Skip to main content

Advertisement

Log in

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

Coral Reefs Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3: a
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baums IB, Hughes CR, Hellberg M (2005) Mendelian microsatellite loci for the Caribbean hard coral Acropora palmata. Mar Ecol Prog Ser 288:115–127

    Article  CAS  Google Scholar 

  • Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure of a reef-building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519

    Article  Google Scholar 

  • 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 29:835–842

    Article  Google Scholar 

  • 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 32:703–717

    Article  Google Scholar 

  • 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 pp

  • Fogarty ND, Vollmer SV, Levitan DR (2012a) Weak prezygotic isolating mechanisms in threatened Caribbean Acropora corals. PLoS One 7:e30486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:2481–2488

    Article  CAS  PubMed  Google Scholar 

  • Foster N, Baums I, Mumby P (2007) Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis. J Anim Ecol 76:384–391

    Article  PubMed  Google Scholar 

  • 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:e53283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 142:679–684

    Article  Google Scholar 

  • Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963

    Article  Google Scholar 

  • 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 5:521–526

    Article  Google Scholar 

  • 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 278:2691–2697

    Article  CAS  Google Scholar 

  • 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 515:1–10

    Article  Google Scholar 

  • 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 65:1254–1270

    Article  PubMed  Google Scholar 

  • 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 58:308–323

    Article  PubMed  Google Scholar 

  • Lirman D, Schopmeyer S (2016) Ecological solutions to reef degradation: optimizing coral reef restoration in the Caribbean and Western Atlantic. PeerJ 4:e2597

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller M, Williams D, Fisch J (2016) Genet-specific spawning patterns in Acropora palmata. Coral Reefs 35:1393–1398

    Article  Google Scholar 

  • 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 183:409–417

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3:160471

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 38:437–457

    Article  Google Scholar 

  • Severance EG, Szmant AM, Karl SA (2004) Microsatellite loci isolated from the Caribbean coral, Montastraea annularis. Mol Ecol Notes 4:74–76

    Article  CAS  Google Scholar 

  • Shearer TL, Porto I, Zubillaga AL (2009) Restoration of coral populations in light of genetic diversity estimates. Coral Reefs 28:727–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smouse PE, Peakall ROD, Gonzales EVA (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17:3389–3400

    Article  PubMed  Google Scholar 

  • Szmant AM, Weil E, Miller MW, Colon DE (1997) Hybridization within the species complex of the scleractinan coral Montastraea annularis. Mar Biol 129:561–572

    Article  Google Scholar 

  • 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 33:595–606

    Article  Google Scholar 

  • 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–S65

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. W. Miller.

Additional information

Communicated by Biology Editor Dr. Line K. Bay

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miller, M.W., Baums, I.B., Pausch, R.E. et al. Clonal structure and variable fertilization success in Florida Keys broadcast-spawning corals. Coral Reefs 37, 239–249 (2018). https://doi.org/10.1007/s00338-017-1651-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-017-1651-0

Keywords

Navigation