Advertisement

Coral Reefs

pp 1–16 | Cite as

A seascape genetic analysis of a stress-tolerant coral species along the Western Australian coast

  • R. D. Evans
  • N. M. Ryan
  • M. J. Travers
  • M. Feng
  • Y. Hitchen
  • W. J. Kennington
Report

Abstract

Genetic diversity and connectivity are key factors in determining a population’s resilience to future disturbance. This is especially relevant to corals, which are in global decline due to increasing frequency and strength of thermal anomalies and severe tropical cyclones. While many studies have investigated genetic diversity and population structure in corals, they focused on species being removed at the greatest rate from coral reefs, acroporids and pocilloporids, and it is unclear whether the patterns observed in these species reflects those found in more resilient species. Here, we use microsatellite markers and two Lagrangian models with differing resolutions, to investigate population structure in a stress-tolerant coral survivor Cyphastrea microphthalma, Family Merulinidae, along the north-western Australian coastline. We found evidence of four genetic clusters with some level of admixture among them. However, while there was evidence of population structure within the intensively sampled Pilbara region, the patterns of connectivity differed to those reported previously. WA populations of C. microphthalma were also characterised by lower levels of genetic diversity at higher latitudes. High- and moderate-resolution Lagrangian models did not significantly predict regional-scale genetic connectivity across the Pilbara and Ningaloo (500 km). Although the high-resolution model explained an order of magnitude more genetic variation, suggesting model resolution and resolving coastal processes are important. Over broad spatial scales (nearly 2000 km), all moderate-resolution model particle release durations significantly predicted the genetic differentiation, although over-water distance best-predicted the genetic distance across this spatial scale. This study improves the understanding of connectivity in this region by focusing on a stress-tolerant species incorporating a spatially more intensive sampling effort than previous coral studies. It also shows that further development of Lagrangian models is required, such as inclusion of multi-generational stepwise models and larval behaviour, to improve predictions of connectivity for this coral species in this region.

Keywords

Cyphastrea microphthalma Seascape genetics Lagrangian models Western Australia Coral bleaching 

Notes

Acknowledgements

We would like to thank Jonathan Kool for his assistance with the moderate-resolution model. Also Luke Thomas, Rachel Marshall, DBCA Exmouth and Shark Bay district staff, Shark Bay Department of Fisheries, and the crew of Keshi Mer for field assistance. We would also like to thank Rachel Binks and Zoe Richards for helpful comments. The helpful comments of three referees have led to an improved manuscript. This research was funded by the Chevron-operated Wheatstone Project and the Woodside-operated Pluto Project for the State Environmental Offsets Program administered by DBCA. The Wheatstone Project is a joint venture between Australian subsidiaries of Chevron, Kuwait Foreign Petroleum Exploration Company (KUFPEC), Woodside Petroleum Limited and Kyushu Electric Power Company, together with PE Wheatstone Pty Ltd. (part owned by TEPCO). Kimberley samples were collected by MT as part of the Lalang-garram Camden Sound Marine Park Project funded by the WA State Government Kimberley Science and Conservation Strategy. For cultural advice, permissions and field assistance, we thank the Dambimangari people, particularly Francis Woolagoodja and Peter McCumstie.

Compliance with ethical standards

All samples were collected under Western Australian Department of Fisheries Exemption No. 2491, and Department of Biodiversity, Conservation and Attractions Fauna Collection Permit No. SC001362.

Conflict of interest

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

Supplementary material

338_2018_1751_MOESM1_ESM.docx (233 kb)
Supplementary material 1 (DOCX 232 kb)

