Skip to main content
Log in

Genetic connectivity among color morphs and Pacific archipelagos for the flame angelfish, Centropyge loriculus

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Color variation is used in taxonomic classification of reef fishes, but it may not reliably indicate evolutionary divergence. In the central Pacific, there are three color morphs of the flame angelfish, Centropyge loriculus: a red morph that occurs primarily in the Hawaiian archipelago, the endemic Marquesan color morph with reduced black markings, and an orange morph that occurs throughout the rest of Oceania. The red and orange morphs co-occur at Johnston Atoll (1,300 km south of Hawai’i), but intermediate forms have not been reported. To determine whether the three color morphs represent distinct evolutionary lineages, we compared 641 base pairs of mitochondrial cytochrome b. Forty-one closely related haplotypes were observed in 116 individuals. Analysis of molecular variance (AMOVA) indicated no significant genetic structure among color morphs (ΦST = 0.011, P = 0.147). Likewise, there was no significant pairwise structure between sampling locations, separated by up to 5,700 km, after a Bonferroni correction (ΦST = 0.000–0.080, P = 0.0130–0.999). Genetic studies in conjunction with larval distribution data indicate that Centropyge species are highly dispersive. While there is a strong geographic component to the distribution of color morphs in C. loriculus, we find no evidence for corresponding genetic partitioning. We do not rule out an adaptive role for color differentiation, but our data do not support emerging species.

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

Similar content being viewed by others

References

  • Ako H, Tamaru CS, Asano L, Yuen B, Yamamoto M (1999) Achieving natural coloration in fish under culture. U.S. Japan Cooperative Program in Natural Resources Technical Report 28 Honolulu, University of Hawai’i, Hawai’i

  • Amos B, Hoelzel AR (1991) Long term preservation of whale skin for DNA analysis. Report of the International Whaling Commission Special Issue 13: 99–103

    Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Bay LK, Crozier RH, Caley MJ (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol 149:1247–1256

    Article  Google Scholar 

  • Bernardi G, Holbrook SJ, Schmitt RJ, Crane NL, DeMartini E (2002) Species boundaries, populations and colour morphs in the coral reef three-spot damselfish (Dascyllus trimaculatus) species complex. Proc R Soc Lond B 269:599–605

    Article  Google Scholar 

  • Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfish (Aulostomus spp.): ring species complex on a global scale. Evolution 55:1029–1039

    Article  CAS  PubMed  Google Scholar 

  • Bowen BW, Bass AL, Muss AJ, Carlin J, Robertson DR (2006a) Phylogeography of two Atlantic squirrelfishes (family Holocentridae): exploring pelagic larval duration and population connectivity. Mar Biol 149:899–913

    Article  Google Scholar 

  • Bowen BW, Muss A, Rocha LA, Grant WS (2006b) Shallow mtDNA coalescence in Atlantic pygmy angelfishes (genus Centropyge) indicates a recent invasion from the Indian Ocean. J Hered 97:1–12

    Article  CAS  Google Scholar 

  • Campton DE, Bass AL, Chapman FA, Bowen BW (2000) Genetic distinction of pallid, shovelnose, and Alabama sturgeon: emerging species and the US Endangered Species Act. Conserv Genet 1:17–32

    Article  CAS  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Craig MT, Hastings PA, Pondella DJ, Robertson DR, Rosales-Casian JA (2006) Phylogeography of the flag cabrilla, Epinephelus labriformis (Serranidae): implications for the biogeography of the tropical eastern Pacific and the early stages of speciation in a marine shore fish. J Biogeog 33:969–979

    Article  Google Scholar 

  • Doherty PJ, Mather P, Planes S (1994) Acanthochromis polyacanthus, a fish lacking larval dispersal, has genetically differentiated populations at local and regional scales on the Great Barrier Reef. Mar Biol 121:11–21

    Article  Google Scholar 

  • Dominey WJ (1984) Effects of sexual selection and life-history on speciation: species flocks in African cichlids and Hawaiian Drosophila. In: Echelle AA, Kornfield I (eds) The evolution of species flocks. University of Maine at Orono Press, Maine, 231–249

    Google Scholar 

  • Endler JA, Westcott DA, Madden JR, Robson T (2005) Animal visual systems and the evolution of color patterns: sensory processing illuminates signal evolution. Evolution 59:1795–1818

    Article  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    Article  CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and backgroud selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grady JM, Quattro JM (1999) Using character concordance to define taxonomic and conservation units. Conserv Biol 13:1004–1007

    Article  Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from the sardines and anchovies and lessons for conservation. J Hered 89: 415–426

    Article  Google Scholar 

  • Günther ACLG (1874) Andrew Garrett’s Fische der Südsee. Band I, Heft II. Journal des Museum Godeffroy, Band II, Heft V. J. Friederichsen, Hamburg, 25–56

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  • Harpending HC, Sherry ST, Rogers AR, Stoneking M (1993) The genetic structure of ancient human populations. Curr Anth 34:483–496

    Article  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15: 1314–1318

    Article  CAS  PubMed  Google Scholar 

  • Kaup JJ (1860) Ueber die Chaetodontidae. Arch Naturgeschichte 26:133–156

    Google Scholar 

  • Kinlan BP, Gaines SD, Lester SE (2005) Propagule dispersal and the scales of marine community process. Divers Distrib 11:139–148

