Skip to main content
SpringerLink
Log in

Geography and spawning season drive genetic divergence among populations of the hard coral Acropora tenuis from Indonesia and Western Australia

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

It has long been hypothesized that Western Australian coral reefs are genetically connected to those in Indonesia via long-distance dispersal, and that this connection may influence the timing of annual mass coral spawning on Western Australian coral reefs. This genetic connection has not been tested, and it requires re-evaluation because spawning patterns of Western Australian corals are not as synchronous or seasonal as originally thought. Here, we used population genetics to examine patterns of gene flow among populations of the scleractinian coral Acropora tenuis in Indonesia and Western Australia. Analysis of microsatellite data showed that Indonesian and Australian populations are highly genetically differentiated. Importantly, this genetic divergence is associated with differences in the seasonal spawning time of A. tenuis between the two regions, with Indonesian populations dominated by ‘spring’ spawners and Western Australian populations dominated by ‘autumn’ spawners, indicating that spawning season has an important influence on genetic structure. Furthermore, negligible gene flow between Indonesia and Western Australia indicates that the recolonization of inshore Western Australian populations since the Last Glacial Maximum was independent of input from Indonesian populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605

    CAS  PubMed  Google Scholar 

  • Ayre DJ, Hughes TP (2004) Climate change, genotypic diversity and gene flow in reef corals. Ecol Lett 7:273–278

    Google Scholar 

  • Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394

    Google Scholar 

  • Babcock RC, Wills BL, Simpson CJ (1994) Mass spawning of corals on a high latitude coral reef. Coral Reefs 13:161–169

    Google Scholar 

  • Baird AH, Marshall PA, Wolstenholme JK (2002) Latitudinal variation in the reproduction of Acropora in the Coral Sea Proceedings of the 9th International Coral Reef Symposium, Bali 385–389

  • Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390

    CAS  PubMed  Google Scholar 

  • Benzie JAH, Ballment E, Forbes AT, Demetriades NT, Sugama K, Haryanti MS (2002) Mitochondrial DNA variation in Indo-Pacific populations of the giant tiger prawn, Penaeus monodon. Mol Ecol 11:2553–2569

    CAS  PubMed  Google Scholar 

  • Benzie JAH, Smith C, Sugama K (2003) Mitochondrial DNA reveals genetic differentiation between Australian and Indonesian pearl oyster Pinctada maxima (Jameson 1901) populations. J Shellfish Res 22:781–787

    Google Scholar 

  • Carpenter KE, Barber PH, Crandall ED, Ablan-Lagman MCA, Ambariyanto MGN, Manjaji-Matsumoto M, Juinio-Menez MA, Santos MD, Starger CJ, Toha AHA (2011) Comparative Phylogeography of the Coral Triangle and Implications for Marine Management. Journal of Marine Biology 2011:1–14

    Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    CAS  PubMed  Google Scholar 

  • Crandall ED, Jones ME, Munoz MM, Akinronbi B, Erdman MV, Barber PH (2008) Comparative phylogeography of two seastars and their ectosymbionts within the Coral Triangle. Mol Ecol 17:5276–5290

    PubMed  Google Scholar 

  • Crandall ED, Treml EA, Liggins L, Gleeson L, Riginos C (2014) Return of the ghosts of dispersal past: Historical spread and contemporary gene flow in the blue sea star Linckia laevigata. Bull Mar Sci 90:399–425

    Google Scholar 

  • D'Adamo N, Fandry C, Buchan S, Domingues C (2009) Northern sources of the Leeuwin Current and the "Holloway Current" on the North West Shelf. J R Soc West Aust 92:53–66

    Google Scholar 

  • Domingues CM, Maltrud ME, Wijffels SE, Church JA, Tomczak M (2007) Simulated lagrangian pathways between the Leeuwin Current system and the upper-ocean circulation of the southeast Indian Ocean. Deep Sea Research II 54:797–817

    Google Scholar 

  • Evanno G, Regnault S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10:564–567

    PubMed  Google Scholar 

  • Fukami H, Omori M, Shimoike K, Hayashibara T, Hatta M (2003) Ecological and genetic aspects of reproductive isolation by different spawning times in Acropora corals. Mar Biol 142:679–684

