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Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef

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Abstract

Adaptation to localised thermal regimes is facilitated by restricted gene flow, ultimately leading to genetic divergence among populations and differences in their physiological tolerances. Allozyme analysis of six polymorphic loci was used to assess genetic differentiation between nine populations of the reef-building coral Acropora millepora over a latitudinal temperature gradient on the inshore regions of the Great Barrier Reef (GBR). Small but significant genetic differentiation indicative of moderate levels of gene flow (pairwise F ST 0.023 to 0.077) was found between southern populations of A. millepora in cooler regions of the GBR and the warmer, central or northern GBR populations. Patterns of genetic differentiation at these putatively neutral allozyme loci broadly matched experimental variation in thermal tolerance and were consistent with local thermal regimes (warmest monthly-averages) for the A. millepora populations examined. It is therefore hypothesized that natural selection has influenced the thermal tolerance of the A. millepora populations examined and greater genetic divergence is likely to be revealed by examination of genetic markers under the direct effects of natural selection.

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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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741

    Article  Google Scholar 

  • Benzie JAH (1994) Patterns of gene flow in the Great Barrier Reef and Coral Sea. In: Beaumont AR (eds) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 67–79

  • Berkelmans R (2001) Bleaching, upper thermal limits and temperature adaptation in reef corals. PhD Thesis, James Cook University of North Queensland, p 179

  • Berkelmans R (2002) Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Mar Ecol Prog Ser 229:73–82

    Google Scholar 

  • Berkelmans R, Oliver JK (1999) Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18:55–60

    Article  Google Scholar 

  • Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc Lond B Biol Sci (in press)

  • Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns and predictions. Coral Reefs 22:74–83

    Article  Google Scholar 

  • Bettencourt BR, InYoung K, Hoffmann AA, Feder ME (2002) Response to natural and laboratory selection at the Drosophila hsp70 genes. Evolution 56:1796–1801

    Article  Google Scholar 

  • Boyer SH, Fainer DC, Watson-Williams EJ (1963) Lactate dehydrogenase variant from human blood: evidence for molecular sub-units. Science 141:642–643

    Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455

    Article  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Article  Google Scholar 

  • Burrage DM, Steinberg CR, Skirving WJ, Kleypas JA (1996) Mesoscale circulation features of the Great Barrier Reef Region inferred from NOAA satellite imagery. Remote Sens Environ 56:21–41

    Article  Google Scholar 

  • Davies P (1994) Evolution of the Great Barrier Reef. Aust Geol 92:21–24

    Article  Google Scholar 

  • Doherty PJ, Planes S, Mather P (1995) Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology 76:2373–2391

    Article  Google Scholar 

  • Done T, Whetton P, Jones R, Berkelmans R, Lough J, Skirving W, Wooldridge S (2003) Global climate change and coral bleaching on the Great Barrier Reef. CSIRO, Australian Institute of Marine Science and CRC Reef research centre, Townsville

  • Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13:2445–2458

    Article  Google Scholar 

  • Frydenber J, Hoffmann AA, Loeschcke V (2003) DNA sequence variation and latitudinal associations in hsp23, hsp26 and hsp27 from natural populations of Drosophila melanogaster. Mol Ecol 12:2025–2032

    Article  Google Scholar 

  • Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17

    Article  Google Scholar 

  • Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Nino-Southern Oscillation Event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109

    Google Scholar 

  • Gomez-Mestre I, Tejedo M (2004) Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of the natterjack Toad Bufo calamita. Evolution 58:2343–2352

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test for Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • Hoegh-Guldberg O (2004) Coral reefs in a century of rapid environmental change. Symbiosis 37:1–32

    Google Scholar 

  • Hoffmann AA, Anderson A, Hallas R (2002) Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecol Lett 5:614–618

    Article  Google Scholar 

  • Lewis PO, Zaykin D (2002) Genetic data analysis: computer program for the analysis of allelic data. Version 1.0 (d16c). Free program distributed by the authors available from http://www.hydrodictyon.eeb.uconn.edu/people/plewis/software.php

  • Luttikhuizen PC, Drent J, Van Delden W, Piersma T (2003) Spatially structured genetic variation in a broadcast spawning bivalve: quantitative vs. molecular traits. J Evol Biol 16:260–272

    Article  Google Scholar 

  • McCulloch M, Fallon S, Wyndham T, Hendy E, Lough J, Barnes D (2003) Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421:727–730

