Abstract
Most hard corals have broad distributions, and historically this was attributed to their capability for extensive dispersal leading to high evolutionary and demographic inter-dependence among regions. More recently there has been a paradigm shift in the understanding of coral dispersal, driven largely by genetic evidence, which has put greater emphasis on self-recruitment and larval retention. There is now a growing body of evidence that morphologically cryptic species exist within many recognized ‘species’ of stony corals. Here, we characterise levels of genetic divergence within and between five species of Acropora sampled from disparate populations spanning the Indo-Pacific Oceans. We find that strong regional genetic differentiation corresponding to the separation of the Indian and Pacific Ocean basins is a consistent pattern in three of the five species examined. Furthermore, the extent of allopatric divergence within species is similar to that observed between species, implying negligible contemporary gene flow between regions in four of the five species examined. This is consistent with the presence of numerous morphologically cryptic allopatric subspecies or incipient Acropora species. If this is confirmed, the conservation status of several species, which are already demonstrably threatened, would require re-evaluation so that risks including silent extinctions and inappropriate translocations are properly managed.
Similar content being viewed by others
References
Aitken SN, Whitlock MC (2013) Assisted gene flow to facilitate local adaptation to climate change. An Rev Ecol Evol Syst 44:367–388
Allendorf FW, Luikart G (2009) Conservation and the genetics of populations. John Wiley and Sons
Arrigoni R, Terraneo TI, Galli P, Benzoni F (2014a) Lobophylliidae (Cnidaria, Scleractinia) reshuffled: pervasive non-monophyly at genus level. Mol Phy Evol 73:60–64
Arrigoni R, Richards ZT, Chen CA, Baird AH, Benzoni F (2014b) Taxonomy and phylogenetic relationships of the coral genera Australomussa and Parascolymia (Scleractinia, Lobophylliidae). Cont Zool 83:195–215
Avise JC (1989) A role for molecular genetics in the recognition and conservation of endangered species. TREE 4:279–281
Ayre DJ, Dufty S (1994) Evidence for restricted gene flow in the viviparous coral Seriatopora hystrix on Australia’s Great Barrier Reef. Evolution 48:1183–1201
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
Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) A marine Wallace’s line. Nature 406:692–693
Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2002) Sharp genetic breaks among populations of Haptosqulla pulchella (Stomatopoda) indicate limits to larval transport patterns, causes and consequences. Mol Ecol 11:59–674
Barber PH, Erdmann MV, Palumbi SR (2006) Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the coral triangle. Evolution 60:1825–1839
Baron-Szabo RC (2006) Corals of the K/T boundary: Scleractinian corals of the suborders Astrocoeniina, Faviina, Rhipidogyrina and Amphiastaena. J Syst Palaeo 4:1–108
Baums IB, Hughes CR, Hellberg MH (2005) Mendlian microsatellite loci for the Caribbean coral Acropora palmata. Mar Ecol Prog Ser 231:91–99
Baums IB, Boulay JN, Polato NR, Hellberg ME (2012) No gene flow across the Eastern Pacific Barrier in the reef-building coral Porites lobata. Mol Ecol 21:5418–5433
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300
Benjamini Y, Yekutieli D (2001) The control of false discovery rate under dependency. Ann Stat 29:1165–1188
Benzie JAH (1994) Patterns of gene flow in the Great Barrier Reef and Coral Sea. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 67–79
Benzie JAH, Ballment E, Forbes AT et al (2002) Mitochondrial DNA variation in Indo-Pacific populations of the giant tiger prawn, Penaeus monodon. Mol Ecol 11:2553–2569
Benzoni F, Stefani F, Pichon M, Galli P (2010) The name game: morpho-molecular species boundaries in the genus Psammocora (Cnidaria, Scleractinia). Zool J Linn Soc 160:421–456
Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJ et al (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS ONE 5:e10871
Boulay JN, Hellberg ME, Cortés J, Baums IB (2014) Unrecognized coral species diversity masks differences in functional ecology. Proc Roy Soc London B 281:20131580
Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:1558–1561
Budd AF, Fukami H, Smith ND, Knowlton N (2012) Taxonomic classification of the reef coral family Mussidae (Cnidaria: anthozoa: Scleractinia). Zool J Linn Soc 166:465–529
