Skip to main content
Log in

Changes in spawning time led to the speciation of the broadcast spawning corals Acropora digitifera and the cryptic species Acropora sp. 1 with similar gamete recognition systems

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Multi-species spawning is reported in the coral genus Acropora, but hybridization in nature rarely occurs because of the incompatibility of gametes and the timing of spawning. However, the evolutionary relationships between gamete compatibility and spawning time are obscure. Investigations of gamete compatibility in sister species that spawn at different times may provide clues to answering this question. Acropora sp. 1 has been defined as a cryptic species of Acropora digitifera, and they are morphologically similar, but spawn in different months, suggesting that they are either a cryptic species or a different species. We examined the morphology and conducted crossing experiments using cryopreserved sperm. The morphologies (branch length, branch width, and outer diameter of axial corallites) of A. digitifera and Acropora sp. 1 differed significantly. A phylogenetic tree of partial Pax-C nuclear sequences from A. digitifera and Acropora sp. 1 shows that they are monophyletic and closely related genetically, based on F ST values and P-distance. These results imply that these two species originated recently from a common ancestor. In addition, cryopreserved sperm from both A. digitifera and Acropora sp. 1 showed bidirectional inter-crossing (cryopreserved sperm of A. digitifera and eggs of Acropora sp. 1 from Sesoko: 32.1 ± 6.7 %, control-conspecific cryopreserved sperm and eggs: 46.1 ± 10.6 %; cryopreserved sperm of Acropora sp. 1 and eggs of A. digitifera from Oku: 63.3 ± 16.6 %, control: 83.6 ± 6.0 %). The results suggest that the gametes of these two species are compatible and that the pre-zygotic isolation mechanism is relaxed because their gametes do not interact. Overall, these two species should be classified as distinct species, and changes in spawning time are related to speciation in a similar gamete recognition system.

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.

Fig. 1
Fig. 2
Fig. 3

References

  • Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394

    Article  Google Scholar 

  • Baird AH, Kospartov MC, Purcell S (2010) Reproductive synchrony in Acropora assemblages on reefs of New Caledonia. Pac Sci 64:405–412

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  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

    Google Scholar 

  • Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337

    Article  CAS  PubMed  Google Scholar 

  • Geyer LB, Palumbi SR (2005) Conspecific sperm precedence in two species of tropical sea urchins. Evolution 59:97–105

    Article  PubMed  Google Scholar 

  • Hagedorn M, Spindler R (2014) The reality, use and potential for cryopreservation of coral reefs. Adv Exp Med Biol 753:317–329

    Article  PubMed  Google Scholar 

  • Hagedorn M, Pan R, Cox EF, Hollingsworth L, Krupp D, Lewis TD, Leong JC, Mazur P, Rall WF, MacFarlane DR, Fahy G, Kleinhans FW (2006) Coral larvae conservation: Physiology and reproduction. Cryobiology 52:33–47

    Article  CAS  PubMed  Google Scholar 

  • Hagedorn M, Carter V, Martorana K, Paresa MK, Acker J, Baums IB, Borneman E, Brittsan M, Byers M, Henley M, Laterveer M, Leong JA, McCarthy M, Meyers S, Nelson BD, Petersen D, Tiersch T, Uribe RC, Woods E, Wildt D (2012) Preserving and using germplasm and dissociated embryonic cells for conserving Caribbean and Pacific coral. PLoS One 7:e33354

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189

    Article  CAS  PubMed  Google Scholar 

  • Hatta M, Matsushima K (2008) Presumed natural hybrids between Acropora donei and Acropora tenuis. Galaxea 10:91–92

    Article  Google Scholar 

  • Hatta M, Fukami H, Wang W, Omori M, Shimoike K, Hayashibara T, Ina Y, Sugiyama T (1999) Reproductive and genetic evidence for a reticulate evolutionary history of mass-spawning corals. Mol Biol Evol 16:1607–1613

    Article  CAS  PubMed  Google Scholar 

  • Hayashibara T, Shimoike K (2002) Cryptic species of Acropora digitifera. Coral Reefs 21:224–225

    Google Scholar 

  • Hayashibara T, Shimoike K, Kimura T, Hosaka S, Heyward A, Harrison P, Kudo K, Omori M (1993) Patterns of coral spawning at Akajima Islands, Okinawa, Japan. Mar Ecol Prog Ser 101:253–262

    Article  Google Scholar 

  • Isomura N, Iwao K, Fukami H (2013) Possible natural hybridization of two morphologically distinct species of Acropora (Cnidaria, Scleractinia) in the Pacific: fertilization and larval survival rates. PLoS One 8:e56701

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT Multiple Sequence Alignment Software Version 7: Improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Knowlton N, Mate JL, Guzman HM, Rowan R, Jara J (1997) Direct evidence for reproductive isolation among the three species of the Montastraea annularis complex in Central America (Panama and Honduras). Mar Biol 127:705–711

