Genetic patterns of the corals Euphyllia glabrescens and Lobophyllia corymbosa across the Indonesian Archipelago
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Abstract. Jompa J, Umar W, Yusuf S, Tassakka ACM, Limmon GV, Rahmi, Putri AP, Halwi, Tamti H, Moore AM. 2020. Genetic patterns of the corals Euphyllia glabrescens and Lobophyllia corymbosa across the Indonesian Archipelago. Biodiversitas 21: xxxx. Scleractinian corals can reproduce in several ways, with two main sexual reproduction modes known as brooding and broadcast spawning. In this study, we described patterns of genetic variation within and connectivity between coral populations in western Indonesia (Seribu Archipelago), central Indonesia (Spermonde Archipelago), and eastern Indonesia (Ambon). We sampled two readily identifiable corals popular in the marine aquarium trade, one species widely reported as a brooder (Euphyllia glabrescens), the other as a broadcast spawner (Lobophyllia corymbosa). The mitochondrial COI genome was amplified for 117 samples. Within-population genetic variation was high, especially at the eastern Indonesia (Ambon) site. The genetic connectivity patterns were similar for the two corals, with high connectivity between the Seribu and Spermonde Archipelagos (despite a geographical separation of more than 1,000 km) and a lack of connectivity between these two sites and Ambon. These results indicate a potential barrier to gene flow between coral populations in western/central Indonesia and those to the east of Sulawesi Island.
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References
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Lugo-Fernandez A. 2001. Inferring probable dispersal of Flower Garden Banks coral larvae (Gulf of Mexico) using observed and simulated drifter trajectories. Continental Shelf Research 21: 47-67. Doi: 0.1016/S0278-4343(00)00072-8
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Moore AM, Tassakka ACM, Ambo-Rappe R, Yasir I, Smith DJ, Jompa J. 2019 Unexpected discovery of Diadema clarki in the Coral Triangle. Mar Biodivers 49:1–19. Doi: 10.1007 /s12526-019-00978-4
Mumby PJ, Steneck RS. 2008. Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends in Ecology and Evolution 23:555–563. Doi: 10.1016/j.tree.2008.06.011
Perry CT, Filip LA. 2019. Changing geo?ecological functions of coral reefs in the Anthropocene. Funct Ecol 33:976–988. Doi: 10.1111/1365-2435.13247
Rinkevich B. 2008. Management of coral reefs: We have gone wrong when neglecting active reef restoration. Marine Pollution Bulletin 56: 1821–1824. Doi: 10.1016/j.marpolbul.2008.08.014
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Selkoe KA, Aloia CCD, Crandall ED, Iacchei M, Liggins L, Puritz JB, von der Heyden S, Toonen RJ. 2016. A decade of seascape genetics: contributions to basic and applied marine connectivity. Marine Ecology Progress Series 554:1–19. Doi: 10.3354/meps11792
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Tamura K, Peterson D, Peterson N, Stecher G, Nei M and Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 12: 2725-9. Doi: 10.1093/molbev/mst197
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Teichberg M, Wild C, Bednarz VN, Kegler, Hauke F, Lukman M., Gärdes AA, Heiden JP, Weiand L, Abu N, Nasir A, Miñarro S, Ferse SCA. Reuter H, Plass-Johnson JG. 2018. Spatio-Temporal Patterns in Coral Reef Communities of the Spermonde Archipelago, 2012–2014, I: Comprehensive Reef Monitoring of Water and Benthic Indicators Reflect Changes in Reef Health. Frontiers in Marine Science 5: 1–18. Doi: 10.3389/fmars.2018.00033
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Timm J, Kochzius M, Madduppa HH, Neuhaus AI. 2017. Small Scale Genetic Population Structure of Coral Reef Organisms in Spermonde Archipelago, Indonesia. Front Mar Sci 4:1--14. Doi: 10.3389/fmars.2017.00294
Trapon ML, Pratchett MS, Penin L. 2011. Comparative effects of different disturbances in coral reef habitats in Moorea, French Polynesia. J Mar Biol 201:1–11
Treml EA, Roberts J, Halpin PN, Possingham HP, Riginos C. 2015. The emergent geography of biophysical dispersal barriers across the Indo-West Pacific. Divers Distrib 21:465–476. Doi: 10.1111/ddi.12307
Umar W, Tassakka ACMAR, Barber PH, Jompa J. 2019a. Unexpected patterns of genetic connectivity in Lobophyllia corymbosa (Forskål, 1775) around Sulawesi, Indonesia. Biodiversitas 20: 2744-2749. Doi: 10.13057/biodiv/d200940
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Umar W, Tassakka ACMAR and Jompa J. 2019c. Potential Uses of Genetic Studies for MPA Design. IOP Conference Series: Earth and Environmental Science. 253. 012032. 10.1088/1755-1315/253/1/012032.