Carbone F, Matteucci R, Pignatti JS, Russo A (1993) Racies analysis and biostratigraphy of the Auradu limestone formation in the Berbera-Sheikh area, north-western Somalia. Geol Rom 29:213–235
Carpenter K, Abrar M, Aeby G et al (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563
Concepcion GT, Baums IB, Toonen RJ (2014) Regional population structure of Montipora capitata across the Hawaiian archipelago. Bull Mar Sci 90:257–275
Duda TF, Palumbi SR (1999) Population structure of the black tiger prawn, Penaeus monodon, among western Indian Ocean and western Pacific populations. Mar Biol 134:705–710
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Faith DP, Richards ZT (2012) Climate change impacts on the tree of life: changes in phylogenetic diversity illustrated for Acropora corals. Biology 1:906–932
Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:1571–1583
Forsman ZH, Johnston EC, Brooks AJ, Adam TC, Toonen RJ (2013) Genetic evidence for regional isolation of Pocillopora corals from Moorea. Oceanography 26:153–155
Froukh T, Kochzius M (2008) Species boundaries and evolutionary lineages in the blue green damselfishes Chromis viridis and Chromis atripectoralis (Pomacentridae). J Fish Biol 72:451–457
Gaither MR, Rocha LA (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. J Biog 40:1638–1648
Gittenberger A, Reijnen BT, Hoeksema BW (2011) A molecularly based phylogeny reconstruction of mushroom corals (Scleractinia:Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Cont Zool 80:107–132
Gordon AL, Fine RA (1996) Pathways of water between the Pacific and Indian Oceans. Nature 379:146–149
Goudet J (2001) Fstat version 1.2: a computer program to calculate Fstastics. J Heredity 86:485–486
Hardie DC, Hutchings JA (2010) Evolutionary ecology at the extremes of species' ranges. Env Revs 18:1–20
Haq BU, Hardenbol J, Vail PR (1987) Chronology of fluctuating sea levels since the Triassic. Science 235:1156–1167
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Hellberg ME, Balch DP, Roy K (2001) Climate driven range expansion and morphological evolution in a marine gastropod. Science 292:1707–1710
Hoegh-Guldberg O (2011) Coral reef ecosystems and anthropogenic climate change. Reg Env Ch 11:215–227
Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, Thomas CD (2008) Assisted colonization and rapid climate change. Science 321:345–346
Huang D (2012) Threatened reef corals of the world. PLoS ONE 7:e34459–e34459
Huang D, Roy K (2015) The future of evolutionary diversity in reef corals. Phil Trans Roy Soc Lon B: Biol Sci 70:20140010
Huang D, Licuanan WY, Baird AH, Fukami H (2011) Cleaning up the ‘Big messidae’: molecular phylogeny of scleractinian corals from Faviidae, Merulinidae Pectiniidae and Trachyphylliidae. BMC Evol Biol 11:37
Hughes TP, Bellwood DR, Connolly SR, Cornell HV, Karlson RH (2014) Double jeopardy and global extinction risk in corals and reef fishes. Cur Biol 24:2946–2951
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
Keshavmurthy S, Yang SY, Alamaru A, ChuangYY Pichon M et al (2013) DNA barcoding reveals the coral “laboratory-rat” Stylophora pistillata encompasses multiple identities. Sci Rep 3:1–7
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kitano YF, Benzoni F, Arrigoni R, Shirayama Y, Wallace CC, Fukami H (2014) A phylogeny of the family Poritidae (Cnidaria, Scleractinia) based on molecular and morphological analyses. PLOS One e98406
Knittweis L, Kramer WE, Timm J, Kochizius M (2008) Genetic structure of Heliofungia actiniformis (Scleractinia: fungiidae) populations in the Indo-Malay Archipelago: implications for live coral trade management efforts. Cons Gen 10:241–249
Knittweis L, Kraemer WE, Timm J, Kochzius M (2009) Genetic structure of Heliofungia actiniformis (Scleractinia: fungiidae) populations in the Indo-Malay Archipelago: implications for live coral trade management efforts. Cons Gen 10:241–249
Knowlton N (1993) Sibling species in the sea. ARES 189–216
Knowlton N (2001) Who are the players on coral reefs and does it matter? The importance of coral taxonomy for coral reef management. Bull Mar Sci 69:305–308
Kochzius M, Nuryanto A (2008) Strong genetic population structure in the boring giant clam, Tridacna crocea, across the Indo-Malay Archipelago: implications related to evolutionary processes and connectivity. Mol Ecol 17:3775–3787
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Res 15:1179–1191
