Journal Article

The rediscovery of a long described species reveals additional complexity in speciation patterns of poeciliid fishes in sulfide springs.

Palacios, M., Arias-Rodriguez, L., Plath, M., Eifert, C., Lerp, H., Lamboj, A. and Tobler, M.

Record Number:
5039
Year:
2013
Journal:
PLoS One
Volume:
8, e71069
Abstract:
The process of ecological speciation drives the evolution of locally adapted and reproductively isolated populations in response to divergent natural selection. In Southern Mexico, several lineages of the freshwater fish species of the genus Poecilia have independently colonized toxic, hydrogen sulfide-rich springs. Even though ecological speciation processes are increasingly well understood in this system, aligning the taxonomy of these fish with evolutionary processes has lagged behind. While some sulfide spring populations are classified as ecotypes of Poecilia mexicana, others, like P. sulphuraria, have been described as highly endemic species. Our study particularly focused on elucidating the taxonomy of the long described sulfide spring endemic, Poecilia thermalis Steindachner 1863, and investigates if similar evolutionary patterns of phenotypic trait divergence and reproductive isolation are present as observed in other sulfidic species of Poecilia. We applied a geometric morphometric approach to assess body shape similarity to other sulfidic and non-sulfidic fish of the genus Poecilia. We also conducted phylogenetic and population genetic analyses to establish the phylogenetic relationships of P. thermalis and used a population genetic approach to determine levels of gene flow among Poecilia from sulfidic and non-sulfidic sites. Our results indicate that P. thermalis' body shape has evolved in convergence with other sulfide spring populations in the genus. Phylogenetic analyses placed P. thermalis as most closely related to one population of P. sulphuraria, and population genetic analyses demonstrated that P. thermalis is genetically isolated from both P. mexicana ecotypes and P. sulphuraria. Based on these findings, we make taxonomic recommendations for P. thermalis. Overall, our study verifies the role of hydrogen sulfide as a main factor shaping convergent, phenotypic evolution and the emergence of reproductive isolation between Poecilia populations residing in adjacent sulfidic and non-sulfidic environments.
Times Cited:
1
Related Records:
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Population Structure, Habitat Use, and Diet of Giant Waterbugs in a Sulfidic Cave
Bierbach, D., Penshorn, M., Hamfler, S., Herbert, D. B., Appel, J., Meyer, P., et al. (2013)
Gradient evolution of body colouration in surface- and cave-dwelling Poecilia mexicana and the role of phenotype-assortative female mate choice.
Bierbach, D., Shulte, M., Hermann, N., Zimmer, C., Arias-Rodriguez, L., Indy, J.R., Riesch, R. and Plath, M. (2013)
Predator avoidance in extremophile fish
Langerhans, R.B. and Riesch, R. (2013)
Speciation by selection: A framework for understanding ecology's role in speciation
Rosales-Lagarde, L., Boston, P., Campbell, A., Hose, L., Axen, G. and Stafford, K.W. (2014)
Hydrogeology of northern Sierra de Chiapas, Mexico: a conceptual model based on a geochemical characterization of sulfide-rich karst brackish springs
Riesch, R., Plath, M., Schlupp, I., Tobler, M. and Langerhans, R.B. (2014)
Colonization of toxic springs drives predictable life-history shift in livebearing fishes (Poeciliidae).
Jourdan, J., Bierbach, D., Riesch, R., Dzienko, J., Karau, N., Oranth, A., Stadler, S., Schießl, A., Wigh, A., Arias-Rodriguez, L., Indy, J.R., Klaus, S., Zimmer, C. and Plath, M. (2014)
Microhabitat use, population densities and size distributions of sulfur cave-dwelling Poecilia mexicana
Tobler, M., Plath, M., Riesch, R., Schlupp, I., Grasse, A., Munimanda, G.K., Setzer, C., Penn, D.J. and Moodley, Y. (2014)
Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations
Pfenninger, M., Lerp, H., Tobler, M., Passow, C., Kelley, J.L., Funke, E., Greshake, B., Erkoc, U.K., Berberich, T. and Plath, M. (2014)
Parallel evolution of cox-genes in H2S-tolerant fish as key adaptation to a toxic environment
Greenway, R., Arias-Rodriguez, L., Diaz, P. and Tobler, M. (2014)
Patterns of macroinvertebrate and fish diversity in freshwater sulphide springs
Eifert, C., Farnworth, M., Schulz-Mirbach, T., Riesch, R., Bierbach, D., Klaus, S., Wurster, A., Tobler, M., Streit, B., Indy, J.R., Arias-Rodriguez, L. and Plath, M. (2014)
Brain size variation in extremophile fish: local adaptation versus phenotypic plasticity
Palacios-Vargas, J.G., Juberthie, C. and Reddell, J. (2014-2015)
