Convergent Patterns of Body Shape Differentiation in Four Different Clades of Poeciliid Fishes Inhabiting Sulfide Springs
We investigated replicated differentiation in four lineages of livebearing fishes (two with the genus Poecilia and two within Gambusia), which inhabit freshwater habitats and have also colonized sulfide springs in Oklahoma, Mexico, and Venezuela. Sulfide springs are characterized by extreme hypoxia and high concentrations of toxic hydrogen sulfide, which provide a strong source of divergent selection compared to adjacent non-sulfidic habitats. Using geometric morphometric analysis of body shape, we found that sulfide spring populations significantly differ from relatives from regular freshwater habitats in all four lineages investigated. Differentiation is characterized by strong patterns of convergent evolution, with sulfide spring populations consistently exhibiting an increase in head size, even though the magnitude and nature differences varied across lineages. Head size is strongly correlated with an increase in gill size in sulfide spring populations of the genus Poecilia, which facilitates efficient oxygen acquisition in the hypoxic H2S-environment and directly affects survival. The convergent patterns of differentiation support previous findings about the effects of sulfide on trait evolution.
KeywordsAdaptation Convergent evolution Divergent selection Gambusia Hydrogen sulfide Poecilia
We thank N. Franssen and C. Tobler for help in the field and D. Hendrickson for help with specimen loans. We are indebted to K. Winemiller for continuous support and for sharing information about sites in Venezuela. N. Franssen, M. Plath, R. Riesch, and C. Tobler kindly provided comments on an earlier version of the manuscript. The Mexican government (CONAPESCA: DGOPA/16986/191205/8101, DGOPA/02232/230706/1079, DGOPA.06192.240608-1562, DGOPA.00093.120110.-0018, and SGPA/DGVS/04751/08) and the United States National Park Service Chickasaw NRA (CHIC-2007-SCI-0001) kindly provided collection permits. Financial support came from the National Geographic Society.
- Beatty, J. (2010). Reconsidering the importance of chance variation. In M. Pigliucci & G. B. Müller (Eds.), Evolution: The extended synthesis (pp. 21–44). Cambridge, MS: MIT Press.Google Scholar
- Covich, A. (1981). Chemical refugia from predation for thin-shelled gastropods in a sulfide-enriched stream. Verhandlungen der Internationalen Vereinigung fuer Limnologie, 21, 1632–1636.Google Scholar
- Endler, J. A. (1986). Natural selection in the wild. Princeton, NJ: Princeton University Press.Google Scholar
- Lovatt Evans, C. (1967). The toxicity of hydrogen sulphide and other sulphides. Quarterly Journal of Experimental Physiology, 52, 231–248.Google Scholar
- Lydeard, C., Wootton, M. C., & Meyer, A. (1995). Molecules, morphology, and area cladograms: A cladistic and biogeographic analysis of Gambusia (Teleostei: Poeciliidae). Systematic Biology, 44(2), 221–236.Google Scholar
- Marcia, M., Ermler, U., Peng, G., & Michel, H. (2009). The structure of Aquifex aeolicus sulfide: Quinone oxidoreductatse, a basis to understand sulfide detoxification and respiration. Proceedings of the National Academy of Sciences of the United States of America, 106(24), 9625–9630.PubMedCrossRefGoogle Scholar
- Miller, R., & Robison, H. (2004). Fishes of Oklahoma. Norman: University of Oklahoma Press.Google Scholar
- Miller, R. R. (1975). Five new species of Mexican poeciliid fishes of the genera Poecilia, Gambusia, and Poeciliopsis. Occasional Papers of the Museum of Zoology, University of Michigan, 672, 1–44.Google Scholar
- Miller, R. R., Minckley, W., & Norris, S. (2005). Freshwater fishes of Mexico. Chicago: University of Chicago Press.Google Scholar
- National Research Council. (1979). Hydrogen sulfide. Baltimore: University Park Press.Google Scholar
- Plath, M., Hauswaldt, S., Moll, K., Tobler, M., Garcia de Leon, F., Schlupp, I., et al. (2007a). Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, inhabiting a Mexican cave with toxic hydrogen sulfide. Molecular Ecology, 16, 967–976.PubMedCrossRefGoogle Scholar
- Reis, R. E., Kullander, S. O., & Ferraris, C. J. (Eds.). (2003). The check list of the freshwater fishes of South and Central America. Porto Alegre: Edipucrs.Google Scholar
- Ricklefs, R. E., & Schluter, D. (1993). Species diversity: Regional and historical influences. In R. E. Ricklefs & D. Schluter (Eds.), Species diversity in ecological communities (pp. 350–363). Chicago, IL: University of Chicago Press.Google Scholar
- Rivas, L. R. (1980). Eight new species of poeciliid fishes of the genus Limia from Hispaniola. Northeast Gulf Science, 2(2), 98–112.Google Scholar
- Rohlf, F. (2004). tpsDig. Available from http://life.bio.sunysb.edu/morph/.
- Rohlf, F. (2005). tpsRegr. Available from http://life.bio.sunysb.edu/morph/.
- Rohlf, F. (2007). tpsRelw. Available from http://life.bio.sunysb.edu/morph/.
- Rosen, D., & Bailey, R. (1963). The poeciliid fishes (Cyprinodontiformes), their structure, zoogeography and systematics. Bulletin of the American Museum of Natural History, 126, 1–176.Google Scholar
- Shahak, Y., & Hauska, G. (2008). Sulfide oxidation from cyanobacteria to humans: Sulfide-quinone oxidoreductase (SQR). In R. Hell, C. Dahl, & T. L. Knaff DB (Eds.), Advances in photosynthesis and respiration (pp. 319–335). Heidelberg: Springer.Google Scholar
- Theissen, U., Hoffmeister, M., Grieshaber, M., & Martin, W. (2003). Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Molecular Biology and Evolution, 20, 1564–1574.PubMedCrossRefGoogle Scholar
- Tobler, M., DeWitt, T. J., Schlupp, I., Garcia de Leon, F. J., Herrmann, R., Feulner, P., et al. (2008a). Toxic hydrogen sulfide and dark caves: Phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana. Evolution, 62(10), 2643–2649.PubMedCrossRefGoogle Scholar
- Tobler, M., Palacios, M., Chapman, L. J., Mitrofanov, I., Bierbach, D., Plath, M., Arias-Rodriguez, L., Garcia de Leon, F. J., Mateos, M. (2011). Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs. Evolution online first:doi: 10.1111/j.1558-5646.2011.01298.x.
- Tobler, M., & Plath, M. (2011). Living in extreme habitats. In J. Evans, A. Pilastro, & I. Schlupp (Eds.), Ecology and evolution of poeciliid fishes (pp. 120–127). Chicago: University of Chicago Press.Google Scholar
- Tobler, M., Riesch, R., Garcia de Leon, F. J., Schlupp, I., & Plath, M. (2008b). Two endemic and endangered fishes, Poecilia sulphuraria (Alvarez, 1948) and Gambusia eurystoma Miller, 1975 (Poeciliidae, Teleostei), as only survivors in a small sulfidic habitat. Journal of Fish Biology, 72(3), 523–533.CrossRefGoogle Scholar
- Tobler, M., Riesch, R., Tobler, C. M., & Plath, M. (2009a). Compensatory behaviour in response to sulfide-induced hypoxia affects time budgets, feeding efficiency, and predation risk. Evolutionary Ecology Research, 11, 935–948.Google Scholar
- Zelditch, M., Swiderski, D., Sheets, H., & Fink, W. (2004). Geometric morphometrics for biologists. Amsterdam: Elsevier Academic Press.Google Scholar