    Article  Google Scholar 

  • Merila J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903

    Article  Google Scholar 

  • Miller MP (1997) Tools for population genetic analyses (TFPGA) Version 1.3, available as free software from http://www.marksgeneticsoftware.net/

  • Ottaviano E, Gorla MS, Pe E, Frova C (1991) Molecular markers (RFLPs and HSPs) for genetic dissection of thermotolerance in maize. Theor Appl Genet 81:713–719

    Article  Google Scholar 

  • Peakall R, Smouse PE (2001) GenAlEx V5: Genetic Analysis in Excel. Population genetic software for teaching and research. Australian National University, Canberra, Austalia http://www.anu.edu.au/BoZo/GenAlEx/

  • Perry GM, Danzmann RG, Ferguson MM, Gibson JP (2001) Quantitative trait loci for upper thermal tolerance in outbred strains of rainbow trout (Oncorhynchus mykiss). Heredity 86:333–341

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Raymond M, Rousset F (1999) GENEPOP Version 3.1d, latest versions of this free software available from http://www.wbiomed.curtin.edu.au/genepop/

  • Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis: a handbook for animal systematics and populations studies. Academic, Sydney

    Google Scholar 

  • Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742

    Article  Google Scholar 

  • Selander RK, Smith MH, Yang SY, Johnson WE, Gentry JB (1971) Biochemical polymorphism and systematics in the genus Peromyscus 1. Variation in the old field mouse (Peromyscus polinotus) Studies in Genetics VI. University of Texas Publication 7103, pp 49–90

  • Shaw CR, Prasard R (1970) Starch gel electrophoresis of enzymes—a compilation of recipes. Biochem Genet 4:297–320

    Article  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Google Scholar 

  • Smith CR (2005) The role of genetic and environmental variation on thermal tolerance of a reef-building coral, Acropora millepora. PhD thesis, University of Queensland, p 166

  • Smith LD, Hughes TP (1999) An experimental assessment of survival, re-attachment and fecundity of coral fragments. J Exp Mar Biol Ecol 235:147–164

    Article  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Willis DPM, Shipley PF (2004a) Micro-checker version 2.2.1 An application for checking microsatellite data for null alleles available from http://www.microchecker.hull.ac.uk

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004b) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. Am Genetic Assoc 89:438–450

    Google Scholar 

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

    Article  Google Scholar 

  • Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619

    Article  Google Scholar 

  • Wilkinson C (2000) The 1997–98 mass coral bleaching and mortality event: 2 years on. In: Wilkinson C (eds) Status of coral reefs of the world: 2000. Australian Institute of Marine Science, Townsville, pp 21–34

  • Williams DM (2001) Impacts of terrestrial run-off on the GBRWHA. Report to CRC Reef, Townsville, Queensland

  • Worheide G, Hooper JNA, Degnan BM (2002) Phylogeography of western Pacific Leucetta ‘chagosensis’ (Porifera: Calcarea) from ribosomal DNA sequences: implications for population history and conservation of the Great Barrier Reef World Heritage Area (Australia). Mol Ecol 11:1753–1768

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    Google Scholar 

Download references

Acknowledgements

We thank Dr. C. van Oosterhout for advice on calculation of null allele frequencies. We thank Dr. T. Done and Mary Wakeford from the Australian Institute of Marine Science, Professor Ove Hoegh-Guldberg and Dr. Sophie Dove from the University of Queensland, Dr. Dean Jerry from James Cook University, Dr. Howard Lasker and two anonymous reviewers for their helpful comments on the manuscript. We thank Dr. Ray Berkelmans for his assistance in the laboratory and his help with field collections. This research was supported by an Australian Institute of Marine Science supplementary research award to C. Smith-Keune.

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Authors and Affiliations

  1. Australian Institute of Marine Science, PMB 3, Townsville MC, QLD 4810, Australia

    Carolyn Smith-Keune & Madeleine van Oppen

  2. Centre for Marine Studies, University of Queensland, St Lucia, QLD, Australia

    Carolyn Smith-Keune

Authors
  1. Carolyn Smith-Keune
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  2. Madeleine van Oppen
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Correspondence to Carolyn Smith-Keune.

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Communicated by Biology Editor H.R. Lasker

Appendix

Appendix

Table 4.

Table 4 Observed and adjusted allele frequencies for six polymorphic allozyme loci for Acropora millepora collected on nine reefs of the GBR
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Smith-Keune, C., van Oppen, M. Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef. Coral Reefs 25, 493–502 (2006). https://doi.org/10.1007/s00338-006-0129-2

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