Coral Reefs

, Volume 39, Issue 1, pp 55–60 | Cite as

Contrasting patterns of genetic connectivity in brooding and spawning corals across a remote atoll system in northwest Australia

  • Luke ThomasEmail author
  • Jim N. Underwood
  • Arne A. S. Adam
  • Zoe T. Richards
  • Laurence Dugal
  • Karen J. Miller
  • James P. Gilmour


An understanding of larval dispersal and connectivity in corals provides valuable insight into the processes of population maintenance and replenishment and is vital for effective management. Here, we used a genotyping by sequencing approach to explore patterns of genetic connectivity in two species of coral with different reproductive modes (brooding and broadcast spawning) at the Rowley Shoals in northwest Australia. Our data revealed strikingly different patterns of genetic structure in the two species. High levels of genetic subdivision in the brooding coral I. brueggemanni was consistent with extensive self-recruitment and restricted connectivity. In contrast, the broadcast spawning coral A. digitifera formed a single panmictic population with extensive gene flow. Our results highlight the wide variation in metapopulation connectivity that exists among corals and support the well-established link between reproductive mode and population genetic structure in the marine environment.


Gene flow Connectivity Rowley Shoals Dispersal 



This work was conducted as part of the North West Shoals to Shore Program, which is proudly supported by Santos as part of the company’s commitment to better understand WA’s marine environment. We would like to acknowledge Woodside Energy Ltd (Woodside) as Operator for and on behalf of the Browse Joint Venture (BJV). The project was also undertaken as part of ARC Linkage Project LP160101508.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

338_2019_1884_MOESM1_ESM.docx (2.1 mb)
Supplementary file 1 (DOCX 2151 kb)