    Google Scholar 

  • Gilmour J, Speed CW, Babcock R (2016a) Coral reproduction in Western Australia PeerJ 4:e2010

    PubMed  Google Scholar 

  • Gilmour JP, Underwood JN, Howells EJ, Gates E, Heyward AJ (2016b) Biannual spawning and temporal reproductive isolation in Acropora corals. PLoS ONE 11:e0150916

    PubMed  PubMed Central  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (vers. 2.9.3). Available from https://www.unilch/izea/softwares/fstat.html

  • Habibi A, Setiawan R, Zuhdy D (2010) Wind-driven coastal upwelling along south Sulawesi island. Ilmu Kelautan 15:113–118

    Google Scholar 

  • Imron JB, Hale P, Degnan BM, Degnan SM (2007) Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity. Mol Ecol 16:289–304

    CAS  PubMed  Google Scholar 

  • Johnson MS, Black R (2006a) Effects of mode of reproduction on genetic divergence over large spatial and temporal scales in intertidal snails of the genus Bembicium Philippi (Gastropoda: Littorinidae). Biol J Linn Soc 89:689–704

    Google Scholar 

  • Johnson MS, Black R (2006b) Islands increase genetic subdivision and disrupt patterns of connectivity of intertidal snails in a complex archipelago. Evolution 60:2498–2506

    CAS  PubMed  Google Scholar 

  • Johnson MS, Hebbert DR, Moran MJ (1993) Genetic analysis of populations of north-western Australian fish species. Aust J Mar Freshw Res 44:673–685

    Google Scholar 

  • Kartadikaria AR, Miyazawa Y, Nadaoka K, Watanbe A (2012) Existence of eddies at crossroad of the Indonesian seas. Ocean Dyn 62:31–44

    Google Scholar 

  • Knowlton N, Mate JL, Guzman HM, Rowan R, Jara J (1997) Direct evidence for reproductive isolation among the three species of the Montastrea annularis complex in Central America (Panama and Honduras). Mar Biol 127:705–711

    Google Scholar 

  • Levitan DR, Fogarty ND, Jara J, Lotterhos KE, Knowlton N (2011) Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex. Evolution 65:1254–1270

    PubMed  Google Scholar 

  • Li Y, Liu J (2018) StructureSelector: A web-based software to select and visualize the optimal number of clusters using multiple methods. Molecular Ecology Resources 18:176–177

    PubMed  Google Scholar 

  • Marra J, Moore TS (2009) Monsoons, islands, and eddies: Their effects on phytoplankton in the Indian Ocean. Geophys Monogr Ser 185:57–70

    Google Scholar 

  • McCaffrey JC, Wallace MW, Gallagher SJ (2020) A Cenozoic Great Barrier Reef on Australia's North West shelf. Global Planet Change 184:103048

    Google Scholar 

  • Moore TS II, Marra J, Alkatiri A (2003) Response of the Banda Sea to the southeast monsoon. Mar Ecol Prog Ser 261:41–49

    Google Scholar 

  • Ningsih NS, Rakhmaputeri N, Harto AB (2013) Upwelling variability along the southern coast of Bali and in Nusa Tenggara waters. Ocean Science Journal 48(1):49–57

    Google Scholar 

  • Nof D, Pichevin T, Sprintall J (2002) "Teddies" and the origin of the Leeuwin Current. J Phys Oceanogr 32:2571–2573

    Google Scholar 

  • Ohki S, Kowalski RK, Kitanobo S, Morita M (2015) Changes in spawning time led to the speciation of the broadcast spawning corals Acropora digitifera and the cryptic species Acropora sp. 1 with similar gamete recognition systems. Coral Reefs 34:1189–1198

    Google Scholar 

  • Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118

    CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Google Scholar 

  • Permata D, Indrayanti E, Haryanti D, Fika L, Arfiyan H, Achmad A (2012) Biannual multispecific spawning in Karimunjawa Archipelago, Indonesia. Coral Reefs DOI 10.1007/s00338–012–0909–9

