Skip to main content
Log in

Morphological and Genetic Divergences in a Coral Reef Damselfish, Pomacentrus coelestis

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

Abstract

Population differentiation is one of the main topics in evolutionary biology. Except the exploration of color variation, few studies focused on morphological divergences among populations of coral reef fishes. In this work, we studied morphological and genetic differentiation among populations of the damselfish, Pomacentrus coelestis, in the northwestern Pacific Ocean. The shapes of the mandible and the premaxilla were explored using geometric morphometric methods and the genetic structure was investigated using microsattelites. Various tests revealed significant shape variation among most P. coelestis populations for both skeletal units. Morphological variation of the mandible accompanies a genetic break between populations of mainland Japan and Okinawa-Taiwan. However, Mantel and Procrustes tests revealed no congruence between morphological and genetic structures. We illustrate that phenotypic plasticity and adaptive divergence are potential evolutionary mechanisms underlying shape difference among P. coelestis populations. An ecomorphological approach suggests that various diet could be related to shape variation of oral jaws.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71(1), 5–16.

    Article  Google Scholar 

  • Albertson, R. C., Streelman, J. T., & Kocher, T. D. (2003). Genetic basis of adaptive shape differences in the cichlid head. Journal of Heredity, 94(4), 291–301.

    Article  PubMed  CAS  Google Scholar 

  • Albertson, R. C., Streelman, J. T., Kocher, T. D., & Yelick, P. C. (2005). Integration and evolution of the cichlid mandible: The molecular basis of alternate feeding strategies. Proceedings of the National Academy of Sciences of the United States of America, 102(45), 16287–16292.

    Article  PubMed  CAS  Google Scholar 

  • Alibert, P., Moureau, B., Dommergues, J. L., & David, B. (2001). Differentiation at a microgeographical scale within two species of ground beetle, Carabus auronitens and C-nemoralis (Coleoptera, Carabidae): A geometrical morphometric approach. Zoologica Scripta, 30(4), 299–311.

    Article  Google Scholar 

  • Allen, G. R. (Ed.). (1991). Damselfishes of the world (p. 271). Melle: Publication of Natural History and Pets Book, Mergus.

    Google Scholar 

  • Barel, C. D. N. (1983). Towards a constructional morphology of cichlid fishes (Teleostei, Perciformes). Netherlands Journal of Zoology, 33(4), 357–424.

    Article  Google Scholar 

  • Bell, L. J., Moyer, J. T., & Numachi, K. (1982). Morphological and genetic variation in Japanese populations of the anemonefish Amphiprion clarkii. Marine Biology, 72, 99–108.

    Article  Google Scholar 

  • Bernardi, G., Holbrook, S. J., Schmitt, R. J., Crane, N. L., & DeMartini, E. (2002). Species boundaries, populations and colour morphs in the coral reef three-spot damselfish (Dascyllus trimaculatus) species complex. Proceedings of the Royal Society of London Series B-Biological Sciences, 269(1491), 599–605.

    Article  Google Scholar 

  • Bookstein, F. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge: University Press.

    Google Scholar 

  • Bookstein, F. L., Gunz, P., Mitteroecker, P., Prossinger, H., Schaefer, K., & Seidler, H. (2003). Cranial integration in Homo: Singular warps analysis of the midsagittal plane in ontogeny and evolution. Journal of Human Evolution, 44(2), 167–187.

    Article  PubMed  Google Scholar 

  • Bouton, N., Witte, F., & Van Alphen, J. J. M. (2002). Experimental evidence for adaptive phenotypic plasticity in a rock-dwelling cichlid fish from Lake Victoria. Biological Journal of the Linnean Society, 77(2), 185–192.

    Article  Google Scholar 

  • Bowen, B. W., Muss, A., Rocha, L. A., & Grant, W. S. (2006). Shallow mtDNA coalescence in atlantic pygmy angelfishes (Genus Centropyge) indicates a recent invasion from the Indian Ocean. Journal of Heredity, 97(1), 1–12.

    Article  PubMed  CAS  Google Scholar 

  • Bunje, P. M. E. (2005). Pan-European phylogeography of the aquatic snail Theodoxus fluviatilis (Gastropoda : Neritidae). Molecular Ecology, 14(14), 4323–4340.

    Article  PubMed  CAS  Google Scholar 

  • Cardini, A., Jansson, A.-U., & Elton, S. (2007). A geometric morphometric approach to the study of ecogeographical and clinal variation in vervet monkeys. Journal of Biogeography, 34(10), 1663–1678.

    Article  Google Scholar 

  • Cooper, W. J., & Westneat, M. W. (2009). Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches. BMC Evolutionary Biology, 9, 24.

