Marine Biology

, Volume 144, Issue 3, pp 567–582

Temporal reproductive isolation and gametic compatibility are evolutionary mechanisms in the Acropora humilis species group (Cnidaria; Scleractinia)

Research Article

Abstract

Patterns of interbreeding between individuals are fundamental to the structure and maintenance of evolutionary boundaries between species. In corals, both hybridisation and reproductive isolation appear to be important evolutionary mechanisms. In this study, I examine evolutionary boundaries using morphological, molecular and reproductive criteria within the Acropora humilis species group at Lizard Island on the Great Barrier Reef, Australia. Five species and seven morphs are recognised on the basis of morphological appearance of features traditionally used to identify corals of the genus Acropora. In a molecular phylogenetic analysis, I examine relationships for the mitochondrial DNA’s putative control region, using maximum-parsimony and maximum-likelihood methods. The reproductive criteria explore whether species and morphs are reproductively isolated on the basis of temporal or fertilisation barriers. Timing of gamete maturity is surveyed for each species and morph, from the month prior to and 3 months after the mass spawning. Time of spawning is documented at the levels of night and hour of spawning, and time taken for egg-sperm bundles to separate. Laboratory fertilisation experiments tested the potential of species and morphs to interbreed. High levels of intraspecific and extremely low or zero fertilisation levels between the five species indicated that they are valid species. Based on the combined assessment of morphological, molecular and reproductive criteria, A. humilis and A. gemmifera appear to be the most closely related species, which are most closely related to the remaining species in the following order: A. samoensis, A. monticulosa and A. digitifera. Evidence derived from one or more of these criteria suggest that the morphs (1) are at various stages of divergence from the species with which they share morphological characters, and (2) may indicate possible zones of speciation and hybridisation. Identification of morphs avoided the possibility of taxonomic error and was essential for accurate interpretation of evolutionary boundaries. Confirmation of morphology as an informative character of evolutionary boundaries is of great significance because most coral research projects rely on morphology as the primary tool for identification of species.