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puechmaille SJ (2016) The program STRUCTURE does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Molecular Ecology Resources 16:608–627

    PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) Population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Riginos C, Hock K, Matias AM, Mumby PJ, van Oppen MJH, Lukoschek V (2019) Asymmetric dispersal is a critical element of concordance between biophysical dispersal models and spatial genetic structure in Great Barrier Reef corals. Divers Distrib 25:1684–1696

    Google Scholar 

  • Rosser NL (2013) Biannual coral spawning decreases at higher latitudes on Western Australian reefs. Coral Reefs 32:455–460

    Google Scholar 

  • Rosser NL (2015) Asynchronous spawning in sympatric populations of a hard coral reveals cryptic species and ancient genetic lineages. Mol Ecol 24:5006–5019

    CAS  PubMed  Google Scholar 

  • Rosser NL (2016) Demographic history and asynchronous spawning shape genetic differentiation among populations of the hard coral Acropora tenuis in Western Australia. Mol Phylogen Evol 98:89–96

    Google Scholar 

  • Rosser NL, Gilmour JP (2008) New insights into patterns of coral spawning on Western Australian reefs. Coral Reefs 27:345–349

    Google Scholar 

  • Simpson CJ (1988) Coral reproduction and mass spawning Ecology of scleractinian corals in the Dampier archipelago. Western Australia, Environmental Protection Authority, Perth, Western Australia

    Google Scholar 

  • Simpson CJ (1991) Mass spawning of corals on Western Australian reefs and comparisons with the Great Barrier Reef. J R Soc West Aust 74:85–91

    Google Scholar 

  • Sprintall J, Wijffels SE, Molcard R, Jaya I (2009) Direct estimates of the Indonesian Throughflow entering the Indian Ocean: 2004–2006. J Geophys Res 114:1–19

    Google Scholar 

  • Stoddart DR (1974) Continuity and crisis in the reef community. Micronesica 12:1–9

    Google Scholar 

  • Thompson DM, Kleypas J, Castruccio F, Curchitser EN, Pinksy MI, Jonsson B, Watson JR (2018) Variability in oceanographic barriers to coral larval dispersal: Do currents shape biodiversity? Prog Oceanogr 165:110–122

    Google Scholar 

  • Treml EA, Halpin PN (2012) Marine population connectivity identifies ecological neighbors for conservation planning in the Coral Triangle. Conservation Letters 5:441–449

    Google Scholar 

  • Treml EA, Roberts JJ, Chao Y, Halpin PN, Possingham HP, Riginos C (2012) Reproductive output and duration of the pelagic larval stage determine seascape-wide connectivity of marine populations. Integrative and Comparative Biology 52:525–537

    PubMed  Google Scholar 

  • Treml EA, Roberts JJ, Halpin PN, Possingham HP, Riginos C (2015) The emergent geography of biophysical dispersal barriers across the Indo-West Pacific. Divers Distrib 21:465–476

    Google Scholar 

  • 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 2:222–233

    PubMed  PubMed Central  Google Scholar 

  • Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP (2006) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

    Google Scholar 

  • Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP (2009) Ecologically relevant dispersal of corals on isolated reefs: implications for management. Ecol Appl 19:18–29

    PubMed  Google Scholar 

  • 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 4:535–538

    Google Scholar 

  • Veron J, Stafford-Smith M, Devantier LM, Turak E (2015) Overview of distribution patterns of zooxanthellate Scleractinia. Front Mar Sci 1:81

    Google Scholar 

  • Vize PD, Embesi JA, Nickell M, Brown DP, Hagman DK (2005) Tight temporal consistency of coral mass spawning at the Flower Garden Banks, Gulf of Mexico, from 1997–2003. Gulf Mex Sci 23:107–114

    Google Scholar 

  • Wang S, Zhang L, Matz M (2009) Microsatellite characterization and marker development from public EST and WGS databases in the reef building coral Acropora millepora (Cnidaria, Anthozoa, Scleractinia). J Hered 100:329–337

    CAS  PubMed  Google Scholar 

  • Ward RDM, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater and anadromous fishes. J Fish Biol 44:213–222

