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Coral Reefs

, Volume 37, Issue 1, pp 239–249 | Cite as

Clonal structure and variable fertilization success in Florida Keys broadcast-spawning corals

  • M. W. Miller
  • I. B. Baums
  • R. E. Pausch
  • A. J. Bright
  • C. M. Cameron
  • D. E. Williams
  • Z. J. Moffitt
  • C. M. Woodley
Report

Abstract

Keystone reef-building corals in the Caribbean are predominantly self-incompatible broadcast spawners and a majority are threatened due to both acute adult mortality and poor recruitment. As population densities decline, concerns about fertilization limitation and effective population size in these species increase and would be further exacerbated by either high clonality or gametic incompatibility of parental genotypes. This study begins to address these concerns for two Caribbean broadcasting species by characterizing clonal structure and quantifying experimental pairwise fertilization success. Orbicella faveolata showed surprisingly high and contrasting levels of clonality between two sampled sites; Acropora palmata was previously known to be highly clonal. Individual pairwise crosses of synchronously spawning genotypes of each species were conducted by combining aliquots of gamete bundles immediately after spawning, and showed high and significant variability in fertilization success. Over half of the individual crosses of O. faveolata and about one-third of A. palmata crosses yielded ≤ 40% fertilization. Total sperm concentration was quantified in only a subset of O. faveolata crosses (range of 1–6 × 107 mL−1), but showed no correlation with fertilization success. We interpret that both parental incompatibility and individual genotypes with low-quality gametes are likely to have contributed to the variable fertilization observed with important implications for conservation. Differential fertilization success implies effective population size may be considerably smaller than hoped and population enhancement efforts need to incorporate many more parental genotypes at the patch scale to ensure successful larval production than indicated by estimates based simply on preserving levels of standing genetic diversity.

Keywords

Genotype Acropora palmata Orbicella faveolata Larval production Microsatellites 

Notes

Acknowledgements

This project was made possible by funding from the NOAA Coral Reef Conservation Program, logistic support from the Florida Keys National Marine Sanctuary, and field and laboratory assistance from A. Chan, M. Devlin-Durante, B. Huntington, L. Richter, K. Kerr, L. MacLaughlin, M. Connelly, J. Fisch, C. Page, and A. Burnett. Work was conducted under permit FKNMS-2014-047.

References

  1. Baums IB, Hughes CR, Hellberg M (2005) Mendelian microsatellite loci for the Caribbean hard coral Acropora palmata. Mar Ecol Prog Ser 288:115–127CrossRefGoogle Scholar
  2. 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
  3. Baums I, Johnson M, Devlin-Durante M, Miller M (2010) Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean. Coral Reefs 29:835–842CrossRefGoogle Scholar
  4. 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
  5. Brainard RE, Birkeland C, Eakin CM, McElhany P, Miller MW, Patterson M, Piniak GA (2011) Status review report of 82 candidate coral species petitioned under the U.S. Endangered Species Act. NOAA Technical Memorandum NOAA-TM-NMFS-PIFSC-27. U.S. Department of Commerce, Honolulu, HI, 530 ppGoogle Scholar
  6. Fogarty ND, Vollmer SV, Levitan DR (2012a) Weak prezygotic isolating mechanisms in threatened Caribbean Acropora corals. PLoS One 7:e30486CrossRefPubMedPubMedCentralGoogle Scholar
  7. Fogarty ND, Lowenberg M, Ojima MN, Knowlton N, Levitan DR (2012b) Asymmetric conspecific sperm precedence in relation to spawning times in the Montastraea annularis species complex (Cnidaria: Scleractinia). J Evol Biol 25:2481–2488CrossRefPubMedGoogle Scholar
  8. Foster N, Baums I, Mumby P (2007) Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis. J Anim Ecol 76:384–391CrossRefPubMedGoogle Scholar
  9. Foster NL, Baums IB, Sanchez JA, Paris CB, Chollett I, Agudelo CL, Vermeij MJA, Mumby PJ (2013) Hurricane-driven patterns of clonality in an ecosystem engineer: the Caribbean coral Montastraea annularis. PLoS One 8:e53283CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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 142:679–684CrossRefGoogle Scholar
  11. Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963CrossRefGoogle Scholar
  12. Iwao K, Wada N, Ohdera A, Omori M (2014) How many donor colonies should be cross-fertilized for nursery farming of sexually propagated corals? Natural Resources 5:521–526CrossRefGoogle Scholar
  13. Kenkel CD, Traylor MR, Wiedenmann J, Salih A, Matz MV (2011) Fluorescence of coral larvae predicts their settlement response to crustose coralline algae and reflects stress. Proc R Soc Lond B Biol Sci 278:2691–2697CrossRefGoogle Scholar
  14. Levitan DR, Boudreau W, Jara J, Knowlton N (2014) Long-term reduced spawning in Orbicella coral species due to temperature stress. Mar Ecol Prog Ser 515:1–10CrossRefGoogle Scholar
  15. 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 65:1254–1270CrossRefPubMedGoogle Scholar
  16. Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308–323CrossRefPubMedGoogle Scholar
  17. Lirman D, Schopmeyer S (2016) Ecological solutions to reef degradation: optimizing coral reef restoration in the Caribbean and Western Atlantic. PeerJ 4:e2597CrossRefPubMedPubMedCentralGoogle Scholar
  18. Miller M, Williams D, Fisch J (2016) Genet-specific spawning patterns in Acropora palmata. Coral Reefs 35:1393–1398CrossRefGoogle Scholar
  19. Oliver J, Babcock R (1992) Aspects of the fertilization ecology of broadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. The Biological Bulletin 183:409–417CrossRefPubMedGoogle Scholar
  20. 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
  21. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  22. Quigley KM, Willis BL, Bay LK (2016) Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis. R Soc Open Sci 3:160471CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij MJA, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci 38:437–457CrossRefGoogle Scholar
  24. Severance EG, Szmant AM, Karl SA (2004) Microsatellite loci isolated from the Caribbean coral, Montastraea annularis. Mol Ecol Notes 4:74–76CrossRefGoogle Scholar
  25. Shearer TL, Porto I, Zubillaga AL (2009) Restoration of coral populations in light of genetic diversity estimates. Coral Reefs 28:727–733CrossRefPubMedPubMedCentralGoogle Scholar
  26. Smouse PE, Peakall ROD, Gonzales EVA (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17:3389–3400CrossRefPubMedGoogle Scholar
  27. Szmant AM, Weil E, Miller MW, Colon DE (1997) Hybridization within the species complex of the scleractinan coral Montastraea annularis. Mar Biol 129:561–572CrossRefGoogle Scholar
  28. Williams DE, Miller M, Baums I (2014) Cryptic changes in the genetic structure of a highly clonal coral population and the relationship with ecological performance. Coral Reefs 33:595–606CrossRefGoogle Scholar
  29. Willis BL, Babcock RC, Harrison PL, Wallace CC (1997) Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16:S53–S65CrossRefGoogle Scholar

Copyright information

© US Government 2017

Authors and Affiliations

  1. 1.Southeast Fisheries Science CenterNational Marine Fisheries ServiceMiamiUSA
  2. 2.Department of BiologyThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Cooperative Institute of Marine and Atmospheric StudiesUniversity of MiamiMiamiUSA
  4. 4.JHT, Inc. Contractor to NOAAOrlandoUSA
  5. 5.National Centers for Coastal Ocean ScienceNOAA National Ocean ServiceCharlestonUSA
  6. 6.SECORE InternationalMiamiUSA

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