van Oppen MJH, Gates RD. 2006. Conservation genetics and the resilience of reef-building corals. Mol Ecol 15(13): 3863–3883. Doi: 10.1111/j.1365-294X.2006.03026.x
von der Heyden, S. 2017. Making evolutionary history count: biodiversity planning for coral reef fishes and the conservation of evolutionary processes. Coral Reefs 36, 183–194. Doi: 10.1007/s00338-016-1512-2.
Woodhead AJ, Hicks CC, Norström AV, Williams GJ, Graham, NAJ. 2019. Coral reef ecosystem services in the Anthropocene. Functional Ecology 33:1023–1034. Doi: 10.1111/1365-2435.13331.
Wooldridge SA. 2017. Instability and breakdown of the coral–algae symbiosis upon exceedence of the interglacial pCO2 threshold (>260 ppmv): the ‘“missing”’ Earth-System feedback mechanism. Coral Reefs 36:1025–1037. Doi: 10.1007/s00338-017-1594-5
Yasuda N, Nagai S, Hamaguchi M, Okaji K, Gérard K, et al. 2009. Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis. Mol Ecol 18: 1574–1590. Doi: 10.1111/j.1365-294X.2009.04133.x
Yusuf S, Ahmad M, Umar W, Limmon GV, Jompa J. 2019. Biogeography and diversity of Lobophyllia, an ornamental coral traded in the coral triangle. IOP Conference Series: Earth Environ Sci 253: 012030. Doi: 10.1088/1755-1315/253/1/012030.
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Ayre DJ, Hughes TP. 2004. Climate change, genotypic diversity and gene flow in reef-building corals. Ecology Letters 7: 273–278. Doi: 10.1111/j.1461-0248.2004.00585.x
Baums IB, Miller MW, Hellberg ME. 2005. Regionally isolated populations of an imperilled Caribbean coral, Acropora palmata. Molecular Ecology 14: 1377–1390. Doi: 10.1111/j.1365-294X.2005.02489.x
Benzie JAH. 1999. Genetic Structure of Coral Reef Organisms: Ghosts of Dispersal Past. American Zoologist 39: 131–145. Doi: 10.1093/icb/39.1.131
Bohonak AJ. 1999. Dispersal, gene flow and population structure. Quarterly Review of Biology 74: 21–45. Doi: 10.1086/392950
Bowden-Kerby A. 2001. Low-tech coral reef restoration methods modelled after natural fragmentation processes. Bulletin of Marine Science 69: 915–931
Bowen BW, Rocha LA, Toonen RJ, Karl SA. 2013. The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366. Doi: 10.1016/j.tree.2013.01.018
Boulay JN, Cortés J, Nivia-Ruiz J, Baums IB. 2012. High genotypic diversity of the reef-building coral Porites lobata (Scleractinia: Poritidae) in Isla del Coco National Park, Costa Rica. Revista de Biología Tropical 60: 279–292.
Carpenter KE, Barber PH, Crandall ED, Ablan-Lagman MCA, Ambariyanto, Mahardika GN, Manjaji-Matsumoto BM, 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(396982): 1–14. Doi: 10.1155/2011/396982
Chust G, Villarino E, Chenuil A, Irigoien X, Bizsel N, Bode A, Broms C, Claus S, Fernández de Puelles ML, Fonda-Umani S, Hoarau G, Mazzocchi MG, Mozeti? P, Vandepitte L, Veríssimo H, Zervoudaki S, Borja A. 2016. Dispersal similarly shapes both population genetics and community patterns in the marine realm. Scientific Reports 6: 28730. Doi: 10.1038/srep28730
Crandall ED, Treml EA, Liggins L, Gleeson L, Yasuda N, Barber PH, Wörheide G, 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. Doi: 10.5343/bms.2013.1052
Durand JR, Petit D. 1995. The Java Sea Environment. In: Potier M, Nurhakim S (eds) Biodynex: biology, dynamics, exploitation of the small pelagic fishes in the Java Sea. Agency for Agricultural Research and Development, Jakarta, pp 15–38
Excoffier L, Laval G, Schneider S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
dx.doi.org/10.1111/j.1365-294X.2012.05576.x
Forêt S, Kassahn K, Grasso LC, Hayward DC, Iguchi A, et al. 2007. Genomic and microarray approaches to coral reef conservation biology. Coral Reefs 26: 475–486. Doi: 10.1007/s00338-007-0206-1
Gilg MR, Kirby SE, Sullivan R, Knapp LW, Hilbish TJ. 2007. Dispersal vs. retention: correspondence of species-specific reproductive cycles and settlement periods in a blue mussel hybrid zone. Marine Ecology Progress Series 351: 151–161. Doi: 10.3354/meps07145
Goodbody-Gringley G, de Putron SJ. 2016. Brooding Corals: Planulation Patterns, Larval Behavior, and Recruitment Dynamics in the Face of Environmental Change. In: Goffredo S., Dubinsky Z. (eds) The Cnidaria, Past, Present and Future. Springer, Cham pp. 279-289. Doi: 10.1007/978-3-319-31305-4_18
Hellberg, ME. 1994. Relationship between inferred levels of gene flow and geographic distance in a philopatric coral Balanophyllia elegans. Evolution 48:1829–1854. Doi: 10.1111/j.1558-5646.1994.tb02218.x
Hellberg ME. 2007. Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26: 463–473. Doi: 10.1007/s00338-007-0205-2
Hoegh-Guldberg O, Hoegh-Guldberg H, Veron JEN, Green A, Gomez ED, Lough J, King M, Ambariyanto, Hansen L, Cinner J, Dews G, Russ G, Schuttenberg HZ, Peñaflor EL, Eakin CM, Christensen TRL, Abbey M, Areki F, Kosaka RA, Tewflik A, Oliver J. 2009. The Coral Triangle and Climate Change: Ecosystems, People and Societies at Risk. WWF Australia, Brisbane. 229 pp.
Hoegh-Guldberg O, Pendleton L, Kaup A. 2019. People and the changing nature of coral reefs. Regional Studies in Marine Science 30:1–20. Doi: 10.1016/j.rsma.2019.100699
Holsinger KE, Weir BS. 2015. Genetics in geographically structured populations: defining, estimating and interpreting FST. Nature Reviews Genetics 10: 639–650. Doi: 10.1038/nrg2611
Holstein DM, Paris CB, Mumby PJ. 2014. Consistency and inconsistency in multispecies population network dynamics of coral reef ecosystems. Marine Ecology Progress Series 499: 1–18. Doi: 10.3354/meps10647.