Keywords

Acropora Morphology mtDNA Reproductive isolation Species boundaries 

References

  1. Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New YorkGoogle Scholar
  2. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  3. Babcock R (1995) Synchronous multispecific spawning on coral reefs: potential for hybridization and roles of gamete recognition. Reprod Fertil Dev 7:943–950Google Scholar
  4. 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 90:379–394Google Scholar
  5. Babcock RC, Willis BL, Simpson CJ (1994) Mass spawning of corals on a high latitude coral reef. Coral Reefs 13:161–169Google Scholar
  6. Baird AH, Marshall PA, Wolstenholme J (2002) Latitudinal variation in the reproduction of Acropora in the Coral Sea. In: Moosa MK, Soemodihardjo S, Soegiarto A, Romimohtarto K, Nontji A, Soekarno, Suharsono (eds) Proceedings of the 9th International Coral Reef Symposium, vol 1. Indonesian Institute of Sciences, Indonesia, pp 385–402Google Scholar
  7. Brook G (1891) Descriptions of new species of Madrepora in the collections of the British Museum. Ann Mag Nat Hist 8:458–471Google Scholar
  8. Brook G (1892) Preliminary descriptions of new species of Madrepora in the collections of the British Museum. Part II. Ann Mag Nat Hist 10:451–465Google Scholar
  9. Brüggemann F (1879) Corals in Zoology of Rodriguez. Philos Trans R Soc Lond B 168:569–579Google Scholar
  10. Coll JC, Bowden BF, Meehan GV, Konig GM, Carroll AR, Tapiolas DM, Aliño PM, Heaton A, De Nys R, Leone PA, Maida M, Aceret TL, Willis RH, Babcock RC, Willis BL, Florian Z, Clayton MN, Miller RL (1994) Chemical aspects of mass spawning in corals. I. Sperm-attractant molecules in the eggs of the scleractinian coral Montipora digitata. Mar Biol 118:177–182Google Scholar
  11. Dana JD (1846) Zoophytes. US Explor Exped 7:1–740Google Scholar
  12. Diekmann OE, Bak RPM, Stam WT, Olsen JL (2001) Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Mar Biol 139:221–233CrossRefGoogle Scholar
  13. 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 142:679–684Google Scholar
  14. Gilbert DG (1994) SEQAPP 1.9. A biological sequence editor and analysis program for Macintosh computers. Available from http://ftp.bio.indiana.edu. Cited 14 April 2003.
  15. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189Google Scholar
  16. 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 16:1607–1613PubMedGoogle Scholar
  17. Hayashibara T, Shimoike K (2002) Cryptic species of Acropora digitifera. Coral Reefs 21:224–225Google Scholar
  18. Hayashibara T, Shimoike K, Kimura T, Hosaka S, Heyward A, Harrison P, Kudo K, Omori M (1993) Patterns of coral spawning at Akajima Island, Okinawa, Japan. Mar Ecol Prog Ser 101:253–262Google Scholar
  19. Kenyon JC (1997) Models of reticulate evolution in the coral genus Acropora based on chromosome numbers: parallels with plants. Evolution 51:756–767Google Scholar
  20. Knowlton N, Maté JL, Guzmán HM, Rowan R, Jara J (1997) Direct evidence for reproductive isolation among the three species of the Montastraea annularis complex in Central America (Panamá and Honduras). Mar Biol 127:705–711CrossRefGoogle Scholar
  21. Lang JC (1984) Whatever works: the variable importance of skeletal and of non-skeletal characters in scleractinian taxonomy. Palaeontogr Am 54:18–44Google Scholar
  22. Márquez 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 269:1289–1294CrossRefPubMedGoogle Scholar
  23. Márquez LM, van Oppen MJH, Willis BL, Reyes A, Miller DJ (2002b) The highly cross-fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Mol Ecol 11:1339–1349CrossRefPubMedGoogle Scholar
  24. Miller K, Babcock R (1997) Conflicting morphological and reproductive species boundaries in the coral genus Platygyra. Biol Bull 192:98–110Google Scholar
  25. Miller KJ, Benzie JAH (1997) No clear genetic distinction between morphological species within the coral genus Platygyra. Bull Mar Sci 61:907–917Google Scholar
  26. Odorico DM, Miller DJ (1997) Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. Mol Biol Evol 14:465–473PubMedGoogle Scholar
  27. Oppen MJH van, Hislop NR, Hagerman PJ, Miller DJ (1999) Gene content and organization in a segment of the mitochondrial genome of the scleractinian coral Acropora tenuis: major differences in gene order within the Anthozoan subclass Zoantharia. Mol Biol Evol 16:1812–1815PubMedGoogle Scholar
  28. Oppen MJH van, Willis BL, van Vugt HWJA, Miller DJ (2000) Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Mol Ecol 9:1363–1373PubMedGoogle Scholar
  29. Oppen MJH van, McDonald BJ, Willis B, Miller DJ (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol Biol Evol 18:1315–1329PubMedGoogle Scholar
  30. Oppen MJH van, Catmull J, McDonald BJ, Hislop NR, Hagerman PJ, Miller DJ (2002a) The mitochondrial genome of Acropora tenuis (Cnidaria; Scleractinia) contains a large group I intron and a candidate control region. J Mol Evol 55:1-13CrossRefPubMedGoogle Scholar
  31. Oppen MJH van, Willis BL, van Rheede T, Miller DJ (2002b) 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 11:1363–1376CrossRefPubMedGoogle Scholar
  32. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  33. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  34. Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389CrossRefGoogle Scholar
  35. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372CrossRefPubMedGoogle Scholar
  36. Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA, Arnheim N (1985) Enzymatic amplification of β-Globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350–1354PubMedGoogle Scholar
  37. Stobart B (2000) A taxonomic reappraisal of Montipora digitata based on genetic and morphometric evidence. Zool Stud 39:179–190Google Scholar
  38. Stobart B, Benzie JAH (1994) Allozyme electrophoresis demonstrates that the scleractinian coral Montipora digitata is two species. Mar Biol 118:183–190Google Scholar
  39. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods). Sinauer, Sunderland, Mass.Google Scholar
  40. Szmant AM, Weil E, Miller MW, Colón DE (1997) Hybridization within the species complex of the scleractinian coral Montastraea annularis. Mar Biol 129:561–572CrossRefGoogle Scholar
  41. Veron JEN (1995) Corals in space and time: the biogeography and evolution of the Scleractinia. UNSW Press, SydneyGoogle Scholar
  42. Veron JEN, Wallace CC (1984) Scleractinia of eastern Australia. Part V. Family Acroporidae. Australian National University Press, CanberraGoogle Scholar
  43. Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025CrossRefPubMedGoogle Scholar
  44. Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar Biol 88:217–233Google Scholar
  45. Wallace CC (1999) Staghorn corals of the world: a revision of the coral genus Acropora (Scleractinia; Astrocoeniina; Acroporidae) worldwide, with emphasis on morphology, phylogeny and biogeography. CSIRO Publishing, CollingwoodGoogle Scholar
  46. Wallace CC, Willis BL (1994) Systematics of the coral genus Acropora: implications of new biological findings for species concepts. Annu Rev Ecol Syst 25:237–262Google Scholar
  47. Willis BL (1990) Species concepts in extant scleractinian corals: considerations based on reproductive biology and genotypic population structures. Syst Bot 15:136–149Google Scholar
  48. Willis BL, Babcock RC, Harrison PL, Oliver JK (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. In: Delesalle B, Galzin R, Salvat B (eds) Proceedings of the 5th International Coral Reef Congress,vol 4. Antenne Museum—EPHE, Moorea, pp 343–348Google Scholar
  49. 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 [Suppl]:S53–S65Google Scholar
  50. Wolstenholme JK, Wallace CC, Chen CA (2003) Species boundaries within the Acropora humilis species group (Cnidaria; Scleractinia): a morphological and molecular interpretation of evolution. Coral Reefs 22:155–166Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Marine Biology and AquacultureJames Cook UniversityTownsvilleAustralia

Personalised recommendations