[en] 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.
Research center :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Zoology
Author, co-author :
Frederich, Bruno ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Liu, S.-Y. Vanson
Dai, C.-F.
Language :
English
Title :
Morphological and genetic divergences in a coral reef damselfish, Pomacentrus coelestis
Publication date :
September 2012
Journal title :
Evolutionary Biology
ISSN :
0071-3260
eISSN :
1934-2845
Publisher :
Springer Science & Business Media B.V.
Volume :
39
Issue :
3
Pages :
359-370
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
National Science Council (Taiwan) NSC95-2611-M002-011- MY3
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.
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.
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.
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.
Allen, G. R. (Ed.). (1991). Damselfishes of the world (p. 271). Melle: Publication of Natural History and Pets Book, Mergus.
Barel, C. D. N. (1983). Towards a constructional morphology of cichlid fishes (Teleostei, Perciformes). Netherlands Journal of Zoology, 33(4), 357-424.
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.
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.
Bookstein, F. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge: University Press.
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.
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.
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.
Bunje, P. M. E. (2005). Pan-European phylogeography of the aquatic snail Theodoxus fluviatilis (Gastropoda: Neritidae). Molecular Ecology, 14(14), 4323-4340.
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.
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.
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.
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.
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.
Escoufier, Y. (1973). Le traitement des variables vectorielles. Biometrics, 29, 751-760.
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.
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.
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.
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.
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.
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.
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.
Goudet, J. (1995). FSTAT (Version 1. 2): A computer program to calculate F-statistics. Journal of Heredity, 86(6), 485-486.
Guo, S. W., & Thompson, E. A. (1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48(2), 361-372.
Hegrenes, S. (2001). Diet-induced phenotypic plasticity of feeding morphology in the orangespotted sunfish, Lepomis humilis. Ecology of Freshwater Fish, 10(1), 35-42.
Jackson, D. A. (1995). PROTEST-A Procrustean randomization test of community environment concordance. Ecoscience, 2(3), 297-303.
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.
Jones, G. P., Planes, S., & Thorrold, S. R. (2005). Coral reef fish larvae settle close to home. Current Biology, 15(14), 1314-1318.
Klingenberg, C. P. (1998). Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biological Reviews, 73(1), 79-123.
Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology, Evolution, and Systematics, 39, 115-132.
Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11(4), 405-421.
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.
Kokita, T. (2004). Latitudinal compensation in female reproductive rate of a geographically widespread reef fish. Environmental Biology of Fishes, 71(3), 213-224.
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.
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.
Liem, K. F. (1978). Modulatory multiplicity in the functional repertoire of the feeding mechanism in cichlid fishes. Journal of Morphology, 158(3), 323-360.
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.
Liem, K. F., & Osse, J. W. M. (1975). Biological versatility, evolution, and food resource exploitation in african cichlid fishes. American Zoologist, 15, 427-454.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Nei, M., Tajima, M., & Tateno, Y. (1983). Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution, 19, 153-170.
Nelson, J. S. (2006). Fishes of the world (p. 601). Hoboken: Wiley.
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.
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.
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.
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.
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.
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.
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.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution, 43(1), 223-225.
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.
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.
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.
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.
Rohlf, F. J., & Corti, M. (2000). Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49(4), 740-753.
Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecology & Evolution, 8(4), 129-132.
Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39(1), 40-59.
Sale, P. F. (1980). The ecology of fishes on coral reefs. Oceanography and Marine Biology, 18, 367-421.
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.
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.
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.
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.
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.
Turelli, M., Barton, N. H., & Coyne, J. A. (2001). Theory and speciation. Trends in Ecology & Evolution, 16(7), 330-343.
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.
Wright, S. (1951). The genetical structure of populations. The Annals of Eugenics, 15, 323-354.
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.
