Marine Biotechnology

, 11:141 | Cite as

Comparative Analyses of Coding and Noncoding DNA Regions Indicate that Acropora (Anthozoa: Scleractina) Possesses a Similar Evolutionary Tempo of Nuclear vs. Mitochondrial Genomes as in Plants

  • I.-Ping Chen
  • Chung-Yu Tang
  • Chih-Yung Chiou
  • Jia-Ho Hsu
  • Nuwei Vivian Wei
  • Carden C. Wallace
  • Paul Muir
  • Henry Wu
  • Chaolun Allen Chen
Original Article

Abstract

Evidence suggests that the mitochondrial (mt)DNA of anthozoans is evolving at a slower tempo than their nuclear DNA; however, parallel surveys of nuclear and mitochondrial variations and calibrated rates of both synonymous and nonsynonymous substitutions across taxa are needed in order to support this scenario. We examined species of the scleractinian coral genus Acropora, including previously unstudied species, for molecular variations in protein-coding genes and noncoding regions of both nuclear and mt genomes. DNA sequences of a calmodulin (CaM)-encoding gene region containing three exons, two introns and a 411-bp mt intergenic spacer (IGS) spanning the cytochrome b (cytb) and NADH 2 genes, were obtained from 49 Acropora species. The molecular evolutionary rates of coding and noncoding regions in nuclear and mt genomes were compared in conjunction with published data, including mt cytochrome b, the control region, and nuclear Pax-C introns. Direct sequencing of the mtIGS revealed an average interspecific variation comparable to that seen in published data for mt cytb. The average interspecific variation of the nuclear genome was two to five times greater than that of the mt genome. Based on the calibration of the closure of Panama Isthmus (3.0 mya) and closure of the Tethy Seaway (12 mya), synonymous substitution rates ranged from 0.367% to 1.467% Ma−1 for nuclear CaM, which is about 4.8 times faster than those of mt cytb (0.076–0.303% Ma−1). This is similar to the findings in plant genomes that the nuclear genome is evolving at least five times faster than those of mitochondrial counterparts.

Keywords

Molecular evolution Nuclear genes Mitochondrial genes Scleractinian corals Acropora Calmodulin 

Notes

Acknowledgements

Many thanks to Grant Burgess and two anonymous referees for constructive comments; Yaoyung Chuang, Cheinwei Chen, and members of the Coral Reef Evolutionary Ecology and Genetics Lab, Research Center for Biodiversity, Academia Sinica (RCBAS), for assistance with field work, and the Penghu Marine Life Propagation Center, a facility of Penghu County, which provided facilities and hospitality during the 2005 coral spawning season in Penghu. C.-Y. Chiou for the receipt of Academia Sinica Postdoctoral Fellowship (2005–2007). This work was supported by NSC grants and Academia Sinica Thematic and Genomics Grants (2002–2004, 2006–2007) to CAC. This is the Coral Reef Evolutionary Ecology and Genetics Lab, RCBAS contribution no. 45.