Hughes TP, Baird AH, Dinsdale EA, Harriott VJ, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL. 2002. Detecting regional variation using meta-analysis and large-scale sampling: latitudinal patterns in recruitment. Ecology 83: 436–451. Doi: 10.1890/0012-9658(2002)083[0436:DRVUMA]2.0.CO;2
Karl SA, Toonen RJ, Grant WS, Bowen BW. 2012. Common misconceptions in molecular ecology: echoes of the modern synthesis. Molecular Ecology 21(17): 4171–4189. Doi: 10.1111/j.1365-294X.2012.05576.x.
Lugo-Fernandez A. 2001. Inferring probable dispersal of Flower Garden Banks coral larvae (Gulf of Mexico) using observed and simulated drifter trajectories. Continental Shelf Research 21: 47-67. Doi: 0.1016/S0278-4343(00)00072-8
Lukoschek V, Cross P, Torda G, Zimmerman R, Willis BL. 2013. The Importance of Coral Larval Recruitment for the Recovery of Reefs Impacted by Cyclone Yasi in the Central Great Barrier Reef. PLoS One 8:1–11. Doi: 10.1371/journal.pone.0065363.
Maier E, Tollrian R, Nuernberger B. 2009. Fine-scale analysis of genetic structure in the brooding coral Seriatopora hystrix from the Red Sea. Coral reefs 28:751–756. Doi: 10.1007/s00338-009-0497-5
McCook LJ, Jompa J, Diaz-Pulido G. 2001. Competition between corals and algae on coral reefs: A review of evidence and mechanisms. Coral Reefs 19:400–417. Doi: 10.1007/s003380000129
Moore AM, Tassakka ACM, Ambo-Rappe R, Yasir I, Smith DJ, Jompa J. 2019 Unexpected discovery of Diadema clarki in the Coral Triangle. Mar Biodivers 49:1–19. Doi: 10.1007 /s12526-019-00978-4
Mumby PJ, Steneck RS. 2008. Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends in Ecology and Evolution 23:555–563. Doi: 10.1016/j.tree.2008.06.011
Perry CT, Filip LA. 2019. Changing geo?ecological functions of coral reefs in the Anthropocene. Funct Ecol 33:976–988. Doi: 10.1111/1365-2435.13247
Rinkevich B. 2008. Management of coral reefs: We have gone wrong when neglecting active reef restoration. Marine Pollution Bulletin 56: 1821–1824. Doi: 10.1016/j.marpolbul.2008.08.014
Nakajima Y, Nishikawa A, Iguchi A, Sakai K. 2010. Gene Flow and Genetic Diversity of a Broadcast-Spawning Coral in Northern Peripheral Populations. PLoS ONE, 5(6), e11149. Doi:10.1371/journal.pone.0011149.
Nielsen ES, Beger M, Henriques R, Selkoe KA, von der Heyden S. 2017. Multispecies genetic objectives in spatial conservation planning. Conservation Biology 31, 872–882. Doi: 10.1111/cobi.12875.
Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij MJ, Paul VJ. 2009. New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithsonian Contributions to the Marine Sciences 38:437–457.