References

  1. Ampou EE, Johan O, Menkes CE, Niño F, Birol F, Ouillon S, Andréfouët S (2017) Coral mortality induced by the 2015–2016 El-Niño in Indonesia: the effect of rapid sea level fall. Biogeosciences 14:817–826CrossRefGoogle Scholar
  2. Ayre DJ, Hughes TP (2004) Climate change, genotypic diversity and gene flow in reef-building corals: Gene flow in reef building corals. Ecol Lett 7:273–278CrossRefGoogle Scholar
  3. Babcock RC, Wills BL, Simpson CJ (1994) Mass spawning of corals on a high latitude coral reef. Coral Reefs 13:161–169CrossRefGoogle Scholar
  4. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571CrossRefGoogle Scholar
  5. Bauman AG, Baird AH, Cavalcante GH (2011) Coral reproduction in the world’s warmest reefs: southern Persian Gulf (Dubai, United Arab Emirates). Coral Reefs 30:405–413CrossRefGoogle Scholar
  6. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological) 57:289–300Google Scholar
  7. Binks R, Byrne M, McMahon K, Pitt G, Murray K, Evans RD (2018) Habitat discontinuities form strong barriers to gene flow among mangrove populations, despite the capacity for long distance dispersal. Divers Distrib.  https://doi.org/10.1111/ddi.12851 Google Scholar
  8. Boyd PW, Lennartz ST, Glover DM, Doney SC (2015) Biological ramifications of climate-change-mediated oceanic multi-stressors. Nature Climate Change 5:71–79CrossRefGoogle Scholar
  9. Bryant EH, Meffert LM (1993) The effect of serial founder-flush cycles on quantitative genetic variation in the housefly. Heredity 70:122–129CrossRefGoogle Scholar
  10. Burt JA, Smith EG, Warren C, Dupont J (2015) An assessment of Qatar’s coral communities in a regional context. Mar Pollut Bull 105:473–479CrossRefPubMedGoogle Scholar
  11. Cahill AE, Levinton JS (2016) Genetic differentiation and reduced genetic diversity at the northern range edge of two species with different dispersal modes. Mol Ecol 25:515–526CrossRefPubMedGoogle Scholar
  12. Chapuis M-P, Estoup A (2006) Microsatellite Null Alleles and Estimation of Population Differentiation. Mol Biol Evol 24:621–631CrossRefPubMedGoogle Scholar
  13. Chassignet EP, Hurlburt HE, Smedstad OM, Halliwell GR, Hogan PJ, Wallcraft AJ, Baraille R, Bleck R (2007) The HYCOM (HYbrid Coordinate Ocean Model) data assimilative system. J Mar Syst 65:60–83CrossRefGoogle Scholar
  14. Commonwealth of Australia (2006). A guide to the integrated marine and coastal regionalisation of Australia version 4.0. Canberra: Department of the Environment and HeritageGoogle Scholar
  15. Cooke GM, Schlub TE, Sherwin WB, Ord TJ (2016) Understanding the Spatial Scale of Genetic Connectivity at Sea: Unique Insights from a Land Fish and a Meta-Analysis. PLOS ONE 11:e0150991.  https://doi.org/10.1371/journal.pone.0150991 CrossRefPubMedPubMedCentralGoogle Scholar
  16. DiBattista JD, Travers MJ, Moore GI, Evans RD, Newman SJ, Feng M, Moyle SD, Gorton RJ, Saunders T, Berry O (2017) Seascape genomics reveals fine-scale patterns of dispersal for a reef fish along the ecologically divergent coast of Northwestern Australia. Mol Ecol 26:6206–6223CrossRefPubMedGoogle Scholar
  17. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20CrossRefGoogle Scholar
  18. Durand E, Chen C, François O (2009) Comment on “On the inference of spatial structure from population genetics data”. Bioinformatics 25:1802–1804CrossRefPubMedGoogle Scholar
  19. Ezer T, Heyman WD, Houser C, Kjerfve B (2011) Modeling and observations of high-frequency flow variability and internal waves at a Caribbean reef spawning aggregation site. Ocean Dyn 61:581–598CrossRefGoogle Scholar
  20. Feng M (2003) Annual and interannual variations of the Leeuwin Current at 32°S. J Geophys Res 108:3355.  https://doi.org/10.1029/2002JC001763 CrossRefGoogle Scholar
  21. Feng M, McPhaden MJ, Xie S-P, Hafner J (2013) La Niña forces unprecedented Leeuwin Current warming in 2011. Sci Rep 3:1277.  https://doi.org/10.1038/srep01277 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Feng M, Colberg F, Slawinski D, Berry O, Babcock R (2016) Ocean circulation drives heterogeneous recruitments and connectivity among coral populations on the North West Shelf of Australia. J Mar Syst 164:1–12CrossRefGoogle Scholar
  23. Figueiredo J, Baird AH, Harii S, Connolly SR (2014) Increased local retention of reef coral larvae as a result of ocean warming. Nature Climate Change 4:498–502CrossRefGoogle Scholar
  24. Foster NL, Paris CB, Kool JT, Baums IB, Stevens JR, Sanchez JA, Bastidas C, Agudelo C, Bush P, Day O, Ferrari R, Gonzalez P, Gore S, Guppy R, McCartney MA, McCoy C, Mendes J, Srinivasan A, Steiner S, Vermeij MJA, Weil E, Mumby PJ (2012) Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow: Caribbean coral connectivity. Mol Ecol 21:1143–1157CrossRefPubMedGoogle Scholar
  25. Fromont J, Abdul Wahab M, Gomez O, Ekins M, Grol M, Hooper J (2016) Patterns of Sponge Biodiversity in the Pilbara, Northwestern Australia. Diversity 8:21CrossRefGoogle Scholar
  26. Gardner MG, Fitch AJ, Bertozzi T, Lowe AJ (2011) Rise of the machines - recommendations for ecologists when using next generation sequencing for microsatellite development: Microsatellite development with NGS. Mol Ecol Resour 11:1093–1101CrossRefPubMedGoogle Scholar
  27. Giles EC, Saenz-Agudelo P, Hussey NE, Ravasi T, Berumen ML (2015) Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea. Ecol Evol 5:2487–2502CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gilmour JP, Smith LD, Brinkman RM (2009) Biannual spawning, rapid larval development and evidence of self-seeding for scleractinian corals at an isolated system of reefs. Marine Biology 156:1297–1309CrossRefGoogle Scholar
  29. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an Isolated Coral Reef System Following Severe Disturbance. Science 340:69–71CrossRefPubMedGoogle Scholar
  30. Gilmour J, Speed CW, Babcock R (2016a) Coral reproduction in Western Australia. PeerJ 4:e2010CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gilmour JP, Underwood JN, Howells EJ, Gates E, Heyward AJ (2016b) Biannual Spawning and Temporal Reproductive Isolation in Acropora Corals. PLOS ONE 11:e0150916CrossRefPubMedPubMedCentralGoogle Scholar
  32. Goudet J (1995) FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics. J Hered 86:485–486CrossRefGoogle Scholar
  33. Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97CrossRefPubMedGoogle Scholar
  34. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. Coral reef ecosystems. Dubinsky Z (eds) Elsevier, Amsterdam, pp 133–207Google Scholar
  35. Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 122–134Google Scholar
  36. Heron SF, Maynard JA, van Hooidonk R, Eakin CM (2016) Warming Trends and Bleaching Stress of the World’s Coral Reefs 1985–2012. Sci Rep 6:38402.  https://doi.org/10.1038/srep38402 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hoey A, Howells E, Johansen J, Hobbs J-P, Messmer V, McCowan D, Wilson S, Pratchett M (2016) Recent Advances in Understanding the Effects of Climate Change on Coral Reefs. Diversity 8:12.  https://doi.org/10.3390/d8020012 CrossRefGoogle Scholar
  38. Howells EJ, Abrego D, Vaughan GO, Burt JA (2015) Coral spawning in the Gulf of Oman and relationship to latitudinal variation in spawning season in the northwest Indian Ocean. Scientific Reports 4Google Scholar
  39. Howells EJ, Ketchum RN, Bauman AG, Mustafa Y, Watkins KD, Burt JA (2016) Species-specific trends in the reproductive output of corals across environmental gradients and bleaching histories. Mar Pollut Bull 105:532–539CrossRefPubMedGoogle Scholar
  40. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, Kuo C, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefPubMedGoogle Scholar
  41. Ivanova NV, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA: Technical note. Mol Ecol Notes 6:998–1002CrossRefGoogle Scholar
  42. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  43. Johnson MS, Black R (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol 70:157–164CrossRefGoogle Scholar