Marti-Puig P, Forsman ZH, Haverkort-Yeh RD, Knapp ISS, Maragos JE, Toonen RJ (2014) Extreme phenotypic polymorphism in the coral genus Pocillopora; micro-morphology corresponds to mitochondrial groups, while colony morphology does not. Bull Mar Sci 90:211–231
McMillan WO, Palumbi SR (1995) Concordant evolutionary patterns among Indo-West Pacific butterflyfishes. Proc Roy Soc Lond 260:229–236
Miller KJ, Benzie JAH (1997) No clear genetic distinction between morphological species within the coral genus Platygyra. Bull Mar Sci 61:907–917
Moritz C (1994) Defining ‘Evolutionarily Significant Units’ for conservation. TREE 9:373–375
Moritz C, Broderick D, Dethmers K, Fitzsimmons N, Limpus CJ (2002) Population genetics of Southeast Asian and Western Pacific green turtles, Chelonia mydas. Final Report to UNEP/CMS. 42 p
Nakajima Y, Nishikawa A, Iguchi A, Sakai K (2012) The population genetic approach delineates the species boundary of reproductively isolated corymbose acroporid corals. Mol Phylo Evol 63:527–531
Nakajima Y, Shinzato C, Satoh N, Mitarai S (2015) Novel polymorphic microsatellite markers reveal genetic differentiation between two sympatric types of Galaxea fascicularis. PLoS ONE 10:e0130176
Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Cons Gen 7:783–787
Nei (1973) Analysis of gene diversity in subdivided populations. PNAS 70:3321–3323
Nelson JS, Hoddell RJ, Chou LM, Chan WK, Phang VPE (2000) Phylogeographhic structure of false clownfish, Amphiprion ocellaris, explained by sea level changes on the Sunda shelf. Mar Biol 137:727–736
Noreen AME, van Oppen MJH, Harrison PL (2013) Genetic diversity and differentiation among high-latitude broadcast-spawning coral populations disjunct from the core range. Mar Ecol Prog Ser 491:101–109
Noreen AM, Schmidt-Roach S, Harrison P, van Oppen MJ (2015) Diverse associations among coral host haplotypes and algal endosymbionts may drive adaptation at geographically peripheral and ecologically margninal locations. J Biog 42:1639–1650
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:47–572
Pandolfi JM (1992) Successive isolation rather than evolutionary centres for the origination of Indo-Pacific reef corals. J Biogeog 593–609
Peakall R, Smouse PE (2005) GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research, Australian National University, Australia
Pinzón JH, LaJeunesse T (2011) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol 20:311–325
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousseu F (1995) Genepop (version 1.2). Population genetics software for exact tests and eumenicism. J Hered 86:248–249
Renema W, Bellwood DR, Braga JC, Bromfield K, Hall R et al (2008) Hopping hotspots: global shifts in marine biodiversity. Science 321:654–657
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. ARES 27:83–105
Richards ZT, van Oppen M (2012) Rarity and genetic diversity in Indo-Pacific Acropora corals. Ecol Evol 2:1867–1888
Richards ZT, van Oppen MJH, Wallace CC, Willis BL, Miller DJ (2008) Some rare Indo-Pacific coral species are probable hybrids. PLoS ONE 3:e3240
Richards ZT, Miller DJ, Wallace CC (2013) Molecular phylogenetics of geographically restricted Acropora species: implications for threatened species conservation. Mol Phy Evol 69:837–851
Robertson DN, Butler MJ (2009) Variable reproductive success in fragmented populations. J Exp Mar Biol Ecol 24:5006–5019
Rosser NL (2015) Asynchronous spawning in sympatric populations of a hard coral reveals cryptic species and ancient genetic lineages. Mol Ecol 24:5006–5019
Schmidt-Roach S, Lundgren P, Miller KJ, Gerlach G, Noreen AME, Andreakis N (2013) Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32:161–172
Starger CJ, Barber PH, Erdmann MV, Toha AH, Baker AC (2013) Strong genetic structure among coral populations within a conservation priority region, the Bird’s Head Seascape (Papua and West Papua, Indonesia). PeerJ e25v1
Stephens PA, Sutherland WJ, Freckleton RP (1999) What is Allele effect. Oikos 87:185–190
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Timm J, Figiel M, Kochzius M (2008) Contrasting patterns in species boundaries and evolution of anemonefishes (Amphiprioninae, Pomacentridae) in the centre of marine biodiversity. Mol Phy Evol 49:268–276
Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337
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 16:771–784
Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2009) Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience. Ecol App 19:18–29
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Microchecker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
