Evolutionary Ecology

, Volume 26, Issue 2, pp 317–335 | Cite as

The role of genes in understanding the evolutionary ecology of reef building corals

  • Stephen R. Palumbi
  • Steven Vollmer
  • Sandra Romano
  • Tom Oliver
  • Jason Ladner
Original Paper


A key tool in evolutionary ecology is information about the temporal dynamics of species over time. Paleontology has long been the major source of this information, however, a very different source of temporal data resides in the variation of genes within and between species. These data provide an independent way to date species divergence but can also uniquely reveal processes such as gene introgression between species and demographic isolation within species. Genetic tools are particularly useful for understanding genera with closely related species that can potentially hybridize, such as reef building corals. Here we use genetic data from four loci (3 introns and 1 mitochondrial) to assay divergence and gene flow in Caribbean corals. The data show that there is persistent gene flow between species in the genus Acropora, but that this gene flow is unidirectional and highly variable among loci. Selection against introgressed alleles is high enough at one locus, Mini-collagen, to prevent gene flow between species. By contrast, selection against mitochondrial introgression appears much weaker, with 40–80 times higher rates of inter-specific gene flow than for any nuclear locus we examined. The same loci also show that gene flow among locations within species is locally restricted, but is nevertheless much higher between populations than between species. Interpretation of population data is complicated by the variable nature of selection on introgressed alleles, and some patterns of genetic differentiation might be driven by local introgression and selection. The combination of inter-specific and intra-specific data using the same loci treated in a genealogical framework helps resolve complications due to introgression and helps paint a picture of the evolution and maintenance of species in a complex spatial and temporal framework.


Coral Genetics FST Acropora 



We thank NSF’s BioComplexity Program, the Gordon and Betty Moore Foundation and NOAA for funding. We also thank Ryan Kelly, Arjun Sivasundar, Melissa Pespeni, Heather Galindo, Malin Pinsky and two anonymous reviewers for discussion and suggestions on earlier drafts of the manuscript. We also thank Jeremy Jackson for ideas and inspiration.

Supplementary material

10682_2011_9517_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)


