Coral Reefs

, Volume 33, Issue 3, pp 595–606 | Cite as

Cryptic changes in the genetic structure of a highly clonal coral population and the relationship with ecological performance

  • Dana E. Williams
  • M. W. Miller
  • I. B. Baums


Elkhorn coral, Acropora palmata, relies heavily on clonal propagation and often displays low genotypic (clonal) diversity. Populations in the Florida Keys experienced rapid declines in tissue cover between 2004 and 2006, largely due to hurricanes and disease, but remained stable from 2006 to 2010. All elkhorn colonies in 150 m2 permanent study plots were genotyped in 2006 (n = 15 plots) and 2010 (n = 24 plots), and plots sampled in both years were examined for changes in allelic and genotypic diversity during this period of stable ecological abundance. Overall, genetic diversity of Florida plots was low and declined further over the 4-yr period; seven of the 36 original genets and two of 67 alleles (among five microsatellite loci) were lost completely from the sampled population, and an additional 15 alleles were lost from individual reefs. In 2010, Florida plots (~19 colonies) contained an average of 2.2 ± 1.38 (mean ± SD) genets with a significant negative correlation between colony abundance and genotypic diversity. When scaled to total tissue abundance, genotypic diversity is even lower, with 43 % of genets below the size of sexual maturity. We examined the hypothesized positive relationship of local genotypic diversity with ecological performance measures. In Florida plots (n = 15), genotypic diversity was not significantly correlated with tissue loss associated with chronic predation, nor with acute disease and storm-fragmentation events, though this relationship may be obscured by the low range of observed diversity and potential confounding with abundance. When more diverse plots in Curaçao (n = 9) were examined, genotypic diversity was not significantly correlated with resistance during an acute storm disturbance or rate of recovery following disturbance. Cryptic loss of genetic diversity occurred in the apparently stable Florida population and confirms that stable or even increasing abundance does not necessarily indicate genetic stability.


Microsatellites Genotype Disease Predation Florida Keys Acropora palmata 



This work was funded by National Undersea Research Center (2004–2006), NOAA’s Coral Reef Conservation Program (2006–2010) and NOAA Fisheries’ Southeast Regional Office, Protected Resources Division, NSF grant OCE-0825979 and permitted by Florida Keys National Marine Sanctuary. M. Devlin-Durante expertly extracted and genotyped samples. Field assistance from A. Bright, C. Cameron, K. Erickson, C. Fasano, L. Johnston, K. L. Kramer, B. Mason, and R. Wilborn is gratefully acknowledged.

Supplementary material

338_2014_1157_MOESM1_ESM.pdf (223 kb)
Supplementary material 1 (PDF 224 kb)