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Wijayanti DP, Indrayanti E, Wirasatriya A, Haryanto A, Haryanti D, Sembiring A, Fajrianzah TA, Bhagooli R (2019) Reproductive Seasonality of Coral Assemblages in the Karimunjawa Archipelago, Indonesia. Frontiers in Marine Science 6:195. https://doi.org/10.3389/fmars.2019.00195

    Article  Google Scholar 

  • Wijffels SE, Beggs H, Griffin C, Middleton JF, Cahill M, King E, Jones E, Feng M, Benthuysen JA, Steinberg CR, Sutton P (2018) A fine spatial-scale sea surface temperature atlas of the Australian regional seas (SSTAARS): Seasonal variability and trends around Australasia and New Zealand revisited. J Mar Syst 187:156–196

    Google Scholar 

  • Willis BL, Babcock RC, Harrison PL, Oliver JK (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. Proc 5th Int Coral Reef Sym 4:343–348

  • Wilson BR (2013) The biogeography of the Australian north west shelf: environmental change and life's response. Elsevier

  • Wood S, Paris CB, Ridgwell A, Hendy EJ (2014) Modelling dispersal and connectivity of broadcast spawning corals at the global scale. Global Ecol Biogeogr 23:1–11

    Google Scholar 

  • Yokoyama Y, Purcell A, Lambeck K, Johnston P (2001) Shore-line reconstruction around Australia during the Last Glacial Maximum and Late Glacial Stage. Quatern Int 83–85:9–18

    Google Scholar 

  • Zhu Y, Wang L, Wang Y, Xu T, Li S, Cao G, Wei Z, Qu T (2019) Stratified circulation in the Banda Sea and its causal mechanism. Journal of Geophysical Research: Oceans 124(10):7030–7045

    Google Scholar 

Download references

Acknowledgements

Special thanks go to Yvette Hitchen for all her help with the laboratory work, Peter Rosser and Eamon Dorricott for their help with the Indonesian field work, Madeline van Oppen for providing the GBR samples, James Gilmour for practical support and ecological guidance during collection and analysis of the WA data, Luke Thomas for constructive reflection on the results and JP Rippe and an anonymous reviewer for their helpful comments on the manuscript. Data from Western Australia were collected as part of the Scott Reef program supported by Woodside Energy Ltd as operator for and on behalf of the Browse Joint Venture (BJV—Woodside Browse Pty Ltd, Shell Australia Pty Ltd, BP Developments Australia Pty Ltd, Japan Australia LNG (MIMI Browse) Pty Ltd and PetroChina International Investment (Australia) Pty Ltd). Co-Author J. N. Underwood is supported by the Woodside Coral Reef Research Fellowship. Samples from Indonesia were collected under Natalie Rosser’s research permit No. 1/TKPIPA/FRP/SM/I/2012, and NLR gratefully received funding from a Holsworth Wildlife Endowment Grant and a UWA Convocation award.

Author information

Author notes

  1. N. L. Rosser

    Present address: School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia

Authors and Affiliations

  1. School of Biological Sciences, University of Western Australia, Crawley, WA, 6009, Australia

    N. L. Rosser & M. S. Johnson

  2. Research Institute for Environment and Livelihoods, Charles Darwin University, Casuarina, NT, 0810, Australia

    K. Edyvane

  3. Faculty of Marine Science and Fisheries, Hasanuddin University, Makassar, 90245, Indonesia

    A. C. Malina

  4. Australian Institute of Marine Science, Indian Ocean Marine Research Centre, Crawley, WA, 6009, Australia

    J. N. Underwood

Authors
  1. N. L. Rosser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Edyvane
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. C. Malina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. N. Underwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. S. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. L. Rosser.

Ethics declarations

Conflict of interest

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

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Carly Kenkel

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 351 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosser, N.L., Edyvane, K., Malina, A.C. et al. Geography and spawning season drive genetic divergence among populations of the hard coral Acropora tenuis from Indonesia and Western Australia. Coral Reefs 39, 989–999 (2020). https://doi.org/10.1007/s00338-020-01923-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-020-01923-9

Keywords

Search

Navigation