  1. Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, OxfordGoogle Scholar
  2. Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148CrossRefGoogle Scholar
  3. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390PubMedCrossRefGoogle Scholar
  4. Budd AF, Wallace CC (2008) First record of the Indo-Pacific reef coral genus Isopora in the Caribbean region: two new species from the Neogene of Caracao, Netherlands Antilles. Paleontology 51:1387–1401CrossRefGoogle Scholar
  5. Budd AF, Stemann TA, Johnson KG (1994) Stratigraphic distributions of genera and species of Neogene to Recent Caribbean reef corals. J Paleontol 68:951–977Google Scholar
  6. Burton RS, Lee B-N (1994) Nuclear and mitochondrial gene genealogies and allozyme polymorphisms across a major phylogeographic break in the copepod Tigriopus californicus. Proc Natl Acad Sci USA 91:5197–5201PubMedCrossRefGoogle Scholar
  7. Cheetham AH, Jackson JBC, Hayek LAC (1993) Quantitative genetics of bryozoan phenotypic evolution.1. Rate tests for random change versus selection in differentiation of living species. Evolution 47:1526–1538CrossRefGoogle Scholar
  8. Cheetham AH, Jackson JBC, Hayek LAC (1994) Quantitative genetics of bryozoan phenotypic evolution.2. Analysis of selection and random change in fossil species using reconstructured genetic parameters. Evolution 48:360–375CrossRefGoogle Scholar
  9. Cheetham AH, Jackson JBC, Hayek LAC (1995) Quantitative genetics of bryozoan phenotypic evolution.3. Phenotypic plasticity and the maintenance of genetic variation. Evolution 49:290–296CrossRefGoogle Scholar
  10. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527PubMedCrossRefGoogle Scholar
  11. Double MC, Peakall R, Beck NR, Cockburn A (2005) Dispersal, philopatry, and infidelity: dissecting local genetic structure in Superb Fairy Wrens (Malurs cyaneus). Evolution 59:625–635PubMedGoogle Scholar
  12. 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 58:324–337PubMedGoogle Scholar
  13. Galindo HM, Olson DB, Palumbi SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Curr Biol 16:1622–1626PubMedCrossRefGoogle Scholar
  14. Harrison RG (1990) Hybrid zones: windows on evolutionary process. In: Futuyma D, Antonovics J (eds) Oxford surveys in evolutionary biology, vol 7. Oxford University Press, Oxford, UK, pp 69–128Google Scholar
  15. Hartl DL, Clark A (1997) Principles of population genetics. Sinauer Press, SunderlandGoogle Scholar
  16. Hellberg M (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24PubMedCrossRefGoogle Scholar
  17. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedCrossRefGoogle Scholar
  18. Hillis DM, Moritz C, Mable BK (eds) (1996) Molecular systematics. Sinauer Associates, Inc., SunderlandGoogle Scholar
  19. Jackson JBC, Cheetham AH (1994) Phylogeny reconstruction and the tempo of speciation in cheilostome Bryozoa. Paleobiology 20:407–423Google Scholar
  20. Jackson JBC, Erwin DH (2006) What can we learn about ecology and evolution from the fossil record? Trends Ecol Evol 21:322–328PubMedCrossRefGoogle Scholar
  21. Jackson JBC, Johnson KG (2000) Life in the last few million years. Paleobiology 26:221–235CrossRefGoogle Scholar
  22. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638PubMedCrossRefGoogle Scholar
  23. Kelly RP, Oliver TA, Sivasundar A, Palumbi SR (2010) A method for detecting population genetic structure in diverse, high gene-flow species. J Hered 101:423–436PubMedCrossRefGoogle Scholar
  24. Knowlton N, Jackson JBC (1994) New taxonomy and niche partitioning on coral reeds—jack of all trades or master of some. Trends Ecol Evol 9:7–9PubMedCrossRefGoogle Scholar
  25. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  26. Marko PB, Hart MW (2011) Retrospective coalescent methods and the reconstruction of metapopulation histories in the sea. Evol Ecol. doi: 10.10007/s10682-011-9467-9
  27. Navarro A, Barton NH (2003a) Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447–459PubMedGoogle Scholar
  28. Navarro A, Barton NH (2003b) Chromosomal speciation and molecular divergence—accelerated evolution in rearranged chromosomes. Science 300:321–324PubMedCrossRefGoogle Scholar
  29. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: an MCMC approach. Genetics 158:885–896PubMedGoogle Scholar
  30. Noor MAF, Grams KL, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci USA 98:12084–12088PubMedCrossRefGoogle Scholar
  31. Ortiz-Barrientos D, Noor MAF (2005) Evidence for a one-allele assortative mating locus. Science 310:1467PubMedCrossRefGoogle Scholar
  32. Peakall ROD, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  33. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  34. Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358PubMedCrossRefGoogle Scholar
  35. Rieseberg LH, Church SA, Morjan CL (2004) Integration of populations and differentiation of species. New Phytol 161:59–69PubMedCrossRefGoogle Scholar
  36. Romano SL, Palumbi SR (1996) Evolution of scleractinian corals inferred from molecular systematics. Science 271:640–642CrossRefGoogle Scholar
  37. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2. Genetics and Biometry Lab, Dept of Anthropology, University of Geneva, GenevaGoogle Scholar
  38. Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910CrossRefGoogle Scholar
  39. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109PubMedCrossRefGoogle Scholar
  40. Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in Neotropical reef gobies (Elacatinus). Evolution 59:374–385PubMedGoogle Scholar
  41. 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 Biol Sci 266:179–183CrossRefGoogle Scholar
  42. van Oppen MJH, Willis BL, Vugt HV, Miller DJ (2000) Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Mol Ecol 9:1363–1373PubMedCrossRefGoogle Scholar
  43. 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 18:1315–1329PubMedCrossRefGoogle Scholar
  44. van Oppen MJH, Koolmees EM, Veron JEN (2004) Patterns of evolution in the scleractinian coral genus Montipora (Acroporidae). Mar Biol 144:9–18CrossRefGoogle Scholar
  45. Veron JEN (1981) The species concept in ‘Scleractinia of Eastern Australia’. In: Proceedings of the 4th international coral reef symposium 2:183–186Google Scholar
  46. Veron JEN (1995) Corals in space and time: the biogeography and evolution of the Scleractinia. University of New South Wales Press, SydneyGoogle Scholar
  47. Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025PubMedCrossRefGoogle Scholar
  48. Vollmer SV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicomis: implications for the recovery of endangered reefs. J Hered 98:40–50PubMedCrossRefGoogle Scholar
  49. Voolstra CR, Sunagawa S, Matz MV, Bayer T, Aranda M, Buschiazzo E, DeSalvo MK, Lindquist E, Szmant AM, Coffroth MA, Medina M (2011) Rapid evolution of coral proteins responsible for interaction with the environment. PLoS ONE 6:e20392PubMedCrossRefGoogle Scholar
  50. 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, Collingwood, Victoria, AustraliaGoogle Scholar
  51. Wang RL, Wakeley J, Hey J (1997) Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics 147:1091–1106PubMedGoogle Scholar
  52. Whitlock M, McCauley D (1999) Indirect measures of gene flow and migration: FST not equal to 1/(4Nm + 1). Heredity 82:117–125PubMedCrossRefGoogle Scholar
  53. Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annu Rev Ecol Evol Syst 37:489–517CrossRefGoogle Scholar
  54. Wright S (1951) The genetical structure of populations. Ann Hum Genet 15:323–354Google Scholar
  55. Wu CI (2001) The genic view of the process of speciation. J Evol Biol 14:851–865CrossRefGoogle Scholar
  56. Wu CI, Ting CT (2004) Genes and speciation. Nat Rev Genet 5:114–122PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Stephen R. Palumbi
    • 1
  • Steven Vollmer
    • 2
  • Sandra Romano
    • 3
  • Tom Oliver
    • 1
  • Jason Ladner
    • 1
  1. 1.Department of BiologyStanford UniversityPacific GroveUSA
  2. 2.Marine Science Center, Northeastern UniversityNahantUSA
  3. 3.University of the Virgin IslandsSt. Croix & St. ThomasUnited States Virgin Islands

Personalised recommendations