van Oppen MJH, McDonald BJ, Willis BL, Miller DJ (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence. Mol Biol Evol 18:1315–1329
van Oppen MJ, Underwood JN, Muirhead AN, Peplow L (2007) Ten microsatellite loci for the reef-building coral Acropora millepora (Cnidaria, Scleractinia) from the Great Barrier Reef, Australia. Mol Ecol Notes 7:436–438
van Oppen MJH, Lutz A, De’ath G, Peplow L, Kininmonth S (2008) Genetic traces of recent long-distant dispersal in a predominantly self-recruiting coral. PLoS ONE 3:e3401
van Oppen MJ, 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 20:1647–1660
van Oppen MJ, Lukoschek V, Berkelmans R, Peplow LM, Jones AM (2015) A population genetic assessment of coral recovery on the highly disturbed reefs of the Keppel Island archipelago in the Southern Great Barrier Reef. PeerJ 3:e1092
Veron JEN (2000) Corals of the world. Australian Institute of Marine Science. Vol 1
Veron JEN, Wallace CC (1984) Scleractinia of Eastern Australia, Part V. Family Acroporidae. AIMS Monograph Series 6:485 pp
Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167
Wallace CC (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO Publishing, Australia
Wallace CC (2001) Wallace’s line and marine organisms: the distribution of staghorn corals (Acropora) in Indonesia. Swets and Zeitlinger, Faunal and Floral Migrations and Evolution in SE Asia-Australia, pp 171–181
Wallace CC, Rosen BR (2006) Diverse staghorn corals (Acropora) in high latitude Eocene assemblages: implications for the evolution of modern diversity patterns in reef corals. Proc Royal Soc B 273:975–982
Wallace CC, Wolstenholme J (1998) Revision of the coral genus Acropora (Scleractinia: astrocoeniina: Acroporidae) in Indonesia. Zool J Linnean Soc 123(3):199–384
Waples RS (1995) Evolutionary significant units and the conservation of biological diversity under the Endangered Species Act. Am Fish Soc Symp 17:8–27
Warner PA, van Oppen M, Willis BL (2015) Unexpected cryptic species diversity in the widespread coral Seriatopora hystrix masks spatial-genetic patterns of connectivity. Mol Ecol. doi:10.1111/mec.13225
Williams ST, Benzie JAH (1997) Indo-West Pacific patterns of genetic differentiation in the high-dispersal starfish Linckia laevigata. Mol Ecol 6:559–573
Williams ST, Benzie JAH (1998) Evidence of a biogeographic break between populations of a high dispersal starfish: congruent regions within the Indo-West Pacific defined by color morphs, Mt DNA and allozyme data. Evolution 52:87–99
Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Ann Rev Ecol Evol Syst 37:489–517
Wilson ME, Rosen BR (1998) Implications of paucity of corals in the Paleogene of SE Asia: plate techtonics or centre of origin? In: Hall R, Holloway JD (eds) Biogeography and Geological Evolution of SE Asia. Backhuys Publishers, Leiden, pp 165–195
Woodland DJ (1983) Zoogeography of the Siganidae (Pisces): an interpretation of distribution and richness patterns. Bull Mar Sci 33:713–717
Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Kackson FBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watxon R (2007) Impacts of biodiversity loss on ocean ecosystem services. Science 318:1737–1742
Yasuda N, Taquet C, Nagai S, Fortes M, Fan TY, Phongsuwan N, Nadaoka K (2014) Genetic structure and cryptic speciation in the threatened reef-building coral Heliopora coerulea along Kuroshio Current. Bull Mar Sci 90(1):233–255
Acknowledgments
Thanks to staff of the Orpheus Island Research Station, the College of the Marshall Islands and the Walindii Research Station. We gratefully acknowledge our colleagues who collected additional samples used in this study (Akira Iguchi; Natalie Rosser; David Abrego; Paul Muir). Thank you to Carden Wallace for verifying specimen identifications and Barbara Done for specimen curation at the Museum of Tropical Queensland. We thank Lesa Peplow and Mr. Andy Muirhead for their assistance in labwork conducted at the Australian Institute of Marine Science. We appreciate the constructive comments by an anonymous reviewer. ZR was supported by an Australian Postgraduate Fellowship at James Cook University and an International Society for Reef Studies Fellowship. ZR was supported in the write-up phase by Woodside Energy.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Richards, Z.T., Berry, O. & van Oppen, M.J.H. Cryptic genetic divergence within threatened species of Acropora coral from the Indian and Pacific Oceans. Conserv Genet 17, 577–591 (2016). https://doi.org/10.1007/s10592-015-0807-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-015-0807-0