  • Dieringer, D., & Schlotterer, C. (2003). MICROSATELLITE ANALYSER (MSA): A platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 3(1), 167–169.

    Article  CAS  Google Scholar 

  • Drew, J. A., Allen, G. R., & Erdmann, M. V. (2010). Congruence between mitochondrial genes and color morphs in a coral reef fish: Population variability in the Indo-Pacific damselfish Chrysiptera rex (Snyder, 1909). Coral Reefs, 29(2), 439–444.

    Article  Google Scholar 

  • Edwards, S., Claude, J., Van Vuuren, B. J., & Matthee, C. A. (2011). Evolutionary history of the Karoo bush rat, Myotomys unisulcatus (Rodentia: Muridae): Disconcordance between morphology and genetics. Biological Journal of the Linnean Society, 102(3), 510–526.

    Article  Google Scholar 

  • Elshoud-Oldenhave, M. J. W., & Osse, J. W. M. (1976). Functional morphology of the feeding system in the ruff—Gymnocephalus cernua (L. 1758)—(Teleostei, Percidae). Journal of Morphology, 150(2), 399–422.

    Article  Google Scholar 

  • Escoufier, Y. (1973). Le traitement des variables vectorielles. Biometrics, 29, 751–760.

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Frédérich, B., Fabri, G., Lepoint, G., Vandewalle, P., & Parmentier, E. (2009). Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Récif of Toliara, Madagascar. Ichthyological Research, 56(1), 10–17.

    Article  Google Scholar 

  • Frédérich, B., Pilet, A., Parmentier, E., & Vandewalle, P. (2008). Comparative trophic morphology in eight species of damselfishes (Pomacentridae). Journal of Morphology, 269(2), 175–188.

    Article  PubMed  Google Scholar 

  • Frédérich, B., & Sheets, H. D. (2010). Evolution of ontogenetic allometry shaping giant species: A case study from the damselfish genus Dascyllus (Pomacentridae). Biological Journal of the Linnean Society, 99(1), 99–117.

    Article  Google Scholar 

  • Frédérich, B., & Vandewalle, P. (2011). Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: An example from damselfishes (Pomacentridae). BMC Evolutionary Biology, 11, 82.

    Google Scholar 

  • Garnier, S., Magniez-Jannin, F., Rasplus, J. Y., & Alibert, P. (2005). When morphometry meets genetics: Inferring the phylogeography of Carabus solieri using Fourier analyses of pronotum and male genitalia. Journal of Evolutionary Biology, 18(2), 269–280.

    Article  PubMed  CAS  Google Scholar 

  • Gluckmann, I., & Vandewalle, P. (1998). Morphofunctional analysis of the feeding apparatus in four Pomacentridae species: Dascyllus aruanus, Chromis retrofasciata, Chrysiptera biocellata and C-unimaculata. Italian Journal of Zoology, 65, 421–424.

    Article  Google Scholar 

  • Goudet, J. (1995). FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity, 86(6), 485–486.

    Google Scholar 

  • Guo, S. W., & Thompson, E. A. (1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48(2), 361–372.

    Article  PubMed  CAS  Google Scholar 

  • Hegrenes, S. (2001). Diet-induced phenotypic plasticity of feeding morphology in the orangespotted sunfish, Lepomis humilis. Ecology of Freshwater Fish, 10(1), 35–42.

    Article  Google Scholar 

  • Jackson, D. A. (1995). PROTEST—A Procrustean randomization test of community environment concordance. Ecoscience, 2(3), 297–303.

    Google Scholar 

  • Jones, G. P., Milicich, M. J., Emslie, M. J., & Lunow, C. (1999). Self-recruitment in a coral reef fish population. Nature, 402(6763), 802–804.

    Article  CAS  Google Scholar 

  • Jones, G. P., Planes, S., & Thorrold, S. R. (2005). Coral reef fish larvae settle close to home. Current Biology, 15(14), 1314–1318.

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg, C. P. (1998). Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biological Reviews, 73(1), 79–123.

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology, Evolution, and Systematics, 39, 115–132.

    Article  Google Scholar 

  • Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11(4), 405–421.

    Article  Google Scholar 

  • Kokita, T. (2003). Potential latitudinal variation in egg size and number of a geographically widespread reef fish, revealed by common-environment experiments. Marine Biology, 143(3), 593–601.

    Article  Google Scholar 

  • Kokita, T. (2004). Latitudinal compensation in female reproductive rate of a geographically widespread reef fish. Environmental Biology of Fishes, 71(3), 213–224.

    Article  Google Scholar 

  • Kuo, S.-R., & Shao, K.-T. (1991). Feeding habits of damselfishes (Pomacentridae) from the southern part of Taiwan. Journal of the Fisheries Society of Taiwan, 18(3), 165–176.

