Skip to main content

Advertisement

SpringerLink
Log in

Species and shape diversification are inversely correlated among gobies and cardinalfishes (Teleostei: Gobiiformes)

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Gobies and their relatives are significant components of nearshore marine, estuarine, and freshwater fish faunas in both tropical and temperate habitats worldwide. They are remarkable for their ability to adapt to and diversify in a wide range of environments. Among gobiiform clades, species diversities vary widely, ranging from two species in Kurtidae to more than 1,000 species in Gobiidae. There is also great variation in head and body shape and in environmental preferences (fresh, brackish, or marine habitats). In this study, I used a time-calibrated molecular phylogeny, coupled with morphometric and comparative analyses, to examine evolutionary rates of both speciation and morphological diversification among gobiiform lineages. Projection of the phylogeny onto a shape-derived morphospace shows that Gobioidei is morphometrically distinct from its sister taxon Apogonoidei, but that families within Gobioidei overlap in morphospace. Analysis of species diversification rates indicates that three rate shifts have occurred over the evolutionary history of Gobiiformes. Relative to the other lineages, Kurtidae has exhibited a slowdown in speciation, whereas both Apogonidae and Gobiidae + Gobionellidae have experienced an increase in diversification. Comparative analyses show that in Apogonidae and Gobiidae + Gobionellidae, increased speciation is correlated with diminished rates of morphological diversification, differently manifested in either clade and among the various sublineages. The elevation in speciation rates and diminishment in rates of morphological change in both Apogonidae and the clade Gobiidae + Gobionellidae are correlated with shifts to oceanic habitats from freshwater. This pattern is the complement to that seen across the global radiation of acanthomorph fishes in which a decrease in species diversification is associated with an increase in morphological disparity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adams, D. C., Burns, C. M., Kozak, K. H., & Wiens, J. J. (2009). Are rates of species diversification correlated with rates of morphological evolution? Proceedings of the Royal Society of London B, 276, 2729–2738.

    Article  Google Scholar 

  • Agoretta, A., San Mauro, S., Schliewen, U., Van Tassell, J. L., Kovacic, M., Zardoya, R., & Rüber, L. (2013). Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies. Molecular Phylogenetics and Evolution, 69(3), 619–633.

    Article  Google Scholar 

  • Aguilar-Medrano, R., Frederich, 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 

  • Alfaro, M. E., Santini, F., & Brock, C. (2007). Do reefs drive diversification in marine teleosts? Evidence from the pufferfishes and their allies (Order Tetraodontiformes). Evolution, 61(9), 2104–2126.

    Article  PubMed  Google Scholar 

  • Alfaro, M. E., Brock, C. D., Banbury, B. L., & Wainwright, P. C. (2009a). Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evolutionary Biology, 9, 255.

    Article  PubMed Central  PubMed  Google Scholar 

  • Alfaro, M. E., Santini, F., Brock, C., Alamillo, H., Dornburg, A., Rabosky, D. L., Carnevale, G., & Harmon, L. J. (2009b). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences of the United States of America, 32, 13410–13414.

    Article  Google Scholar 

  • Bajpai, S., & Kapur, V. V. (2004). Oldest known gobiids from vastan lignite mine (early Eocene), Surat district, Gujarat. Current Science, 87, 433–435.

    CAS  Google Scholar 

  • Bannikov, A. F. (2008). Revision of some Eocene fishes from Bolca, northern Italy, previously classified with the Apogonidae and Enoplosidae (Perciformes). Studi e Ricerche sui giacimenti Terziari di Bolca, XII Miscellanea Paleontologica, 9, 65–76.

    Google Scholar 

  • Bellwood, D. R., & Wainwright, P. C. (2002). The history and biogeography of fishes on coral reefs. In P. F. Sale (Ed.), Coral reef fishes: Dynamics and diversity in a complex ecosystem (pp. 5–32). USA: Elsevier Science.

    Chapter  Google Scholar 

  • Betancur-R, R., Broughton, R. E., Wiley, E. O., Carpenter, K., Lopez, J. A., Li, C., et al. (2013). The tree of life and a new classification of bony fishes. PLoS Currents Tree of Life, 18, 5.

