Abstract
Coastal regions represent environments with heterogenic ecological conditions and with potential barriers to dispersal, making them ideal systems to study the variation of morphology and genetics of the organisms inhabiting them. Using individuals of the damselfish Abudefduf saxatilis from the three main reef systems along the Mexican Atlantic coast, we examined genetic and environmental variation to evaluate their relative contribution to body and head shape, and body size. We determined if there was a relationship between morphological variation and environmental factors and whether morphological, mitochondrial DNA (mtDNA) and microsatellite variation were concordant. We found morphological differences among A. saxatilis individuals from the Tuxpan, Veracruz and Mexican Caribbean reef systems. Differences in body and head shape involved positions of pectoral fins and mouth. Individuals from Tuxpan and Veracruz were larger than those from the Mexican Caribbean. Furthermore, we found a significant correlation between shape (body and head) and environmental variables (chlorophyll-a, geostrophic velocity and temperature) as well as between body size and chlorophyll-a concentration. Both mtDNA and microsatellite markers detected high levels of genetic diversity and lack of population genetic differentiation among reefs, reef systems and between marine regions. We did not find a correlation between morphological and genetic differentiation. Our results suggest that the phenotypic differences of A. saxatilis along the Mexican Atlantic coast may be determined by environmental factors in the presence of gene flow.
Similar content being viewed by others
References
Aguilar-Medrano, R., Frédérich, B., Balart, E. F., & De Luna, E. (2013). Diversification of the pectoral fin shape in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific. Zoomorphology, 132, 197–213.
Aguilar-Medrano, R., Frédérich, B., De Luna, E., & Balart, E. F. (2011). Patterns of morphological evolution of the cephalic region in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific. Biological Journal of the Linnean Society, 102, 593–613.
Albrecht, H. (1969). Behavior of four species of Atlantic damselfish from Columbia, South America, (Abudefduf saxatilis, A. taurus, Chromis multilineata, C. cyanea; Pisces Pomacentridae). Zeitschrift Fur Tierpsychologie-Journal Of Comparative Ethology, 26, 662–676.
Aljanabi, S. M., & Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25, 4692–4693.
Andersson, J., Byström, P., Persson, L., & Roos, A. M. D. (2005). Plastic resource polymorphism: Effects of resource availability on Arctic char (Salvelinus alpinus) morphology. Biological Journal of the Linnean Society, 85, 341–351.
Andras, J. P., Kirk, N. L., & Harvell, C. D. (2011). Range-wide population genetic structure of Symbiodinium associated with the Caribbean Sea fan coral, Gorgonia ventalina. Molecular Ecology, 20, 2525–2542.
Andras, J. P., Kirk, N. L., & Harvell, C. D. (2013). Range-wide population genetic structure of the Caribbean sea fan coral, Gorgonia ventalina. Molecular Ecology, 22, 56–73.
Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge: Harvard University Press.
Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.
Binning, S. A., Roche, D. G., & Fulton, C. J. (2014). Localised intraspecific variation in the swimming phenotype of a coral reef fish across different wave exposures. Oecologia, 174, 623–630.
Booth, D. J., & Hixon, M. A. (1999). Food ration and condition affect early survival of the coral reef damselfish, Stegastes partitus. Oecologia, 121, 364–368.
Bowen, B. W., Bass, A. L., Muss, A., Carlin, J., & Robertson, D. R. (2006). Phylogeography of two Atlantic squirrelfishes (Family Holocentridae): Exploring links between pelagic larval duration and population connectivity. Marine Biology, 149, 899–913.
Carvalho, M. C., Streiff, R., Guillemaud, T., Afonso, P., Santos, R. S., & Cancela, M. L. (2000). Isolation and characterization of polymorphic microsatellite markers in Abudefduf luridus (Pisces: Pomacentridae). Molecular Ecology, 9, 993–1011.
Castro, J. J., Santiago, J. A., & Santana-Ortega, A. T. (2002). A general theory on fish aggregation to floating objects: An alternative to the meeting point hypothesis. Reviews in Fish Biology and Fisheries, 11, 255–277.
