Skip to main content

Advertisement

Log in

Morphological Differentiation in the Damselfish Abudefduf saxatilis Along the Mexican Atlantic Coast is Associated with Environmental Factors and High Connectivity

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

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.

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

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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge: Harvard University Press.

    Google Scholar 

  • Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Cavalli-Sforza, L. L., & Edwards, A. W. F. (1967). Phylogenetic analysis models and estimation procedures. American Journal of Human Genetics, 19, 233–257.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chapuis, M. P., & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621–631.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • 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.

    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, 439–444.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  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 

  • Fishelson, L. (1970). Behaviour and ecology of a population of Abudefduf saxatilis (Pomacentridae, Teleostei) at Eilat (Red Sea). Animal Behaviour, 18, 225–237.

    Article  Google Scholar 

  • 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.

    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, 175–188.

    Article  PubMed  Google Scholar 

  • 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.

    Article  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, 269–280.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Heatwole, S. J., & Fulton, C. J. (2013). Behavioural flexibility in reef fishes responding to a rapidly changing wave environment. Marine Biology, 160, 677–689.

    Article  Google Scholar 

  • Hendry, A. P. (2013). Key questions in the genetics and genomics of eco-evolutionary dynamics. Heredity, 111, 456–466.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Jost, L. (2008). GST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015–4016.

    Article  PubMed  Google Scholar 

  • Kalinowski, S. T. (2004). Counting alleles with rarefaction: Private alleles and hierarchical sampling designs. Conservation Genetics, 5, 539–543.

    Article  CAS  Google Scholar 

  • Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Kingsolver, J. G., & Huey, R. B. (2008). Size, temperature, and fitness: Three rules. Evolutionary Ecology Research, 10, 251–268.

    Google Scholar 

  • Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.

    Article  PubMed  Google Scholar 

  • Lalli, C. M., & Parson, T. R. (2006). Biological oceanography: An introduction (p. 20). Oxford: Elsevier Butterworth-Heinemann.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Macdonnell, J. A. (1990). Biomechanics of rheotaxis in hill stream fish. Vancuver, British Columbia: The University of British Columbia.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Mitteroecker, P., & Bookstein, F. (2011). Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evolutionary Biology, 38, 100–114.

    Article  Google Scholar 

  • Mitteroecker, P., & Gunz, P. (2009). Advances in geometric morphometrics. Evolutionary Biology, 36, 235–247.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Nosil, P. (2008). Speciation with gene flow could be common. Molecular Ecology, 17, 2103–2106.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Pakkasmaa, S., & Pironen, J. (2001). Water velocity, shape juvenile salmonids. Evolutionary Ecology, 14, 721–730.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Pritchard, J. K., Stephens, P., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rice, W. R., & Hostert, E. E. (1993). Laboratory experiments on speciation: What have we learned in forty years? Evolution, 47, 1637–1653.

    Article  Google Scholar 

  • Rohlf, F. J. (2004). TpsDig, digitize landmarks and outlines, version 2.0.. Stony Brook, New York: Stony Brook State University of New York.

    Google Scholar 

  • Rohlf, F. J. (2014). TpsPLS, version 1.22. Stony Brook, New York: Stony Brook State University of New York.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rousset, F. (2008). Genepop’007: A complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103–106.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Sheets, H. D. (2001). CoordGen6. Buffalo, New York: Canisius College.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Weir, B. S., & Cockerham, C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.

    Article  Google Scholar 

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

    Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Oscar Rios-Cardenas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 328 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-015-9314-y

Keywords

Navigation