    Article  Google Scholar 

  • Levitan DR (2002) The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins. Evolution 56:1599–1609

    Article  PubMed  Google Scholar 

  • Levitan DR (2004) Density-dependent sexual selection in external fertilizers: variances in male and female fertilization success along the continuum from sperm limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus. Am Nat 164:298–309

    Article  PubMed  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 

  • Marquez LM, van Oppen MJH, Willis BL, Miller DJ (2002a) Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and Acropora cytherea are genetically distinct. Proc R Soc Lond B Biol Sci 269:1289–1294

    Article  CAS  Google Scholar 

  • Marquez LM, Van Oppen MJ, Willis BL, Reyes A, Miller DJ (2002b) The highly cross-fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Mol Ecol 11:1339–1349

    Article  CAS  PubMed  Google Scholar 

  • Morita M, Nishikawa A, Nakajima A, Iguchi A, Sakai K, Takemura A, Okuno M (2006) Eggs regulate sperm flagellar motility initiation, chemotaxis and inhibition in the coral Acropora digitifera, A. gemmifera and A. tenuis. J Exp Biol 209:4574–4579

    Article  CAS  PubMed  Google Scholar 

  • Nakajima Y, Nishikawa A, Iguchi A, Sakai K (2012) The population genetic approach delineates the species boundary of reproductively isolated corymbose acroporid corals. Mol Phylogenet Evol 63:527–531

    Article  PubMed  Google Scholar 

  • Nozawa Y (2012) Annual variation in the timing of coral spawning in a high-latitude environment: influence of temperature. Biol Bull 222:192–202

    PubMed  Google Scholar 

  • Ohki S, Morita M, Kitanobo S, Kowalska AA, Kowalski RK (2014) Cryopreservation of Acropora digitifera sperm with use of sucrose and methanol based solution. Cryobiology 69:134–139

    Article  CAS  PubMed  Google Scholar 

  • Omori M, Fukami H, Kobinata H, Hatta M (2001) Significant drop of fertilization of Acropora corals in 1999: An after-effect of heavy coral bleaching? Limnol Oceanogr 46:704–706

    Article  Google Scholar 

  • Palumbi SR, Vollmer S, Romano S, Oliver T, Ladner J (2012) The role of genes in understanding the evolutionary ecology of reef building corals. Evol Ecol 26:317–335

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Oppen MJ, Willis BL, Van Rheede T, Miller DJ (2002) Spawning times, reproductive compatibilities and genetic structuring in the Acropora aspera group: evidence for natural hybridization and semi-permeable species boundaries in corals. Mol Ecol 11:1363–1376

    Article  PubMed  Google Scholar 

  • Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025

    Article  CAS  PubMed  Google Scholar 

  • Wallace CC (1999) Staghorn corals of the world: A revision of the genus Acropora. CSIRO Publishing, Collingwood, Australia

    Google Scholar 

  • Wallace CC, Willis BL (1994) Systematics of the coral genus Acropora: implications of new biological findings for species concepts. Annu Rev Ecol Evol Syst 25:237–262

    Article  Google Scholar 

  • Wei NV, Hsieh HJ, Dai CF, Wallace CC, Baird AH, Chen CA (2012) Reproductive isolation among Acropora species (Scleractinia: Acroporidae) in a marginal coral assemblage. Zool Stud 51:85–92

    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 

  • Wilson JR, Harrison PL (2003) Spawning patterns of scleractinian corals at the Solitary Islands—a high latitude coral community in eastern Australia. Mar Ecol Prog Ser 260:115–123

    Article  Google Scholar 

  • Wolstenholme JK (2004) Temporal reproductive isolation and gametic compatibility are evolutionary mechanisms in the Acropora humilis species group (Cnidaria; Scleractinia). Mar Biol 144:567–582

    Article  Google Scholar 

  • Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? Trends Ecol Evol 15:10–13

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partly supported by Okinawa Churashima Foundation (No. 119) to M.M., Uruma Foundation (Grant No. 13-13) to MM, and Grant for Basic Science Research Projects from The Sumitomo Foundation (Grant No. 131244) to M.M. We also appreciate to Prof. Andrew Baird of James Cook University to give us valuable comments to improve the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masaya Morita.

Additional information

Communicated by Ecology Editor Dr. Michael Berumen

Shun Ohki and Radoslaw K. Kowalski have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ohki, S., Kowalski, R.K., Kitanobo, S. et al. Changes in spawning time led to the speciation of the broadcast spawning corals Acropora digitifera and the cryptic species Acropora sp. 1 with similar gamete recognition systems. Coral Reefs 34, 1189–1198 (2015). https://doi.org/10.1007/s00338-015-1337-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-015-1337-4

Keywords

Navigation