  44. Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325CrossRefGoogle Scholar
  45. Kawecki TJ (2008) Adaptation to Marginal Habitats. Annu Rev Ecol Evol Syst 39:321–342CrossRefGoogle Scholar
  46. Kool JT, Nichol SL (2015) Four-dimensional connectivity modelling with application to Australia’s north and northwest marine environments. Environ Model Softw 65:67–78CrossRefGoogle Scholar
  47. Lafratta A, Fromont J, Speare P, Schönberg CHL (2016) Coral bleaching in turbid waters of north-western Australia. Mar Freshw Res 68:65–75Google Scholar
  48. Lefebvre A, Ellien C, Davoult D, Thiébaut E, Salomon J (2003) Pelagic dispersal of the brittle-star Ophiothrix fragilis larvae in a megatidal area (English Channel, France) examined using an advection/diffusion model. Estuar Coast Shelf Sci 57:421–433CrossRefGoogle Scholar
  49. Legendre P, Fortin M-J (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data: Spatial Analysis of genetic data. Molecular Ecology Resources 10:831–844CrossRefPubMedGoogle Scholar
  50. Liggins L, Treml EA, Possingham HP, Riginos C (2016) Seascape features, rather than dispersal traits, predict spatial genetic patterns in co-distributed reef fishes. J Biogeogr 43:256–267CrossRefGoogle Scholar
  51. McClanahan TR, Graham NA, Darling ES (2014) Coral reefs in a crystal ball: predicting the future from the vulnerability of corals and reef fishes to multiple stressors. Curr Opin Environ Sustain 7:59–64CrossRefGoogle Scholar
  52. McLean DL, Langlois TJ, Newman SJ, Holmes TH, Birt MJ, Bornt KR, Bond T, Collins DL, Evans SN, Travers MJ, Wakefield CB, Babcock RC, Fisher R (2016) Distribution, abundance, diversity and habitat associations of fishes across a bioregion experiencing rapid coastal development. Estuarine, Coastal and Shelf Science 178:36–47CrossRefGoogle Scholar
  53. Meglécz E, Costedoat C, Dubut V, Gilles A, Malausa T, Pech N, Martin J-F (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26:403–404CrossRefPubMedGoogle Scholar
  54. Meirmans PG (2012) The trouble with isolation by distance: news and views: opinion. Molecular Ecology 21:2839–2846CrossRefPubMedGoogle Scholar
  55. Messmer V, Jones GP, Munday PL, Planes S (2012) Concordance between genetic and species diversity in coral reef fishes across the Pacific Ocean biodiversity gradient: parallel patterns in species and genetic diversity. Evolution 66:3902–3917CrossRefPubMedGoogle Scholar
  56. Miller KJ, Ayre DJ (2008) Protection of Genetic Diversity and Maintenance of Connectivity among Reef Corals within Marine Protected Areas. Conserv Biol 22:1245–1254CrossRefPubMedGoogle Scholar
  57. Moore JAY, Bellchambers LM, Depczynski MR, Evans RD, Evans SN, Field SN, Friedman KJ, Gilmour JP, Holmes TH, Middlebrook R, Radford BT, Ridgway T, Shedrawi G, Taylor H, Thomson DP, Wilson SK (2012) Unprecedented Mass Bleaching and Loss of Coral across 12° of Latitude in Western Australia in 2010–11. PLoS ONE 7:e51807.  https://doi.org/10.1371/journal.pone.0051807 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Nei M (1973) Analysis of Gene Diversity in Subdivided Populations. Proc Natl Acad Sci U S A 70:3321–3323CrossRefPubMedPubMedCentralGoogle Scholar
  59. Nishikawa A (2008) Degree and Pattern of Gene Flow in Several Scleractinian Corals in the Ryukyu Archipelago, Southern Japan. Pac Sci 62:413–421CrossRefGoogle Scholar
  60. Noreen AME, Harrison PL, Van Oppen MJH (2009) Genetic diversity and connectivity in a brooding reef coral at the limit of its distribution. Proc R Soc B Biol Sci 276:3927–3935CrossRefGoogle Scholar
  61. Nychka D, Furrer R, Paige J, Sain S (2015) Fields: Tools for spatial data [ https://doi.org/10.5065/d6w957ct] http://doi.org/10.5065/D6W957CT, R package version 9.0