    Google Scholar 

  • Leis, J. M. (1991). The pelagic stage of reef fishes. In P. F. Sale (Ed.), The ecology of fishes on coral reefs (pp. 183–230). San Diego: Academic Press.

    Google Scholar 

  • Liem, K. F. (1978). Modulatory multiplicity in the functional repertoire of the feeding mechanism in cichlid fishes. Journal of Morphology, 158(3), 323–360.

    Article  Google Scholar 

  • Liem, K. F. (1993). Ecomorphology of the teleostean skull. In J. Hanken & B. K. Hall (Eds.), The skull: functional and evolutionary mechanisms (pp. 422–452). Chicago: The University of Chicago Press.

    Google Scholar 

  • Liem, K. F., & Osse, J. W. M. (1975). Biological versatility, evolution, and food resource exploitation in african cichlid fishes. American Zoologist, 15, 427–454.

    Google Scholar 

  • Liu, S., Dai, C. F., Fan, T. Y., & Yu, H. T. (2005). Cloning and characterization of Microsatellite loci in a gorgonian coral, Junceella juncea (Anthozoa; Octocorallia; Ellisellidae) and its application in clonal genotyping. Marine Biotechnology, 7(1), 26–32.

    Article  PubMed  CAS  Google Scholar 

  • Liu, S.-Y. V., Kokita, T., & Dai, C.-F. (2008). Population genetic structure of the neon damselfish (Pomacentrus coelestis) in the northwestern Pacific Ocean. Marine Biology, 154(4), 745–753.

    Article  Google Scholar 

  • Liu, S.-Y. V., Yu, H.-T., & Dai, C.-F. (2007). Eight microsatellite loci in Clark’s anemonefish, Amphiprion clarkii. Molecular Ecology Notes, 7(6), 1169–1171.

    Article  CAS  Google Scholar 

  • Loh, Y.-H. E., Katz, L. S., Mims, M. C., Kocher, T. D., Yi, S. V., & Streelman, J. T. (2008). Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids. Genome Biology, 9(7), R113.

    Google Scholar 

  • Mabuchi, K., Miya, M., Azuma, Y., & Nishida, M. (2007). Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes. BMC Evolutionary Biology, 7, 10.

    Google Scholar 

  • McMillan, W. O., Weigt, L. A., & Palumbi, S. R. (1999). Color pattern evolution, assortative mating, and genetic differentiation in brightly colored butterflyfishes (Chaetodontidae). Evolution, 53(1), 247–260.

    Article  Google Scholar 

  • Michaux, J. R., Magnanou, E., Paradis, E., Nieberding, C., & Libois, R. (2003). Mitochondrial phylogeography of the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Molecular Ecology, 12(3), 685–697.

    Article  PubMed  CAS  Google Scholar 

  • Miller-Sims, V., Delaney, M., Atema, J., Kingsford, M. J., & Gerlach, G. (2005). DNA microsatellites in the neon damselfish (Pomacentrus coelestis). Molecular Ecology Notes, 5(2), 424–426.

    Article  CAS  Google Scholar 

  • Molina, W. F., Shibatta, O. A., & Galetti-Jr, P. M. (2006). Multivariate morphological analysis in continental and island populations of Abudefduf saxatilis (Linnaeus) (Pomacentridae, Perciformes) of Wesern Atlantic. Pan-American Journal of Aquatic Sciences, 1(2), 49–56.

    Google Scholar 

  • Muschick, M., Barluenga, M., Salzburger, W., & Meyer, A. (2011). Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evolutionary Biology, 11, 116.

    Google Scholar 

  • Nei, M., Tajima, M., & Tateno, Y. (1983). Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution, 19, 153–170.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, J. S. (2006). Fishes of the world (p. 601). Hoboken: Wiley.

    Google Scholar 

  • Nice, C. C., & Shapiro, A. M. (1999). Molecular and morphological divergence in the butterfly genus Lycaeides (Lepidoptera: Lycaenidae) in North America: Evidence of recent speciation. Journal of Evolutionary Biology, 12(5), 936–950.

    Article  CAS  Google Scholar 

  • Osse, J. W. M. (1969). Functional morphology of the head of the perch (Perca fluvatilis L.): An electromyographic study. Netherlands Journal of Zoology, 19(3), 289–392.

    Article  Google Scholar 

  • Otten, E. (1983). The jaw mechanism during growth of a genralized Haplochromis species: H. elegans Trewavas 1933 (Pisces, Cichlidae). Netherlands Journal of Zoology, 33(1), 55–98.

    Article  Google Scholar 

  • Parsons, K. J., & Albertson, R. C. (2009). Roles for Bmp4 and CaM1 in shaping the jaw: Evo-devo and beyond. Annual Review of Genetics, 43, 369–388.