References

  1. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawning of 105 coral species on the Great Barrier Reef. Mar Biol 90:379–394CrossRefGoogle Scholar
  2. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390PubMedCrossRefGoogle Scholar
  3. Bellwood DR, Wainwright PC, Fulton CJ, Hoey A (2002) Assembly rules and functional groups at global biogeographical scales. Funct Ecol 16:557–562CrossRefGoogle Scholar
  4. Black KP, Moran PJ, Hammond LS (1991) Numerical-models show coral reefs can be self-seeding. Mar Ecol Prog Ser 74(1):1–11CrossRefGoogle Scholar
  5. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial-DNA sequences of primates tempo and mode of evolution. J Mol Evol 18:225–239PubMedCrossRefGoogle Scholar
  6. Cairns S (2000) A revision of the shallow-water zooxanthellate Scleractinia of the Western Atlantic. Stud Nat Hist Caribb Reg 75:1–240Google Scholar
  7. Carlon DB (1999) The evolution of mating systems in tropical reef corals. Trends Ecol Evol 14:491–495PubMedCrossRefGoogle Scholar
  8. Chen CA, Yu J-K (2000) Universal primers for amplification of mitochondrial small subunit ribosomal RNA-encoding gene in scleractinian corals. Mar Biotech 2:146–153Google Scholar
  9. Chen C, Dai C-F, Chiou C-Y, Plathong S, Chen CA (2008) The Complete mitochondrial genomes of needle corals, Seriatopora spp (Scleractinia; Pocilloporidae): idiosyncratic atp8 gene, duplicated tRNA-Trp, and the hypervariable regions for species phylogenies and recently diverged populations. Mol Phylogen Evol 46:19–33CrossRefGoogle Scholar
  10. Chiou C-Y, Chen I-P, Chen C-H, Wei NV, Wu H, Wallace CC, Chen CA (2008) Analysis of Acropora muricata calmodulin (CaM) indicates scleractinian coral possess the ancestral exon/intron organization of eumetazoan CaM gene. J Mol Evol 66:317–324 doi:10.1007/s00239-008-9084-6 PubMedCrossRefGoogle Scholar
  11. Clayton DA (1982) Replication of animal mitochondrial-DNA. Cell 28:693–705PubMedCrossRefGoogle Scholar
  12. Coates AG, Obando JA (1996) The geological evolution of the central American Isthmus. University of Chicago Press, ChicagoGoogle Scholar
  13. Dauget JM (1991) Application of tree architectural models to reef-coral growth forms. Mar Biol 111:157–165CrossRefGoogle Scholar
  14. Donoghue MJ (2005) Key innovations, convergence, and success: macroevolutionary lessons from plant phylogeny. Paleobiology 31:77–93CrossRefGoogle Scholar
  15. Duquecaro H (1990) Neogene stratigraphy, paleoceanography and paleobiogeography in northwest south-America and the evolution of the Panama seaway. Palaeogeogr Palaeoclimateol Palaeoecol 77:203–234CrossRefGoogle Scholar
  16. Friedberg F, Rhoads AR (2001) Evolutionary aspects of calmodulin. IUBMB Life 51:215–221PubMedCrossRefGoogle Scholar
  17. Fukami H, Knowlton N (2005) Analysis of complete mitochondrial DNA sequences of three members of the Montastraea annularis coral species complex (Cnidaria,Anthozoa, Scleractinia). Coral Reefs 24:410–417CrossRefGoogle Scholar
  18. Fukami H, Omori M, Hatta M (2000) Phylogenetic relationships in the coral family Acroporidae, reassessed by inference from mitochondrial genes. Zool Sci 17:689–696PubMedGoogle Scholar
  19. Fukami H, Omori M, Shimoike T, Hayashibara T, Hatta M (2003) Ecological and genetics aspects concerned with reproductive isolation by differential spawning timing in Acropora corals. Mar Biol 142:679–684Google Scholar
  20. Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004a) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337PubMedGoogle Scholar
  21. Fukami H, Budd AF, Paulay G, Sol Cava A, Chen CA, Iwao K, Knowlton N (2004b) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427:832–835PubMedCrossRefGoogle Scholar
  22. Gaut BS (1998) Molecular clocks and nucleotide substitution rates in higher plants. Evol Biol 30:93–120Google Scholar
  23. Govindarajan AF, Halanych KK, Cunningham CW (2005) Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Mar Biol 146:213–222CrossRefGoogle Scholar
  24. Hatta M, Fukami H, Wang WQ, 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
  25. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189PubMedCrossRefGoogle Scholar
  26. Hellberg ME (1994) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48:1829–1854CrossRefGoogle Scholar
  27. Hellberg ME (1995) Stepping-stone gene flow in the solitary coral Balanophyllia elegans—equilibrium and nonequilibrium at different spatial scales. Mar Biol 123:573–581CrossRefGoogle Scholar
  28. Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24–32PubMedCrossRefGoogle Scholar
  29. Heyward AJ, Babcock RC (1986) Self-fertilization and cross-fertilization in scleractinian corals. Mar Biol 90:191–195CrossRefGoogle Scholar
  30. Keigwin L (1982) Isotopic paleo-oceanography of the Caribbean and East Pacific—role of Panama uplift in late Neogene time. Science 217:350–352PubMedCrossRefGoogle Scholar
  31. Kimura M (1980) A Simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  32. Knowlton N, Weigt LA, Solórzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260:1629–1632PubMedCrossRefGoogle Scholar
  33. Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 13:2190–2195PubMedCrossRefGoogle Scholar
  34. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  35. Li WH (1997) Molecular evolution. Sinauer, Sunderland, MAGoogle Scholar
  36. Li WH, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA Sequences. J Mol Evol 25:330–342PubMedCrossRefGoogle Scholar
  37. Martin AP, Palumbi SR (1993) Body size, metabolic rate, generation time and the molecular clock. Proc Natl Acad Sci U S A 90:4087–4091PubMedCrossRefGoogle Scholar