  62. Pante E, Simon-Bouhet B (2013) marmap: A Package for Importing, Plotting and Analyzing Bathymetric and Topographic Data in R. PLoS ONE 8:e73051.  https://doi.org/10.1371/journal.pone.0073051 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Paz-García DA, Chávez-Romo HE, Correa-Sandoval F, Reyes-Bonilla H, López-Pérez A, Medina-Rosas P, Hernández-Cortés MP (2012) Genetic Connectivity Patterns of Corals Pocillopora damicornis and Porites panamensis (Anthozoa: Scleractinia) Along the West Coast of Mexico. Pac Sci 66:43–61CrossRefGoogle Scholar
  64. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  65. Pineda J, Hare JA, Sponaugle S (2007) Larval Transport and Dispersal in the Coastal Ocean and Consequences for Population Connectivity. Oceanography 20:22–39CrossRefGoogle Scholar
  66. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847-846CrossRefGoogle Scholar
  67. Radford B, Babcock R, Van Niel K, Done T (2014) Are cyclones agents for connectivity between reefs? J Biogeogr 41:1367–1378CrossRefGoogle Scholar
  68. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  69. Rice WR (1989) Analyzing Tables of Statistical Tests. Evolution 43:223–225CrossRefPubMedGoogle Scholar
  70. Ridgway T, Inostroza K, Synnot L, Trapon M, Twomey L, Westera M (2016) Temporal patterns of coral cover in the offshore Pilbara, Western Australia. Marine Biol 163:182.  https://doi.org/10.1007/s00227-016-2956-1 CrossRefGoogle Scholar
  71. Riegl B, Purkis S (2015) Coral population dynamics across consecutive mass mortality events. Glob Change Biol 21:3995–4005CrossRefGoogle Scholar
  72. Riegl B, Berumen M, Bruckner A (2013) Coral population trajectories, increased disturbance and management intervention: a sensitivity analysis. Ecol Evol 3:1050–1064CrossRefPubMedPubMedCentralGoogle Scholar
  73. Riginos C, Crandall ED, Liggins L, Bongaerts P, Treml EA (2016) Navigating the currents of seascape genomics: how spatial analyses can augment population genomic studies. Curr Zool 62:581–601CrossRefPubMedPubMedCentralGoogle Scholar
  74. Ross CL, Falter JL, Schoepf V, McCulloch MT (2015) Perennial growth of hermatypic corals at Rottnest Island, Western Australia (32°S). PeerJ 3:e781.  https://doi.org/10.7717/peerj.781 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rosser NL (2015) Asynchronous spawning in sympatric populations of a hard coral reveals cryptic species and ancient genetic lineages. Mol Ecol 24:5006–5019CrossRefPubMedGoogle Scholar
  76. Rosser NL (2016) Demographic history and asynchronous spawning shape genetic differentiation among populations of the hard coral Acropora tenuis in Western Australia. Mol Phylogenet Evol 98:89–96CrossRefPubMedGoogle Scholar
  77. Rosser N, Gilmour JP (2008) New insights into patterns of coral spawning on Western Australian reefs. Coral Reefs 27:345–349CrossRefGoogle Scholar
  78. Rousset F (2008) genepop’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  79. RStudio Team (2016) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA URL http://www.rstudio.com/
  80. Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198CrossRefGoogle Scholar
  81. Schaberg PG, DeHayes DH, Hawley GJ, Nijensohn SE (2008) Anthropogenic alterations of genetic diversity within tree populations: Implications for forest ecosystem resilience. For Ecol Manag 256:855–862CrossRefGoogle Scholar
  82. Selkoe K, D’Aloia C, Crandall E, Iacchei M, Liggins L, Puritz J, von der Heyden S, Toonen R (2016) A decade of seascape genetics: contributions to basic and applied marine connectivity. Mar Ecol Prog Ser 554:1–19CrossRefGoogle Scholar
  83. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792CrossRefPubMedGoogle Scholar
  84. Sobel AH, Camargo SJ, Hall TM, Lee C-Y, Tippett MK, Wing AA (2016) Human influence on tropical cyclone intensity. Science 353:242–246CrossRefPubMedGoogle Scholar
  85. Szmant AM, Meadows MG (2006) Developmental changes in coral larval buoyancy and vertical swimming behavior: implications for dispersal and connectivity. Proc 10th Int Coral Reef Symp 431–437Google Scholar
  86. Thomas L, Kendrick G, Stat M, Travaille K, Shedrawi G, Kennington W (2014) Population genetic structure of the Pocillopora damicornis morphospecies along Ningaloo Reef, Western Australia. Mar Ecol Prog Ser 513:111–119CrossRefGoogle Scholar