  • Birdsong, R. S., Murdy, E. O., & Pezold, F. L. (1988). A study of the vertebral column and median fin osteology in gobioid fishes with comments on gobioid relationships. Bulletin of Marine Science, 42(2), 174–214.

    Google Scholar 

  • Chakrabarty, P., Davis, M. P., & Sparks, J. S. (2012). The first record of a trans-oceanic sister-group relationship between obligate vertebrate troglobites. PLoS One, 7(8), e44083. doi:10.1371/journal.pone.0044083.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Collar, D. C., O’Meara, B. C., Wainwright, P. C., & Near, T. J. (2009). Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution, 63(6), 1557–1573.

    Article  PubMed  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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cowman, P. F., & Bellwood, D. R. (2011). Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. Journal of Evolutionary Biology, 24, 2543–2562.

    Article  CAS  PubMed  Google Scholar 

  • Dornburg, A., Sidlauskas, B., Santini, F., Sorenson, L., Near, T. J., & Alfaro, M. E. (2011). The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (Family: Balistidae). Evolution, 65(7), 1912–1926.

    Article  PubMed  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969–1973.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eastman, J. M., Alfaro, M. E., Joyce, P., Hipp, A. L., & Harmon, L. J. (2011). A novel comparative method for identifying shifts in the rate of character evolution on trees. Evolution, 65(12), 3578–3589.

    Article  PubMed  Google Scholar 

  • Eschmeyer, W. N. (ed). (2013). Catalog of Fishes. http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed June 2013.

  • Frédérich, B., Sorenson, L., Santini, F., Slater, G. J., & Alfaro, M. E. (2013). Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). American Naturalist, 181(3), 94–113.

    Article  PubMed  Google Scholar 

  • Friedman, M. (2010). Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction. Proceedings of the Royal Society of London B, 277, 1675–1683.

    Article  Google Scholar 

  • Froese, R., & Pauly, D. (2013) FishBase. http://www.fishbase.org. Accessed June 2013.

  • Gierl, C., Reichenbacher, B., Gaudant, J., Erpenbeck, D., & Pharisat, A. (2013). An extraordinary gobioid fish fossil from southern France. PLoS One, 8(5), e64117.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hunt, D. M., Fitzgibbon, J., Slobodyanyuk, S. J., Bowmaker, J. K., & Dulai, K. S. (1997). Molecular evolution of the cottoid fish endemic to Lake Baikal deduced from nuclear DNA evidence. Molecular Phylogenetics and Evolution, 8(3), 415–422.

    Article  CAS  PubMed  Google Scholar 

  • Jobb, G., von Haeseler, A., & Strimmer, K. (2004). TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evolutionary Biology, 4, 18.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Leviton, A. E., Gibbs, R. H., Jr., Heal, E., & Dawson, C. E. (1985). Standards in herpetology and ichthyology: Part I. Standard symbolic codes for institutional resource collections in herpetology and ichthyology. Copeia, 1985, 802–832.

    Google Scholar 

  • Litsios, G., Pellissier, L., Forest, F., Lexer, C., Pearman, P. B., Zimmermann, N. E., & Salamin, N. (2012). Trophic specialization influences the rate of environmental niche evolution in damselfishes (Pomacentridae). Proceedings of the Royal Society of London B, 279, 3662–3669.

    Article  Google Scholar 

  • Maddison, W. P. & Madison, D. R. (2011). Mesquite: a modular system for evolutionary analysis. Version 2.75. www.mesquiteproject.org. Accessed Jan 2012.

  • Martin, C. H., & Wainwright, P. C. (2011). Trophic novelty is linked to exceptional rates of morphological diversification in two adaptive radiations of Cyprinodon pupfish. Evolution, 65(8), 2197–2212.