  38. Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155PubMedCrossRefGoogle Scholar
  39. Medina M, Weil E, Szmant AM (1999) Examination of the Montastraea annularis species complex (Cnidaria: Scleractinia) using ITS and COI sequences. Mar Biotech 1:89–97CrossRefGoogle Scholar
  40. Medina M, Collins AG, Takaoka TL, Kuehl JV, Boore JL (2006) Naked corals: skeleton loss in Scleractinia. Proc Natl Acad Sci U S A 103:9096–9100PubMedCrossRefGoogle Scholar
  41. Miller K, Mundy C (2003) Rapid settlement in broadcast spawning corals: implications for larval dispersal. Coral Reefs 22:99–106CrossRefGoogle Scholar
  42. Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA relevance for population biology and systematics. Ann Rev Ecol Syst 18:269–292CrossRefGoogle Scholar
  43. Muse SV (2000) Examining rates and patterns of nucleotide substitution in plants. Plant Mol Biol 42:25–43PubMedCrossRefGoogle Scholar
  44. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  45. Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic variability in Populations. Evolution 29:1–10CrossRefGoogle Scholar
  46. Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structures, but slowly in sequence. J Mol Evol 28:87–97PubMedCrossRefGoogle Scholar
  47. Palmer JD, Adams KL, Cho Y, Parkinson CL, Qiu Y-L, Song K (2000) Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc Natl Acad Sci U S A 97:6960–6966PubMedCrossRefGoogle Scholar
  48. Pont-Kingdon G, Okada NA, Macfarlane JL, Beagley CT, Watkins-Sims CD, Cavalier-Smith T, Clark-Walker GD, Wolstenholme DR (1998) Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homologue of bacterial MutS: A possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46:419–431PubMedCrossRefGoogle Scholar
  49. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  50. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175PubMedCrossRefGoogle Scholar
  51. Sharp PM, Li WH (1987) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nuclei Acids Res 15:1281–1295CrossRefGoogle Scholar
  52. Shearer TL, van Oppen MJH, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487PubMedCrossRefGoogle Scholar
  53. Snell TL, Foltz DW, Sammarco PW (1998) Variation in morphology vs. conservatism of a mitochondrial gene in Montastrea cavernosa (Cnidaria, Scleractinia). Gulf Mexico Sci 70:188–195Google Scholar
  54. Tamura KDJ, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  55. Thomas MK, Christopher JC, Melissa MP, Thomas JN, James OM (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29CrossRefGoogle Scholar
  56. Thomas MK, Thomas JN, James OM (2007) MultiPhyl: a high-throughput phylogenomics webserver using distributed computing. Nucleic Acids Res 35:W33–W37CrossRefGoogle Scholar
  57. Tseng C-C, Wallace CC, Chen CA (2005) Mitogenomic analysis of Montipora cactus and Anacropora matthai (Cnidaria; Scleractinia; Acroporidae) indicates an unequal rate of mitochondrial evolution among Acroporidae corals. Coral Reefs 24:502–508CrossRefGoogle Scholar
  58. van Oppen MJH, Willis BL, Miller DJ (1999) Atypically low rate of cytochrome b evolution in the scleractinian coral genus Acropora. Proc R Soc Lond B 266:179–183CrossRefGoogle Scholar
  59. van Oppen MJH, 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
  60. Vermeij GJ (1973) Adaptation, versatility, and evolution. Syst Zool 22(4):466–477CrossRefGoogle Scholar
  61. Veron JEN (1993) A biogeographic database of hermatypic corals. Species of the central Indo-Pacific genera of the world. Aust Inst Mar Sci 10:9Google Scholar
  62. Wallace CC (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO, Collingwood, Victoria, AustraliaGoogle Scholar
  63. Wallace CC, Chen CA, Fukami H, Muir PR (2007) Recognition of separate genera within Acropora based on new morphological, reproductive and genetic evidence from Acropora togianensis, and elevation of the subgenus Isopora Studer, 1878 to genus (Scleractinia: Astrocoeniidae; Acroporidae). Coral Reefs 26:231–239CrossRefGoogle Scholar
  64. Wei NWV, Wallace CC, Dai CF, Pillay KRM, Chen CA (2006) Analyses of the ribosomal internal transcribed spacers (ITS) and the 5.8S gene indicate that extremely high rDNA heterogeneity is a unique feature in the scleractinian coral genus Acropora (Scleractinia; Acroporidae). Zool Stud 45:404–418Google Scholar
  65. Willis BL, Babcock RC, Harrison PL, Oliver JK, Wallace CC (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. Proc 5th Int Coral Reef Symp 4:343–348Google Scholar
  66. Willis BL, Babcock RC, Harrison PL, Wallace CC (1997) Experimental hybridisation and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16:553–565CrossRefGoogle Scholar
  67. Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Ann Rev Ecol Evol Syst 37:489–517CrossRefGoogle Scholar
  68. Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A 84:9054–9058PubMedCrossRefGoogle Scholar
  69. Wright S (1931) Evolution in Mendelian populations. Genetics 16:0097–0159Google Scholar
  70. Wu CI, Li WH (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci U S A 82:1741–1745PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • I.-Ping Chen
    • 1
  • Chung-Yu Tang
    • 1
  • Chih-Yung Chiou
    • 1
  • Jia-Ho Hsu
    • 1
    • 2
  • Nuwei Vivian Wei
    • 1
    • 2
  • Carden C. Wallace
    • 3
  • Paul Muir
    • 3
  • Henry Wu
    • 1
  • Chaolun Allen Chen
    • 1
    • 2
  1. 1.Biodiversity Research CenterAcademia SinicaTaipeiTaiwan
  2. 2.Institute of OceanographyNational Taiwan UniversityTaipeiTaiwan
  3. 3.Museum of Tropical QueenslandQueenslandAustralia

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