  1. Adamack AT, Gruber B (2014) PopGenReport: Simplifying basic population genetic analyses in R. Methods Ecol Evol 5:384–387CrossRefGoogle Scholar
  2. Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep 6:1–15CrossRefGoogle Scholar
  3. Ayre D, Hughes TP, Standish RJ (1997) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the GBR, Australia. Mar Ecol Prog Ser 159:175–187CrossRefGoogle Scholar
  4. Benzie JAH, Smith-Keune C (2006) Microsatellite variation in Australian and Indonesian pearl oyster Pinctada maxima populations. Mar Ecol Prog Ser 314:197–211CrossRefGoogle Scholar
  5. Bernhardt JR, Leslie HM (2013) Resilience to climate change in coastal marine ecosystems. Ann Rev Mar Sci 5:371–392CrossRefGoogle Scholar
  6. Cawthorn DM, Steinman HA, Witthuhn RC (2011) Comparative study of different methods for the extraction of DNA from fish species commercially available in South Africa. Food Control 22:231–244CrossRefGoogle Scholar
  7. DiBattista JD, Wakefield CB, Moore GI, Bunce M, Williams AJ, O’Malley JM, Humphreys RL, Halafihi T, Williams A, Green MA, Graham K, Tucker S, Cruz E, Newman SJ (2018) Genomic and life-history discontinuity reveals a precinctive lineage for a deep-water grouper with gene flow from tropical to temperate waters on the west coast of Australia. Ecol Genet GenomicsGoogle Scholar
  8. Dray S, Dufour A-B (2007) The ade4 Package: Implementing the Duality Diagram for Ecologists. J Stat Softw 1:128–129Google Scholar
  9. Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics 180:977–993CrossRefGoogle Scholar
  10. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an Isolated Coral Reef System Following Severe Disturbance. Science (80-) 340:69–71CrossRefGoogle Scholar
  11. Gilmour JP et al (2019) The state of Western Australia’s coral reefs. Coral Reefs 38:651–667CrossRefGoogle Scholar
  12. Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186CrossRefGoogle Scholar
  13. Hanski I (1998) Metapopulation dynamics. Nature 396:41–49CrossRefGoogle Scholar
  14. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral Reefs (Ecosystems of the World; 25). Elsevier, New York, pp 133–207Google Scholar
  15. Hastings A, Botsford LW (2006) Persistence of spatial populations depends on returning home. Proc Natl Acad Sci 103:6067–6072CrossRefGoogle Scholar
  16. Holborn K, Johnson MS, Black R (1994) Population genetics of the corallivorous gastropod Drupella cornus at Ningaloo Reef, Western Australia. Coral Reefs 33–39CrossRefGoogle Scholar
  17. Johnson MS, Joll LM (1992) Genetic Subdivision of the Pearl Oyster _Pinctada maxima_ in Northern Australia. AustJMarFreshwater Res 44:519–526CrossRefGoogle Scholar
  18. Jombart T (2008) Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefGoogle Scholar
  19. Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281CrossRefGoogle Scholar
  20. Kennington WJ, Berry O, Groth D, Johnson MS, Melville-Smith R (2013) Spatial scales of genetic patchiness in the western rock lobster Panulirus cygnus. Mar Ecol Prog Ser 486:213–221CrossRefGoogle Scholar
  21. Kininmonth S, van Oppen MJH, Castine S, Peplow L, Lutz A (2012) The small genetic world of Seriatopora hystrix. Netw Biol 2:1–15Google Scholar
  22. Lin S, Ceng S, Song B, Zhong X, Lin X, Li W, Li L (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science (80-) 350:691–694CrossRefGoogle Scholar
  23. Liu H, Stephens TG, González-Pech RA, Beltran VH, Lapeyre B, Bongaerts P, Cooke I, Aranda M, Bourne DG, Forêt S, Miller DJ, van Oppen MJH, Voolstra CR, Ragan MA, Chan CX (2018) Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun Biol 1:1–11CrossRefGoogle Scholar
  24. Miller K, Ayre D (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. J Anim Ecol 77:713–724CrossRefGoogle Scholar
  25. Nei M (1973) Analysis of Gene Diversity in Subdivided Populations MASATOSHI NEI Center for Demographic and Population. Proc Natl Acad Sci 70:3321–3323CrossRefGoogle Scholar
  26. van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660CrossRefGoogle Scholar
  27. Pazmiño DA, Maes GE, Green ME, Simpfendorfer CA, Hoyos-Padilla EM, Duffy CJA, Meyer CG, Kerwath SE, Salinas-De-León P, Van Herwerden L (2018) Strong trans-Pacific break and local conservation units in the Galapagos shark (Carcharhinus galapagensis) revealed by genome-wide cytonuclear markers. Heredity (Edinb) 120:407–421CrossRefGoogle Scholar
  28. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  29. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Bhattacharya D, Satoh N (2013) Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399–1408CrossRefGoogle Scholar
  30. Thomas L, Kendrick GGA, Stat M, Travaille KKL, Shedrawi G, Kennington WJJ (2014) Population genetic structure of the Pocillopora damicornis morphospecies along Ningaloo Reef, Western Australia. Mar Ecol Prog Ser 513:111–119CrossRefGoogle Scholar
  31. 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 Chang Biol 38:42–49Google Scholar
  32. Underwood JN (2007) Routine and rare genetic connections in corals off northwest Australia and the implications for conservation.Google Scholar
  33. Underwood JN (2009) Genetic diversity and divergence among coastal and offshore reefs in a hard coral depend on geographic discontinuity and oceanic currents. Evol Appl 2:222–233CrossRefGoogle Scholar
  34. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784CrossRefGoogle Scholar
  35. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2009) Ecologically Relevant Dispersal of Corals on Isolated Reefs : Implications for Managing Resilience. Ecol Appl 19:18–29CrossRefGoogle Scholar
  36. Underwood JN, Travers MJ, Gilmour JP (2012) Subtle genetic structure reveals restricted connectivity among populations of a coral reef fish inhabiting remote atolls. Ecol EvolGoogle Scholar
  37. Underwood JN, Wilson SK, Ludgerus L, Evans RD (2013) Integrating connectivity science and spatial conservation management of coral reefs in north-west Australia. J Nat Conserv 1–10Google Scholar
  38. Underwood JN, Richards ZT, Miller KJ, Puotinen ML, Gilmour JP (2018) Genetic signatures through space, time and multiple disturbances in a ubiquitous brooding coral. Mol Ecol 1586–1602CrossRefGoogle Scholar
  39. 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
  40. Winter DJ (2012) MMOD: An R library for the calculation of population differentiation statistics. Mol Ecol Resour 12:1158–1160CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Australian Institute of Marine ScienceIndian Ocean Marine Research CentreCrawleyAustralia
  2. 2.Oceans Graduate SchoolFaculty of Engineering and Mathematical Sciences, The University of Western AustraliaCrawleyAustralia
  3. 3.Coral Conservation and Research Group, Trace Environmental DNA Lab, School of Molecular and Life SciencesCurtin UniversityPerthAustralia

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