  1. Alò D, Turner TF (2005) Effects of habitat fragmentation on effective population size in the endangered Rio Grande silvery minnow. Conserv Biol 19:1138–1148CrossRefGoogle Scholar
  2. Arnaud-Haond S, Belkhir K (2007) GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7:15–17CrossRefGoogle Scholar
  3. Bailey JK, Schweitzer JA, Úbeda F, Koricheva J, LeRoy CJ, Madritch MD, Rehill BJ, Bangert RK, Fischer DG, Allan GJ, Whitham TG (2009) From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Phil Trans R Soc Lond 364:1607–1616CrossRefGoogle Scholar
  4. Baums IB, Miller MW, Szmant AM (2003) Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two scleractinian hosts. I: population structure of snails and corals. Mar Biol 142:1083–1091Google Scholar
  5. Baums IB, Hughes CR, Hellberg M (2005a) Mendelian microsatellite loci for the Caribbean hard coral Acropora palmata. Mar Ecol Prog Ser 288:115–127CrossRefGoogle Scholar
  6. Baums IB, Miller MW, Hellberg ME (2005b) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390PubMedCrossRefGoogle Scholar
  7. Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure of a reef-building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519CrossRefGoogle Scholar
  8. Baums IB, Devlin-Durante MK, Brown L, Pinzon JH (2009) Nine novel, polymorphic microsatellite markers for the study of threatened Caribbean acroporid corals. Mol Ecol Resour 9:1155–1158PubMedCrossRefGoogle Scholar
  9. Baums IB, Devlin-Durante MK, Polato NR, Xu D, Giri S, Altman NS, Ruiz D, Parkinson JE, Boulay JN (2013) Genotypic variation influences reproductive success and thermal stress tolerance in the reef building coral, Acropora palmata. Coral Reefs 32:703–717CrossRefGoogle Scholar
  10. Bright AJ, Williams DE, Kramer KL, Miller MW (2013) Recovery of Acropora palmata in Curaçao: a comparison with the Florida Keys. Bull Mar Sci 89:747–757CrossRefGoogle Scholar
  11. Bruckner AW (2002) Proceedings of the Caribbean Acropora Workshop: potential application of the U.S. Endangered Species Act as a conservation strategy. NOAA Technical Memorandum NMFS-OPR-24, Silver Spring, MD, p 199Google Scholar
  12. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:1220–1227CrossRefGoogle Scholar
  13. Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429PubMedCrossRefGoogle Scholar
  14. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortes J, Delbeek JC, Devantier L, Edgar GJ, Edwards AJ, Fenner D, Guzman HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JE, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563PubMedCrossRefGoogle Scholar
  15. Coffroth MA, Lasker HR (1998) Population structure of a clonal gorgonian coral: the interplay between clonal reproduction and disturbance. Evolution 52:379–393CrossRefGoogle Scholar
  16. Drummond EBM, Vellend M (2012) Genotypic diversity effects on the performance of Taraxacum officinale populations increase with time and environmental favorability. PLoS ONE 7:e30314PubMedCrossRefPubMedCentralGoogle Scholar
  17. Ellers J, Rog S, Braam C, Berg MP (2011) Genotypic richness and phenotypic dissimilarity enhance population performance. Ecology 92:1605–1615PubMedCrossRefGoogle Scholar
  18. Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327PubMedCrossRefGoogle Scholar
  19. Frankham R (2005) Ecosystem recovery enhanced by genotypic diversity. Heredity 95:183PubMedCrossRefGoogle Scholar
  20. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226CrossRefGoogle Scholar
  21. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528PubMedCrossRefGoogle Scholar
  22. Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002PubMedCrossRefPubMedCentralGoogle Scholar
  23. Hughes AR, Stachowicz JJ (2009) Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina. Ecology 90:1412–1419PubMedCrossRefGoogle Scholar
  24. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623PubMedCrossRefGoogle Scholar
  25. Hunter CL (1993) Genotypic variation and clonal structure in coral populations with different disturbance histories. Evolution 47:1213–1228CrossRefGoogle Scholar
  26. Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14:537–545PubMedCrossRefGoogle Scholar
  27. Jump AS, Marchant R, Peñuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58PubMedCrossRefGoogle Scholar
  28. Le Goff M, Rogers A (2002) Characterization of 10 microsatellite loci for the deep-sea coral Lophelia pertusa (Linnaeus 1758). Mol Ecol Notes 2:164–166CrossRefGoogle Scholar
  29. Levitan D (1995) The ecology of fertilization in free-spawning invertebrates. In: McEdward LR (ed) Ecology of Marine Invertebrate Larvae. CRC Press, Boca RatonGoogle Scholar
  30. Lirman D (2000) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments. J Exp Mar Biol Ecol 251:41–57PubMedCrossRefGoogle Scholar
  31. Maier E, Tollrian R, Nürnberger B (2001) Development of species-specific markers in an organism with endosymbionts: microsatellites in the scleractinian coral Seriatopora hystrix. Mol Ecol Notes 1:157–159CrossRefGoogle Scholar
  32. McArt SH, Thaler JS (2013) Plant genotypic diversity reduces the rate of consumer resource utilization. Proc R Soc B: Biol Sci 208:20130639. doi: 10.1098/rspb.2013.0639:20130639
  33. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  34. NMFS (2012) Endangered and Threatened wildlife and plants: proposed listing determinations for 82 reef-building coral species; proposed reclassification of Acropora palmata and Acropora cervicornis from Threatened to Endangered. National Marine Fisheries Service, pp 73220–73262Google Scholar
  35. Ohsako T (2010) Clonal and spatial genetic structure within populations of a coastal plant, Carex kobomugi (Cyperaceae). Am J Bot 97:458–470PubMedCrossRefGoogle Scholar
  36. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  37. Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826PubMedCrossRefPubMedCentralGoogle Scholar
  38. Sherman CDH, Ayre DJ, Miller KJ (2006) Asexual reproduction does not produce clonal populations of the brooding coral Pocillopora damicornis on the Great Barrier Reef, Australia. Coral Reefs 25:7–18CrossRefGoogle Scholar
  39. Smouse PE, Peakall ROD, Gonzales EVA (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17:3389–3400PubMedCrossRefGoogle Scholar
  40. Soong K, Lang JC (1992) Reproductive integration in reef corals. Biol Bull 183:418–431CrossRefGoogle Scholar
  41. Souter P, Willis B, Bay L, Caley M, Muirhead A, Van Oppen M (2010) Location and disturbance affect population genetic structure in four coral species of the genus Acropora on the Great Barrier Reef. Mar Ecol Prog Ser 416:35–45CrossRefGoogle Scholar
  42. Stoddart JA, Taylor JF (1988) Genotypic diversity: estimation and prediction in samples. Genetics 118:705–711PubMedPubMedCentralGoogle Scholar
  43. Szmant AM (1986) Reproductive ecology of reef corals. Coral Reefs 5:43–54CrossRefGoogle Scholar
  44. Vardi T, Williams DE, Sandin SA (2012) Population dynamics of threatened elkhorn coral in the northern Florida Keys, USA. Endanger Species Res 19:157–169CrossRefGoogle Scholar
  45. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756PubMedCrossRefGoogle Scholar
  46. Williams DE, Miller MW (2012) Attributing mortality among drivers of population decline in Acropora palmata in the Florida Keys (USA). Coral Reefs 31:369–382CrossRefGoogle Scholar
  47. Williams DE, Miller MW, Kramer KL (2008) Recruitment failure in Florida Keys Acropora palmata, a threatened Caribbean coral. Coral Reefs 27:697–705CrossRefGoogle Scholar
  48. Williams SL, Heck KL (2001) Seagrass community ecology. In: Bertness MD, Gaines SD, Hay ME (eds) Marine Community Ecology. Sinauer Associates, Sunderland, MA, pp 317–338Google Scholar
  49. Willis BL, Ayre DJ (1985) Asexual reproduction and genetic determination of growth form in the coral Pavona cactus: biochemical genetic and immunogenic evidence. Oecologia 65:516–525CrossRefGoogle Scholar

Copyright information

© US Government 2014

Authors and Affiliations

  • Dana E. Williams
    • 1
    • 2
  • M. W. Miller
    • 2
  • I. B. Baums
    • 3
  1. 1.Cooperative Institute for Marine and Atmospheric StudiesUniversity of MiamiMiamiUSA
  2. 2.National Marine Fisheries ServiceSoutheast Fisheries Science CenterMiamiUSA
  3. 3.Department of BiologyThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations