier Reef, Australia). The BBN model enabled the putative responses of populations investigated to be extrapolated to other ‘equivalent’ populations that were previously not surveyed due to constraints of time, cost and logistics. 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. The Bayesian simulation approach demonstrates that synergism between highly fluctuating temperatures and high nitrate concentrations may be the primary driver of selection for this locus. Consistently, spatial mapping of predicted allele frequencies reveals the tolerance allele is most likely to be concentrated in populations near the mouths of the Burdekin and Fitzroy Rivers. Corals from these river mouths are good candidates for assisted gene flow initiatives and also to restore reefs that are likely to be affected by eutrophication and ocean warming in the future. This approach opens up new opportunities for more efficient and effective coral reef management and conservation through direct intervention to ensure coral populations have the genetic diversity needed to optimise adaptation to rapid environmental change.

Keywords

Coral Bleaching Environmental stressor Eutrophication Sea surface temperature Bayesian belief network Allele frequency Assisted gene flow Coral reef restoration 

Notes

Acknowledgements

We thank L. M. Peplow and J. Doyle for their technical support. Funding for this project was supported by the Australian Institute of Marine Science (AIMS), the Australian Research Council Centre of Excellence, AIMS@JCU (James Cook University), and a JCU Graduate Research Scheme Grant to Y. K. Jin. SK acknowledges that this research was funded through the 2015–2016 BiodivERsA COFUND call for research proposals, with the national funders FORMAS.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2019_1873_MOESM1_ESM.docx (720 kb)
Supplementary file 1 (DOCX 719 kb)

References

  1. Anthony KRN, Marshall PA, Abdulla A, Beeden R, Bergh C, Black R, Eakin CM, Game ET, Gooch M, Graham NAJ, Green A, Heron SF, van Hooidonk R, Knowland C, Mangubhai S, Marshall N, Maynard JA, McGinnity P, McLeod E, Mumby PJ, Nystrom M, Obura D, Oliver J, Possingham HP, Pressey RL, Rowlands GP, Tamelander J, Wachenfeld D, Wear S (2015) Operationalizing resilience for adaptive coral reef management under global environmental change. Glob Change Biol 21:48–61CrossRefGoogle Scholar
  2. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci 110:1387–1392CrossRefPubMedPubMedCentralGoogle Scholar
  3. Brodie JE, McKergow LA, Prosser IP, Furnas M, Hughes AO, Hunter H (2003) Sources of sediment and nutrient exports to the Great Barrier Reef World Heritage Area. ACTFR Report No. 03/11, Australian Centre for Tropical Freshwater Research, James Cook University, TownsvilleGoogle Scholar
  4. Brodie J, Devlin M, Haynes D, Waterhouse J (2011) Assessment of the eutrophication status of the Great Barrier Reef lagoon (Australia). Biogeochemistry 106:281–302CrossRefGoogle Scholar
  5. Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal Complex Syst 1695:1–9Google Scholar
  6. Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262CrossRefGoogle Scholar
  7. De’ath G (2007) The spatial, temporal and structural composition of water quality of the Great Barrier Reef, and indicators of water quality and mapping risk. Report to the Marine and Tropical Sciences Research Facility. Reef and Rainforest Research Centre Limited, Cairns, Queensland, AustraliaGoogle Scholar
  8. De'ath G, Fabricius K (2008) Water quality of the Great Barrier Reef: distributions, effects on reef biota and trigger values for the protection of ecosystem health. Australian Institute of Marine Science, Townsville, Final Report to the Great Barrier Reef Marine Park Authority, p 104Google Scholar
  9. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B (Methodological) 39(1):1–22Google Scholar
  10. Devlin M, Waterhouse J, Taylor J, Brodie J (2001) Flood plumes in the Great Barrier Reef: spatial and temporal patterns in composition and distribution. GBRMPA Research Publication 68. Great Barrier Reef Marine Park Authority, TownsvilleGoogle Scholar
  11. Devlin MJ, McKinna LW, Alvarez-Romero JG, Petus C, Abott B, Harkness P, Brodie J (2012) Mapping the pollutants in surface riverine flood plume waters in the Great Barrier Reef, Australia. Mar Pollut Bull 65:224–235CrossRefGoogle Scholar
  12. Fabricius KE, Cooper TF, Humphrey C, Uthicke S, De’ath G, Davidson J, LeGrand H, Thompson A, Schaffelke B (2012) A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar Pollut Bull 65:320–332CrossRefGoogle Scholar
  13. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685CrossRefGoogle Scholar
  14. Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner SD, Hoegh-Guldberg O (2013) Limiting global warming to 2 degrees C is unlikely to save most coral reefs. Nat Clim Chang 3:165–170CrossRefGoogle Scholar
  15. Furnas M, Mitchell A (1996) Nutrient inputs into the central Great Barrier Reef (Australia) from subsurface intrusions of Coral Sea waters: a two-dimensional displacement model. Cont Shelf Res 16:1127–1148CrossRefGoogle Scholar
  16. Furnas M, Mitchell A, Skuza M, Brodie J (2005) In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar Pollut Bull 51:253–265CrossRefGoogle Scholar
  17. Furnas M, Alongi D, McKinnon D, Trott L, Skuza M (2011) Regional-scale nitrogen and phosphorus budgets for the northern (14 S) and central (17 S) Great Barrier Reef shelf ecosystem. Cont Shelf Res 31:1967–1990CrossRefGoogle Scholar
  18. Gagnaire P-A, Normandeau E, Côté C, Hansen MM, Bernatchez L (2012) The genetic consequences of spatially varying selection in the panmictic American eel (Anguilla rostrata). Genetics 190:725–736CrossRefPubMedPubMedCentralGoogle Scholar
  19. Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558CrossRefGoogle Scholar
  20. Harrell FE, Dupont C Jr (2018) Hmisc: Harrell miscellaneous. R package version 4.1–1.Google Scholar
  21. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshw Res 50:839–866Google Scholar
  22. Howells EJ, Berkelmans R, van Oppen MJH, Willis BL, Bay LK (2013) Historical thermal regimes define limits to coral acclimatization. Ecology 94:1078–1088CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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:e1500842CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kininmonth S, van Oppen MJH, Possingham HP (2010) Determining the community structure of the coral Seriatopora hystrix from hydrodynamic and genetic networks. Ecol Modell 221:2870–2880CrossRefGoogle Scholar
  25. Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172CrossRefPubMedPubMedCentralGoogle Scholar
  26. Larcombe P, Ridd P, Prytz A, Wilson B (1995) Factors controlling suspended sediment on inner-shelf coral reefs, Townsville, Australia. Coral Reefs 14:163–171CrossRefGoogle Scholar