Cavalli-Sforza, L. L., & Edwards, A. W. F. (1967). Phylogenetic analysis models and estimation procedures. American Journal of Human Genetics, 19, 233–257.
Chapuis, M. P., & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621–631.
Chávez-Hidalgo, A. (2009). Conectividad de los arrecifes coralinos del Golfo de México y Caribe mexicano. Master thesis. Instituto Politécnico Nacional.
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.
Costa, C., Vandeputte, M., Antonucci, F., Boglione, I., Menesatti, P., Cenadelli, S., et al. (2010). Genetic and environmental influences on shape variation in the European sea bass (Dicentrarchus labrax). Biological Journal of the Linnean Society, 101, 427–436.
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.
DeWoody, J. A., & Avise, J. C. (2000). Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. Journal of Fish Biology, 56, 461–473.
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, 439–444.
Elmer, K. R., Kusche, H., Lehtonen, T. K., & Meyer, A. (2010). Local variation and parallel evolution: Morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 1763–1782.
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software structure: A simulation study. Molecular Ecology, 14, 2611–2620.
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.
Fishelson, L. (1970). Behaviour and ecology of a population of Abudefduf saxatilis (Pomacentridae, Teleostei) at Eilat (Red Sea). Animal Behaviour, 18, 225–237.
Frédérich, B., Liu, S. Y. V., & Dai, C. F. (2012). Morphological and genetic divergences in a coral reef damselfish, Pomacentrus coelestis. Evolutionary Biology, 39, 359–370.
Frédérich, B., Pilet, A., Parmentier, E., & Vandewalle, P. (2008). Comparative trophic morphology in eight species of damselfishes (Pomacentridae). Journal of Morphology, 269, 175–188.
Fulton, C. J., Binning, S. A., Wainwright, P. C., & Bellwood, D. R. (2013). Wave-induced abiotic stress shapes phenotypic diversity in a coral reef fish across a geographical cline. Coral Reefs, 32, 685–689.
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, 269–280.
Gerlanch, G., Jueterbock, A., Kraemer, P., Deppermann, J., & Hardmand, P. (2010). Calculations of populations differentiation based on GST and D: Forget GST but not all of statistics! Molecular Ecology, 19, 2845–3852.
Gompert, Z., Comeault, A. A., Farkas, T. E., Feder, J. L., Parchman, T. L., Buerkle, C. A., & Nosil, P. (2014). Experimental evidence for ecological selection on genome variation in the wild. Ecology Letters, 17, 369–379.
Goudet, J. (1995). Fstat version 1.2: A computer program to calculate F statistics. Journal of Heredity, 86, 485–486.
Heatwole, S. J., & Fulton, C. J. (2013). Behavioural flexibility in reef fishes responding to a rapidly changing wave environment. Marine Biology, 160, 677–689.
Hendry, A. P. (2013). Key questions in the genetics and genomics of eco-evolutionary dynamics. Heredity, 111, 456–466.
Ho, A. L. F. C., Pruett, C. L., & Lin, J. (2012). Population genetic structure, coloration, and morphometrics of yellowhead jawfish Opistognathus aurifrons (Perciformes: Opistognathidae) in the Caribbean region. Marine Ecology Progress Series, 444, 275–287.
Hubisz, M. J., Falush, D., Stephens, M., & Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322–1332.
Imre, I., McLaughlin, R. L., & Noakes, D. L. G. (2002). Phenotypic plasticity in brook charr: Changes in caudal fin induced by water flow. Journal of Fish Biology, 61, 1171–1181.
Jost, L. (2008). GST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015–4016.
Kalinowski, S. T. (2004). Counting alleles with rarefaction: Private alleles and hierarchical sampling designs. Conservation Genetics, 5, 539–543.
Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241.
Keeney, D. B., Heupel, M. R., Hueter, R. E., & Heist, E. J. (2005). Microsatellite and mitochondrial DNA analyses of the genetic structure of black tip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Molecular Ecology, 14, 1911–1923.
Kingsolver, J. G., & Huey, R. B. (2008). Size, temperature, and fitness: Three rules. Evolutionary Ecology Research, 10, 251–268.
Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.
Lalli, C. M., & Parson, T. R. (2006). Biological oceanography: An introduction (p. 20). Oxford: Elsevier Butterworth-Heinemann.
Langella, O. (2004). POPULATIONS 1.2.29.: Population genetic software (individuals or populations distances, phylogenetic trees), http://www.bioinformatics.org/download/populations/. Accessed 20 Oct 2013.
Langerhans, R. B. (2008). Predictability of phenotypic differentiation across flow regimes in fishes. Integrative and Comparative Biology, 48, 750–768.
Lauder, G. V., & Jayne, B. C. (1996). Pectoral fin locomotion in fishes: Testing drag-based models using 3-dimensional kinematics. American Zoologist, 36, 567–581.
Loh, Y.-H., Katz, L. S., Mims, M. C., Kocher, T. D., Yis, S. V., & Streelam, J. T. (2008). Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids. Genome Biology, 2008(9), r113.
Macdonnell, J. A. (1990). Biomechanics of rheotaxis in hill stream fish. Vancuver, British Columbia: The University of British Columbia.
Marcil, J., Swain, D. P., & Hutchings, J. A. (2006). Genetic and environmental components of phenotypic variation in body shape among populations of Atlantic cod (Gadus morhua L.). Biological Journal of the Linnean Society, 88, 351–365.
McLaughlin, R. L., & Grant, J. W. A. (1994). Morphological and behavioural differences among recently-emerged brook charr, Salvelinus fontinalis, foraging in slow- vs. fast-running water. Environmental Biology of Fishes, 39, 289–300.
Meekan, M. G., Ackerman, J. L., & Wellington, G. M. (2001). Demography and age structures of coral reef damselfishes in the tropical eastern Pacific Ocean. Marine Ecology Progress Series, 212, 223–232.
Mitteroecker, P., & Bookstein, F. (2011). Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evolutionary Biology, 38, 100–114.
Mitteroecker, P., & Gunz, P. (2009). Advances in geometric morphometrics. Evolutionary Biology, 36, 235–247.
Molina, W. F., Shibatta, O. A., & Galetti-Jr, P. M. (2006). Multivariate morphological analyses in continental and island populations of Abudefduf saxatilis (Linnaeus) (Pomacentridae, Perciformes) of Western Atlantic. Pan-American Journal of Aquatic Science, 1, 49–56.
Nei, M., & Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings National Academy of Sciences Usa, 76, 5269–5273.
Nosil, P. (2008). Speciation with gene flow could be common. Molecular Ecology, 17, 2103–2106.
Okolodkov, Y. B. (2003). A review of Russian plankton research in the Gulf of Mexico and the Caribbean Sea in the 1960–1980s. Hidrobiologica, 13, 207–221.
Pakkasmaa, S., & Pironen, J. (2001). Water velocity, shape juvenile salmonids. Evolutionary Ecology, 14, 721–730.
Peakall, R., & Smouse, P. E. (2006). GENALEX 6 genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.
Piñeros, V. J., Gutiérrez-Rodríguez, C., & Lance, S. L. (2015). Development and characterization of 29 microsatellite markers for the sergeant major damselfish (Abudefduf saxatilis) using paired-Illumina shotgun sequencing. Conservation Genetic Resources, 7, 103–105.
Poelstra, J. W., Vijay, N., Bossu, C. M., Lantz, H., Ryll, B., Müller, I., et al. (2014). The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science, 344, 1410–1414.
Pritchard, J. K., Stephens, P., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
Purcell, J. F. H., Cowen, R. K., Hughes, C. R., & Williams, D. A. (2006). Weak genetic structure indicates strong dispersal limits: A tale of two coral reef fish. Proceedings of the Royal Society B: Biological Sciences, 273, 1483–1490.
R Development Core Team. (2009). 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.
Rice, W. R. (1989). Analyzing tables of statistical test. Evolution, 43, 223–2235.
Rice, W. R., & Hostert, E. E. (1993). Laboratory experiments on speciation: What have we learned in forty years? Evolution, 47, 1637–1653.