    Article  PubMed  Google Scholar 

  • Near, T. J., Dornburg, A., Kuhn, K. L., Eastman, J. T., Pennington, J. N., Patarnello, T., Zane, L., Fernandez, D. A., & Jones, C. D. (2012a). Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proceedings of the National Academy of Sciences of the United States of America, 109(9), 3434–3439.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Near, T. J., Eytan, R. I., Dornburg, A., Kuhn, K. L., Moore, J. A., Davis, M. P., Wainwright, P. C., Friedman, M., & Smith, W. L. (2012b). Resolution of ray-finned fish diversity and timing of diversification. Proceedings of the National Academy of Sciences of the United States of America, 109(34), 13698–13703.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Near, T. J., Dornburg, A., Eytan, R. I., Keck, B. P., Smith, W. L., Kuhn, K. L., et al. (2013). Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proceedings of the National Academy of Sciences of the United States of America, 110(31), 12738–12743.

  • Nelson, J. S. (2006). Fishes of the world (4th ed.). New Jersey: Wiley.

    Google Scholar 

  • O’Meara, B. C., Ane, C., Sanderson, M. J., & Wainwright, P. C. (2006). Testing for different rates of continuous trait evolution using likelihood. Evolution, 60(5), 922–933.

    Article  PubMed  Google Scholar 

  • Pothoff, T. (1984). Clearing and staining techniques. In H. G. Moser (Ed.), Ontogeny and systematics of fishes (Spec. Pub. ASIH No. 1, pp. 35–37). Lawrence: Allen.

    Google Scholar 

  • Price, S. A., Wainwright, P. C., Bellwood, D. R., Kazancioglu, E., Collar, D. C., & Near, T. J. (2010). Functional innovations and morphological diversification in parrotfish. Evolution, 64(10), 3057–3068.

    PubMed  Google Scholar 

  • Price, S. A., Holzman, R., Near, T. J., & Wainwright, P. C. (2011). Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes. Ecology Letters, 14, 462–469.

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2011). R: a Language and Environment for Statistical Computing. http://www.r-project.org. Accessed Mar 2012.

  • Rabosky, D. L., & Adams, D. C. (2012). Rates of morphological evolution are correlated with species richness in salamanders. Evolution, 66(6), 1807–1818.

    Article  PubMed  Google Scholar 

  • Rabosky, D. L., Santini, F., Eastman, J., Smith, S. A., Sidlauskas, B., Chang, J., & Alfaro, M. E. (2013). Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications, 4, 1958.

    Article  PubMed  Google Scholar 

  • Reichenbacher, B., & Schwarz, J. (1997). Charophyten und Otolithen aus den Cyrenen-Schichten des nördlichen Alpenvorlandes. Paläontologische Zeitschrift, 71, 173–188.

    Article  Google Scholar 

  • Renema, W., Bellwood, D. R., Braga, J. C., Bromfield, K., Hall, R., Johnson, K. G., Lunt, P., Meyer, C. P., McMonagle, L. B., Morley, R. J., O’Dea, A., Todd, J. A., Wesselingh, F. P., Wilson, M. E. J., & Pandolfi, J. M. (2008). Hopping hotspots: global shifts in marine biodiversity. Science, 321, 654–657.

    Article  CAS  PubMed  Google Scholar 

  • Rohlf, F. J. (2010). TpsDig2 Software package. http://life.bio.sunysb.edu/morph. Accessed Mar 2010.

  • Sallan, L. C., & Friedman, M. (2012). Heads or tails: staged diversification in vertebrate evolutionary radiations. Proceedings of the Royal Society of London B, 279, 2025–2032.

    Article  Google Scholar 

  • Salzburger, W. S., Meyer, A., Baric, S., Verheyen, E., & Sturmbauer, C. (2002). Phylogeny of the Lake Tanganyika Cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. Systematic Biology, 51(1), 113–135.

    Article  PubMed  Google Scholar 

  • Santini, F., Harmon, L. J., Carnevale, G., & Alfaro, M. E. (2009). Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evolutionary Biology, 9, 194.

    Article  PubMed Central  PubMed  Google Scholar 

  • Santini, F., Nguyen, N. T. T., Sorenson, L., Waltzek, T. B., Lynch Alfaro, J. W., Eastman, J. M., & Alfaro, M. E. (2013). Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae). Journal of Evolutionary Biology, 26(5), 1003–1018.