  87. Thomas L, Kennington WJ, Stat M, Wilkinson SP, Kool JT, Kendrick GA (2015) Isolation by resistance across a complex coral reef seascape. Proc R Soc B Biol Sci 282:20151217CrossRefGoogle Scholar
  88. Thomas L, Kennington WJ, Evans RD, Kendrick GA, Stat M (2017) Restricted gene flow and local adaptation highlight the vulnerability of high-latitude reefs to rapid environmental change. Glob Change Biol 23:1365–2486Google Scholar
  89. Travers MJ, Potter IC, Clarke KR, Newman SJ, Hutchins JB (2009) The inshore fish faunas over soft substrates and reefs on the tropical west coast of Australia differ and change with latitude and bioregion: Ichthyofaunas of soft substrates and reefs. J Biogeogr 37:148–169CrossRefGoogle Scholar
  90. Underwood JN (2009) Genetic diversity and divergence among coastal and offshore reefs in a hard coral depend on geographic discontinuity and oceanic currents. Evolutionary Applications 2:222–233CrossRefPubMedPubMedCentralGoogle Scholar
  91. Underwood JN, Smith LD, van Oppen MJ, Gilmour JP (2009) Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience. Ecol Appl 19:18–29CrossRefPubMedGoogle Scholar
  92. Underwood JN, Wilson SK, Ludgerus L, Evans RD (2013) Integrating connectivity science and spatial conservation management of coral reefs in north-west Australia. Journal for Nature Conservation 21:163–172CrossRefGoogle Scholar
  93. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  94. Veron JEN (2000) Corals of the world. M. Stafford Smith (eds). Australian Institute of Marine Science, Townsville, AustraliaGoogle Scholar
  95. Wang IJ (2013) Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation: special section. Evolution 67:3403–3411CrossRefPubMedGoogle Scholar
  96. Weir BS, Cockerham CC (1984) Estimating F-Statistics for the Analysis of Population Structure. Evolution 38:1358PubMedGoogle Scholar
  97. Whitaker K (2004) Non-random mating and population genetic subdivision of two broadcasting corals at Ningaloo Reef, Western Australia. Marine Biology 144:593–603CrossRefGoogle Scholar
  98. Whitaker K (2006) Genetic evidence for mixed modes of reproduction in the coral Pocillopora damicornis and its effect on population structure. Mar Ecol Prog Ser 306:115–124CrossRefGoogle Scholar
  99. Williamson DH, Ceccarelli DM, Evans RD, Jones GP, Russ GR (2014) Habitat dynamics, marine reserve status, and the decline and recovery of coral reef fish communities. Ecol Evol 4:337–354CrossRefPubMedPubMedCentralGoogle Scholar
  100. Wilson BR (2013) The biogeography of the Australian north west shelf: environmental change and life’s response. Elsevier, Burlington, MAGoogle Scholar
  101. Wilson JR, Harrison PL (1998) Settlement-competency periods of larvae of three species of scleractinian corals. Mar Biol 131:339–345CrossRefGoogle Scholar
  102. Woo M, Pattiaratchi C, Schroeder W (2006) Dynamics of the Ningaloo Current off Point Cloates, Western Australia. Marine and Freshwater Research 57:291CrossRefGoogle Scholar
  103. Zhang N, Feng M, Hendon HH, Hobday AJ, Zinke J (2017) Opposite polarities of ENSO drive distinct patterns of coral bleaching potentials in the southeast Indian Ocean. Scientific Reports 7:2443CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biodiversity Conservation and AttractionsKensingtonAustralia
  2. 2.Oceans InstituteThe University of Western AustraliaCrawleyAustralia
  3. 3.Western Australian Fisheries and Marine Research Laboratories, Department of Primary Industries and Regional DevelopmentGovernment of Western AustraliaNorth BeachAustralia
  4. 4.CSIRO Oceans and AtmosphereIndian Ocean Marine Research CentreCrawleyAustralia
  5. 5.School of Biological SciencesThe University of Western AustraliaCrawleyAustralia
  6. 6.Centre for Evolutionary Biology, School of Biological SciencesThe University of Western AustraliaCrawleyAustralia

Personalised recommendations