  27. Lough JM (2007) Tropical river flow and rainfall reconstructions from coral luminescence: Great Barrier Reef, Australia. Paleoceanography 22(2)Google Scholar
  28. Le Corre V, Kremer A (2003) Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 164:1205–1219PubMedPubMedCentralGoogle Scholar
  29. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189CrossRefGoogle Scholar
  30. Lema KA, Willis BL, Bourneb DG (2012) Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78:3136–3144CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lema KA, Willis BL, Bourne DG (2014) Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ Microbiol 16:3345–3359CrossRefGoogle Scholar
  32. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Ann Rev Physiol 68(1):253–278CrossRefGoogle Scholar
  33. Lesser MP (2011) Coral Bleaching: Causes and Mechanisms. In: Dubinsky Z, Stambler N (eds) Coral Reefs: An Ecosystem in Transition. Springer, Netherlands, Dordrecht, pp 405–419CrossRefGoogle Scholar
  34. Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152CrossRefGoogle Scholar
  35. Little AF, Van Oppen MJ, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494CrossRefPubMedPubMedCentralGoogle Scholar
  36. Marcot BG, Steventon JD, Sutherland GD, McCann RK (2006) Guidelines for developing and updating Bayesian belief networks applied to ecological modeling and conservation. Can J For Res 36:3063–3074CrossRefGoogle Scholar
  37. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211(7):1050–1056CrossRefPubMedPubMedCentralGoogle Scholar
  38. Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc - R Soc London, B 236:311–324CrossRefGoogle Scholar
  39. Packett R, Dougall C, Rohde K, Noble R (2009) Agricultural lands are hot-spots for annual runoff polluting the southern Great Barrier Reef lagoon. Mar Pollut Bull 58:976–986CrossRefPubMedPubMedCentralGoogle Scholar
  40. Safaie A, Silbiger NJ, McClanahan TR, Pawlak G, Barshis DJ, Hench JL, Rogers JS, Williams GJ, Davis KA (2018) High frequency temperature variability reduces the risk of coral bleaching. Nat Commun 9:1671CrossRefPubMedPubMedCentralGoogle Scholar
  41. Santos HF, Carmo FL, Duarte G, Dini-Andreote F, Castro CB, Rosado AS, Van Elsas JD, Peixoto RS (2014) Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J 8:2272–2279CrossRefPubMedPubMedCentralGoogle Scholar
  42. Shashar N, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals - Evidence for coral-bacteria interactions. Mar Ecol Prog Ser 111:259–264CrossRefGoogle Scholar
  43. Su C, Andrew A, Karagas MR, Borsuk ME (2013) Using Bayesian networks to discover relations between genes, environment, and disease. BioData Min 6:6CrossRefPubMedPubMedCentralGoogle Scholar
  44. Thomas CD (2011) Translocation of species, climate change, and the end of trying to recreate past ecological communities. Trends Ecol Evol 26:216–221CrossRefPubMedPubMedCentralGoogle Scholar
  45. Thorburn PJ, Wilkinson SN, Silburn DM (2013) Water quality in agricultural lands draining to the Great Barrier Reef: a review of causes, management and priorities. Agric Ecosyst Environ 180:4–20CrossRefGoogle Scholar
  46. 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. Mol Ecol 20:4899–4914CrossRefPubMedPubMedCentralGoogle Scholar
  47. van Oppen MJH, Puill-Stephan E, Lundgren P, De'ath G, Bay LK (2014) First-generation fitness consequences of interpopulational hybridisation in a Great Barrier Reef coral and its implications for assisted migration management. Coral Reefs 33:607–611CrossRefGoogle Scholar
  48. Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret FE, Postle AD, Achterberg EP (2013) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:160–164CrossRefGoogle Scholar
  49. Wooldridge SA (2009) Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wooldridge SA, Brodie JE, Kroon FJ, Turner RDR (2015) Ecologically based targets for bioavailable (reactive) nitrogen discharge from the drainage basins of the Wet Tropics region, Great Barrier Reef. Mar Pollut Bull 97:262–272CrossRefPubMedPubMedCentralGoogle Scholar
  51. Wooldridge SA, Heron SF, Brodie JE, Done TJ, Masiri I, Hinrichs S (2017) Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 2. Mar Pollut Bull, A regional-scale predictive model for the Great Barrier Reef, AustraliaGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Australian Institute of Marine ScienceTownsvilleAustralia
  2. 2.Australian Research Council Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  3. 3.College of Science and EngineeringJames Cook UniversityTownsvilleAustralia
  4. 4.College of Marine and Environmental SciencesAIMS@JCU, Australian Institute of Marine Science, James Cook UniversityTownsvilleAustralia
  5. 5.Marine and Coastal Resources InstitutePrince of Songkla UniversityHat YaiThailand
  6. 6.School of Marine StudiesUniversity of the South PacificSuvaFiji
  7. 7.Centre for Ecology and Evolutionary SynthesisUniversity of OsloOsloNorway
  8. 8.Great Barrier Reef FoundationBrisbaneAustralia
  9. 9.School of BioSciencesThe University of MelbourneParkvilleAustralia

Personalised recommendations