    Google Scholar 

  • Peres-Neto, P. R., & Jackson, D. A. (2001). How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia, 129(2), 169–178.

    Article  Google Scholar 

  • Planes, S. (1993). Genetic differentiation in relation to restricted larval dispersal of the convict surgeonfish Acanthurus triostegus in French Polynesia. Marine Ecology-Progress Series, 98(3), 237–246.

    Article  Google Scholar 

  • R Development Core Team. (2011). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN: 3-900051-07-0. http://www.R-project.org/.

  • Raymond, M., & Rousset, F. (1995). GENEPOP (Version-1.2)—Population-genetics software for exact tests and ecumenicism. Journal of Heredity, 86(3), 248–249.

    Google Scholar 

  • Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution, 43(1), 223–225.

    Article  Google Scholar 

  • Roberts, R. B., Hu, Y., Albertson, R. C., & Kocher, T. D. (2011). Craniofacial divergence and ongoing adaptation via the hedgehog pathway. Proceedings of the National Academy of Sciences of the United States of America, 108(32), 13194–13199.

    Article  PubMed  CAS  Google Scholar 

  • Rocha, L. A. (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 

  • Rocha, L. A., Robertson, D. R., Roman, J., & Bowen, B. W. (2005). Ecological speciation in tropical reef fishes. Proceedings of the Royal Society B-Biological Sciences, 272(1563), 573–579.

    Google Scholar 

  • Rohlf, F. J. (1993). Relative warps analysis and an example of its application to mosquito wings. In L. F. Marcus, E. Bello, A. G-V, (Eds.), Contributions to morphometrics (pp. 131–159). Madrid: Monografias del Museo Nacional de Ciencias Naturales, CSIC.

  • Rohlf, F. J. (1999). On the use of shape spaces to compare morpho-metric methods. Hystrix, 11, 1–17.

    Google Scholar 

  • Rohlf, F. J., & Corti, M. (2000). Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49(4), 740–753.

    Article  PubMed  CAS  Google Scholar 

  • Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecology & Evolution, 8(4), 129–132.

    Article  Google Scholar 

  • Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39(1), 40–59.

    Article  Google Scholar 

  • Sale, P. F. (1980). The ecology of fishes on coral reefs. Oceanography and Marine Biology, 18, 367–421.

    Google Scholar 

  • Sale, P. F. (1991). Reef fish communities: open nonequilibrial systems. In P. F. Sale (Ed.), The ecology of fishes on coral reefs (pp. 564–598). San Diego, CA: Academic Press.

    Google Scholar 

  • Schultz, J. K., Pyle, R. L., DeMartini, E., & Bowen, B. W. (2007). Genetic connectivity among color morphs and Pacific archipelagos for the flame angelfish, Centropyge loriculus. Marine Biology, 151(1), 167–175.

    Article  Google Scholar 

  • Streelman, J. T., Albertson, R. C., & Kocher, T. D. (2007). Variation in body size and trophic morphology within and among genetically differentiated populations of the cichlid fish, Metriaclima zebra, from Lake Malawi. Freshwater Biology, 52(3), 525–538.

    Article  Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24(8), 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, W. R., & Van Dyke, G. C. (1985). Revised procedure for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9, 107–121.

    Google Scholar 

  • Turelli, M., Barton, N. H., & Coyne, J. A. (2001). Theory and speciation. Trends in Ecology & Evolution, 16(7), 330–343.

    Article  Google Scholar 

  • Wainwright, P. C., & Richard, B. A. (1995). Predicting patterns of prey use from morphology of fishes. Environmental Biology of Fishes, 44(1–3), 97–113.

    Article  Google Scholar 

  • Wright, S. (1951). The genetical structure of populations. The Annals of Eugenics, 15, 323–354.

    Article  Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer (p. 443). San Diego: Elsevier Academic Press.

    Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Kokita, Ming-Jay Ho and Dr. Yu-Rong Cheng for fish sampling. We thank two anonymous reviewers for valuable comments on this manuscript. This study was partially supported by a grant (NSC95-2611-M002-011-MY3) from the National Science Council, ROC to CFD. Bruno Frédérich is a Postdoctoral Researcher of the F.R.S.-FNRS (Belgium).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. Frédérich.

Additional information

B. Frédérich and S.-Y. V. Liu contributed equally to this study.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frédérich, B., Liu, SY.V. & Dai, CF. Morphological and Genetic Divergences in a Coral Reef Damselfish, Pomacentrus coelestis . Evol Biol 39, 359–370 (2012). https://doi.org/10.1007/s11692-011-9158-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-011-9158-z

Keywords

Navigation