Rozas J, Sanchez-DeI BJC, Messeguer and Rozas XR. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19: 2496–2497. Doi: 10.1093/bioinformatics/btg359
Selkoe KA, Aloia CCD, Crandall ED, Iacchei M, Liggins L, Puritz JB, von der Heyden S, Toonen RJ. 2016. A decade of seascape genetics: contributions to basic and applied marine connectivity. Marine Ecology Progress Series 554:1–19. Doi: 10.3354/meps11792
Serrano, X., Baums, I., Smith, T. Jones RJ, Shearer TL, Baker AC. 2016. Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Scientific Reports 6, 21619. Doi: 10.1038/srep21619.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M and Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 12: 2725-9. Doi: 10.1093/molbev/mst197
Taylor HR, Dussex N, van Heezik Y. 2017. Bridging the conservation genetics gap by identifying barriers to implementation for conservation practitioners. Global Ecology and Conservation 10: 231–242. Doi: 10.1016/j.gecco.2017.04.001
Teichberg M, Wild C, Bednarz VN, Kegler, Hauke F, Lukman M., Gärdes AA, Heiden JP, Weiand L, Abu N, Nasir A, Miñarro S, Ferse SCA. Reuter H, Plass-Johnson JG. 2018. Spatio-Temporal Patterns in Coral Reef Communities of the Spermonde Archipelago, 2012–2014, I: Comprehensive Reef Monitoring of Water and Benthic Indicators Reflect Changes in Reef Health. Frontiers in Marine Science 5: 1–18. Doi: 10.3389/fmars.2018.00033
Thomas L, Underwood JN, Adam AAS, Richards ZT, Dugal L, Miller KJ, Gilmour JP. 2019. Contrasting patterns of genetic connectivity in brooding and spawning corals across a remote atoll system in northwest Australia. Coral Reefs 35:55–60. Doi: 10.1007/s00338-019-01884-8
Timm J, Kochzius M, Madduppa HH, Neuhaus AI. 2017. Small Scale Genetic Population Structure of Coral Reef Organisms in Spermonde Archipelago, Indonesia. Front Mar Sci 4:1--14. Doi: 10.3389/fmars.2017.00294
Trapon ML, Pratchett MS, Penin L. 2011. Comparative effects of different disturbances in coral reef habitats in Moorea, French Polynesia. J Mar Biol 201:1–11
Treml EA, Roberts J, Halpin PN, Possingham HP, Riginos C. 2015. The emergent geography of biophysical dispersal barriers across the Indo-West Pacific. Divers Distrib 21:465–476. Doi: 10.1111/ddi.12307
Umar W, Tassakka ACMAR, Barber PH, Jompa J. 2019a. Unexpected patterns of genetic connectivity in Lobophyllia corymbosa (Forskål, 1775) around Sulawesi, Indonesia. Biodiversitas 20: 2744-2749. Doi: 10.13057/biodiv/d200940
Umar W, Tassakka ACMAR, Jompa J. 2019b. High genetic connectivity in a scleractinian coral (Lobophyllia corymbosa) around Sulawesi, Indonesia. Biodiversitas 20: 3484-3492. Doi: 10.13057/biodiv/d201204
Umar W, Tassakka ACMAR and Jompa J. 2019c. Potential Uses of Genetic Studies for MPA Design. IOP Conference Series: Earth and Environmental Science. 253. 012032. 10.1088/1755-1315/253/1/012032.
van Oppen MJH, Gates RD. 2006. Conservation genetics and the resilience of reef-building corals. Mol Ecol 15(13): 3863–3883. Doi: 10.1111/j.1365-294X.2006.03026.x
von der Heyden, S. 2017. Making evolutionary history count: biodiversity planning for coral reef fishes and the conservation of evolutionary processes. Coral Reefs 36, 183–194. Doi: 10.1007/s00338-016-1512-2.
Woodhead AJ, Hicks CC, Norström AV, Williams GJ, Graham, NAJ. 2019. Coral reef ecosystem services in the Anthropocene. Functional Ecology 33:1023–1034. Doi: 10.1111/1365-2435.13331.
Wooldridge SA. 2017. Instability and breakdown of the coral–algae symbiosis upon exceedence of the interglacial pCO2 threshold (>260 ppmv): the ‘“missing”’ Earth-System feedback mechanism. Coral Reefs 36:1025–1037. Doi: 10.1007/s00338-017-1594-5
Yasuda N, Nagai S, Hamaguchi M, Okaji K, Gérard K, et al. 2009. Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis. Mol Ecol 18: 1574–1590. Doi: 10.1111/j.1365-294X.2009.04133.x
Yusuf S, Ahmad M, Umar W, Limmon GV, Jompa J. 2019. Biogeography and diversity of Lobophyllia, an ornamental coral traded in the coral triangle. IOP Conference Series: Earth Environ Sci 253: 012030. Doi: 10.1088/1755-1315/253/1/012030.
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