Rohlf, F. J. (2004). TpsDig, digitize landmarks and outlines, version 2.0.. Stony Brook, New York: Stony Brook State University of New York.
Rohlf, F. J. (2014). TpsPLS, version 1.22. Stony Brook, New York: Stony Brook State University of New York.
Rohlf, F. J., & Corti, M. (2000). The use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49, 740–753.
Rousset, F. (2008). Genepop’007: A complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103–106.
Rüber, L., & Adams, D. C. (2001). Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika. Journal of Evolutionary Biology, 14, 325–332.
Salas-Pérez, J. J., Salas-Monreal, D., Monreal-Gómez, M. A., Riveron-Enzastiga, M. L., & Llasat, C. (2012). Seasonal absolute acoustic intensity, atmospheric forcing and currents in a tropical coral reef system. Estuarine, Coastal and Shelf Science, 100, 102–112.
Schlager, S. (2014). Package Morpho. http://cran.r-project.org/web/packages/Morpho/Morpho.pdf
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, 167–175.
Sfakianakis, D. G., Leris, I., Laggis, A., & Kentouri, M. (2011). The effect of rearing temperature on body shape and meristic characters in zebrafish (Danio rerio) juveniles. Enviromental Biology of Fishes, 92, 197–205.
Sheets, H. D. (2001). CoordGen6. Buffalo, New York: Canisius College.
Streelman, J. T., Alfaro, M., Westneat, M. W., Bellwood, D. R., & Karl, S. A. (2002). Evolutionary history of the parrotfishes: Biogeography, ecomorphology, and comparative diversity. Evolution, 56, 961–971.
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., & Shipley, P. (2004). MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538.
Villegas Sánchez, C. A., Pérez-España, H., Rivera-Madrid, R., Salas-Monreal, D., & Arias-González, J. E. (2014). Subtle genetic connectivity between Mexican Caribbean and south-western Gulf of Mexico reefs: The case of the bicolor damselfish, Stegastes partitus. Coral Reefs, 33, 241–251.
Villegas-Sánchez, C. A., Rivera-Madrid, R., & Arias-González, J. E. (2010). Small-scale genetic connectivity of bicolor damselfish (Stegastes partitus) recruits in Mexican Caribbean reefs. Coral Reefs, 29, 1023–1033.
Wainwright, P. C., Bellwood, D. R., Westneat, M. W., Grubich, J. R., & Hoey, A. S. (2004). A functional morphospace for the skull of labrid fishes: Patterns of diversity in a complex biomechanical system. Biological Journal of the Linnean Society, 82, 1–25.
Weir, B. S., & Cockerham, C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. New York: Elsevier Academic Press.
Acknowledgments
We would like to thank Rogelio Macías-Ordóñez, Borja Mila and Molly Morris for valuable comments on earlier versions of this work. Arturo Serrano-Solis and Horacio Perez-España provided logistic support in Tuxpan and Veracruz respectively. We are grateful to Ismael Valdivieso for his help in the field, to Roger Guevara for statistical assistance, to Cristina Barcenas and Denisse Maldonado for laboratory assistance, and to Israel Lorea for his help with the maps. The Comisión Nacional de Areas Naturales Protegidas (CONANP) also provided logistic support in Contoy Island, Cozumel Island and Sian Ka’an. Sara Lariza Rivera made the A. saxatilis drawing. This work was supported by a Sigma Xi Grant (G2009151270) to VJP and a Consejo Nacional de Ciencia y Tecnología (CONACyT) Grant (134804) to ORC. VJP was supported by a Doctoral scholarship (20163) from CONACyT. Collecting permits (DGOPA/00327/250110.0195, 07510/220911/2718) were granted by the Comisión Nacional de Acuacultura y Pesca (CONAPESCA).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Piñeros, V.J., Rios-Cardenas, O., Gutiérrez-Rodríguez, C. et al. Morphological Differentiation in the Damselfish Abudefduf saxatilis Along the Mexican Atlantic Coast is Associated with Environmental Factors and High Connectivity. Evol Biol 42, 235–249 (2015). https://doi.org/10.1007/s11692-015-9314-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-015-9314-y