    Article  Google Scholar 

  • Lee MS (2004) The molecularisation of taxonomy. Invert Syst 18:1–6

    Article  CAS  Google Scholar 

  • Leis JM, Carson-Ewart BM (1998) Complex behaviour by coral-reef fish larvae in open-water and near-reef pelagic environments. Environ Biol Fish 53:259–266

    Article  Google Scholar 

  • Loytynoja A, Milinkovitch MC (2003) ProAlign, a probabilistic multiple alignment program. Bioinformatics 19:1505–1513

    Article  PubMed  Google Scholar 

  • Lutnesky MMF (1992) Behavioral ecology of reproduction in the pomacanthid angelfish Centropyge potteri. Ph.D. Dissertation, University of Hawai’i, Honolulu, p 155

  • McCartney MA, Acevedo J, Heredia C, Rico C, Quenoville B, Bermingham E, McMillan WO (2003) Genetic mosaic in a marine species flock. Mol Ecol 12:2963–2973

    Article  CAS  PubMed  Google Scholar 

  • McMillan WO, Weigt LA, Palumbi SR (1999) Color pattern evolution, assortative mating, and genetic differentiation in brightly colored butterflyfishes (Chaetodontidae). Evolution 53:247–260

    Article  PubMed  Google Scholar 

  • Moyer JT, Nakazono A (1978) Population structure, reproductive behavior, and protogynous hermaphroditism in the angelfish Centropyge interruptus at Miyake-jima, Japan. Japan J Ichthyol 25:25–39

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488

    Article  CAS  PubMed  Google Scholar 

  • Pyle RL (2003) A systematic treatment of the reef-fish family Pomacanthidae (Pisces: Perciformes). Ph.D. Dissertation, University of Hawai’i, Honolulu, 422 pp

  • Pyle RL, Randall JE (1994) A review of hybridization in marine angelfishes (Perciformes: Pomacanthidae). Environ Biol Fishes 41:127–145

    Article  Google Scholar 

  • Ramon ML, Lobel PS, Sorenson MD (2003) Lack of mitochondrial genetic structure in hamlets (Hypoplectrus spp.): recent speciation or ongoing hybridization? Mol Ecol 12:2975–2980

    Article  PubMed  Google Scholar 

  • Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37:227–268

    Google Scholar 

  • Rocha LA (2004) Mitochondrial DNA and color pattern variation in three western Atlantic Halichoeres (Labridae), with the revalidation of two species. Copeia 4:770–782

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic tree. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Song CB, Near TJ, Page LM (1998) Phylogenetic relations among percid fishes as inferred from mitochondrial cytochrome b DNA sequence data. Mol Phyl Evol 10:343–353

    Article  CAS  Google Scholar 

  • Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP: phylogeny analysis using parsimony. Version 4, Sinauer Associates, Sunderland

  • Taberlet P, Meyer A, Bouvet J (1992) Unusually large mitochondrial variation in populations of the blue tit, Parus caeruleus. Mol Ecol 1:27–36

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takahata N, Slatkin M (1984) Mitochondrial gene flow. Proc Natl Acad USA 81:1764–1767

    Article  CAS  Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  PubMed  Google Scholar 

  • Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–809

    Article  PubMed  Google Scholar 

  • Thresher RE (1984) Reproduction in reef fishes. TFH, Neptune City

    Google Scholar 

  • Thresher RE, Brothers EB (1985) Reproductive ecology and biogeography of Indo-West Pacific angelfishes (Pisces: Pomacanthidae). Evolution 39:878–887

    Article  PubMed  Google Scholar 

  • Wiens JJ (2004) The role of morphological data in phylogeny reconstruction. Syst Biol 53:653–661

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

For acquisition of samples, we thank T. McGovern, J. Mahon, J. Philibotte, B. Greene, D. R. Robertson, J. Earle, L. Rocha, R. Kosaki, M. Lameier, J. Eble, C. Meyer, M. Ross, Y. Papastamatiou, the National Marine Sanctuary Program and the crew of the NOAA ship Hi’ialakai. We thank M. Crepeau and members of the Toonen-Bowen laboratory for their assistance. Thanks to F. Baensch, M. Lutnesky, J. Randall, D. Smith, K. Hartel, S. Karl, R. Toonen, M. Craig, S. Nishida, and three anonymous reviewers for invaluable advice. Thank you to J. Randall for all photographs. Funding for this work was provided by an NSF grant (OCE-0453167) and the HIMB-NWHI Coral Reef Research Partnership (NMSP MOA 2005-008/66882) awarded to BWB, an EPSCoR grant (EPS-0554657) awarded to the University of Hawaii, and an EPA STAR Fellowship awarded to JKS. All collections and analyses comply with the current laws of the countries in which they were performed. This is HIMB contribution 1238 and contribution 6824 from the School of Ocean and Earth Science and Technology at the University of Hawaii.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jennifer K. Schultz.

Additional information

Communicated by S. Nishida, Tokyo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schultz, J.K., Pyle, R.L., DeMartini, E. et al. Genetic connectivity among color morphs and Pacific archipelagos for the flame angelfish, Centropyge loriculus . Mar Biol 151, 167–175 (2007). https://doi.org/10.1007/s00227-006-0471-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0471-5

Keywords

Navigation