    Article  CAS  PubMed  Google Scholar 

  • Sidlauskas, B. (2007). Testing for unequal rates of morphological diversification in the absence of a detailed phylogeny: a case study from characiform fishes. Evolution, 61(2), 299–316.

    Article  PubMed  Google Scholar 

  • Sidlauskas, B. (2008). Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution, 62(12), 3135–3156.

    Article  PubMed  Google Scholar 

  • Stone, J. R. (2003). Mapping cladograms into morphospaces. Acta Zoologica, 84, 63–68.

    Article  Google Scholar 

  • Tallebois, L., Castalin, M., Lord, C., Chabarria, R., Dettai, A., & Keith, P. (2013). New Sicydiinae phylogeny (Teleostei: Gobioidei) inferred from mitochondrial and nuclear genes: insights on systematics and ancestral areas. Molecular Phylogenetics and Evolution, 70, 260–271.

    Article  Google Scholar 

  • Thacker, C. E. (2009). Phylogeny of Gobioidei and placement within Acanthomorpha, with a new classification and investigation of diversification and character evolution. Copeia, 2009, 93–104.

    Article  Google Scholar 

  • Thacker, C. E. (2013). Phylogenetic placement of the European sand gobies in Gobionellidae and characterization of gobionellid lineages (Gobiiformes: Gobioidei). Zootaxa, 3619(3), 369–382.

    Article  Google Scholar 

  • Thacker, C. E., & Roje, D. M. (2009). Phylogeny of cardinalfishes (Teleostei: Gobiiformes: Apogonidae) and the evolution of visceral bioluminescence. Molecular Phylogenetics and Evolution, 52, 735–745.

    Article  CAS  PubMed  Google Scholar 

  • Thacker, C. E., & Roje, D. M. (2011). Phylogeny of Gobiidae and identification of gobiid lineages. Systematics and Biodiversity, 9(4), 329–347.

    Article  Google Scholar 

  • Tornabene, L., Chen, Y., & Pezold, F. (2013). Gobies are deeply divided: phylogenetic evidence from nuclear DNA (Teleostei: Gobioidei: Gobiidae). Systematics and Biodiversity, 11, 1–17.

    Article  Google Scholar 

  • Wood, R. (1999). Reef evolution. Oxford: Oxford University.

    Google Scholar 

  • Yoder, J. B., Clancey, E., Des Roches, S., Eastman, J. M., Gentry, L., Godsoe, W., Hagey, T. J., Jochimsen, D., Oswald, B. P., Robertson, J., Sarver, B. A. J., Schenk, J. J., Spear, S. F., & Harmon, L. J. (2010). Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology, 23, 1581–1596.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation (NSF DEB 0108416) and by grants from the W. M. Keck and R. M. Parsons Foundations in support of the program in Molecular Systematics and Evolution at the Natural History Museum of Los Angeles County. I am grateful to P. Chakrabarty, W. L. Smith, and B. Sidlauskas for their extremely generous assistance with and advice on morphometrics and analyses. Helpful advice and assistance with the MEDUSA analyses were provided by M. Alfaro and P. Gilbert. I also thank P. Chakrabarty and J. Sparks (AMNH), M. McGrouther (AMS), S. Raredon (USNM), K. Swagel (FMNH), and J. Seigel (LACM) for providing specimens and radiographs. H. Larson generously provided specimens of Kurtus gulliveri on exchange to LACM, and D. Geiger expertly prepared Figs. 3, 4, 6, and 7.

Author information

Authors and Affiliations

  1. Research and Collections, Section of Ichthyology, Natural History Museum of Los Angeles County, 900 Exposition Blvd., Los Angeles, CA, 90007, USA

    Christine E. Thacker

Authors
  1. Christine E. Thacker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine E. Thacker.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thacker, C.E. Species and shape diversification are inversely correlated among gobies and cardinalfishes (Teleostei: Gobiiformes). Org Divers Evol 14, 419–436 (2014). https://doi.org/10.1007/s13127-014-0175-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-014-0175-5

Keywords

Search

Navigation