Encyclopaedia Biospeologica Mexico
Pfenninger, M., Patel, S., Arias-Rodriguez, L., Feldmeyer, B., Riesch, R. and Plath, M. (2015)
Unique evolutionary trajectories in repeated adaptation to hydrogen sulphide-toxic habitats of a neotropical fish (Poecilia mexicana)
Tobler, M., Scharnweber, K., Greenway, R., Passow, C.N., Arias-Rodriguez, L. and Garcıa-De-Leon, F.J.. (2015)
Convergent changes in the trophic ecology of extremophile fish along replicated environmental gradients
Riesch, R., Tobler, M. and Plath, M. (2015)
Extremophile Fishes: Ecology, Evolution, and Physiology of Teleosts in Extreme Environments
Passow, C.N., Greenway, R., Arias-Rodriguez, L., Jeyasingh, P.D. and Tobler, M. (2015)
Reduction of energetic demands through modification of body size and routine metabolic rates in extremophile fish
Riesch, R, Tobler, CM and Plath, M (2015)
Hydrogen sulphide-toxic habitats
Plath, M., Tobler, M. and Riesch, R. (2015)
Extremophile fishes: An introduction
Tobler, M. and Riesch, R. and Plath, M. (2015)
Extremophile fishes: An integrative synthesis
Riesch, R., Reznick, D.N., Plath, M. and Schlupp, I. (2016)
Sex-specific local life-history adaptation in surface- and cave-dwelling Atlantic mollies (Poecilia mexicana).
Jourdan, J., Jordan, M., Zimmer, C., Eifert, C., Arias-Rodriguez, L. and Plath, M. (2016)
Response to conspecific chemical cues in surface- and cave-dwelling populations of Atlantic mollies, Poecilia mexicana
Sommer-Trembo, C., Bierbach, D., Arias Rodriguez, L., Verel, Y., Jourdan, J., Zimmer, C. and Plath, M. (2016)
Does personality affect premating isolation between locally-adapted populations?
Kelley, J.L., Arias-Rodriguez, L., Patacsil Martin, D., Yee, M.C., Bustamante, C.D. and Tobler, M. (2016)
Mechanisms underlying adaptation to life in Hydrogen sulfide–rich environments
Tobler, M., Passow, C.N., Greenway, R., Kelley, J.L. and Shaw, J.H. (2016)
The evolutionary ecology of animals inhabiting hydrogen sulfide-rich environments
Palacios, M., Voelker, G. and Rodriguez, L.A. (2016)
Phylogenetic analyses of the subgenus Mollienesia (Poecilis, Poeciliidae, Teleostei) reveal taxonomic inconsistencies, cryptic biodiversity and spatio-temporal aspects of diversification in Middle America
Riesch, R., Tobler, C.M., Lerp, H., Jourdan, J., Doumas, T., Nosil, P., Langerhans, R.B. and Plath, M. (2016)
Extremophile Poeciliidae: Multivariate insights into the complexity of speciation along replicated ecological gradients
Culumber, Z.W., Hopper, G.W., Barts, N., Passow, C.N., Morgan, S., Brown, A. andTobler, M. (2016)
Habitat use of two extremophile, highly endemic, and critically endangered fish species (Gambusia eurystoma and Poecilia sulphurophila; Poeciliidae).
Greenway, R., Drexler, S., Arias-Rodriguez, L. and Tobler, M. (2016)
Adaptive, but not condition-dependent, body shape differences contribute to assortative mating preferences during ecological speciation.
Schulz-Mirbach, T.. Eifert, C., Riesch, R. et al. (2016)
Toxic hydrogen sulphide shapes brain anatomy: a comparative study of sulphide-adapted ecotypes in the Poecilia mexicana complex
Passow, C.N., Henpita, C., Shaw, J.H., Quakenbush, C., Warren, W.C., Schartl, M. and Tobler, M. (2017)
The roles of plasticity and evolutionary change in shaping gene expression variation in natural populations of extremophile fish
Reznick, D.N., Furness, A.I., Meredith, R.W. and Springer, M.S. (2017)
The origin and biogeographic diversification of fishes in the family Poeciliidae
Oke, K. B., Rolshausen, G., LeBlond, C. and Hendry, A. P. (2017)
How parallel is parallel evolution? A comparative analysis in fishes
Passow C.N., Arias-Rodriguez L. and Tobler, M. (2017)
Convergent evolution of reduced energy demands in extremophile fish
Brown, A.P., Greenway, R., Morgan, S., Quackenbush, C.R., Giordani, L., Arias-Rodriguez, L., Tobler, M. and Kelley, J.L. (2017)
Genome-scale data reveal that endemic Poecilia populations from small sulphidic springs display no evidence of inbreeding
Passow, C.N., Brown, A.P., Kelley, J.L. and Tobler, M. (2017)
Organ-specific patterns of gene expression among extremophile fish populations exposed to toxic hydrogen sulfide and permanent darkness
Passow, Courtney N.; Brown, Anthony P.; Arias-Rodriguez, Lenin; et al. (2017)
Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana, Poeciliidae)
Hose, L.D. and Rosales-Lagarde, L. (2017)
Sulfur-rich caves of southern Tabasco, Mexico
Barts, N., Greenway, R., Passow, C.N., Arias Rodriguez, L., Kelley, J.L., and Tobler, M. (2017)
Expression and molecular evolution of oxygen transport genes in livebearing fishes (Poeciliidae) from hydrogen sulfide rich springs
Culumber, Z.W. and Tobler, M. (2017)
Sex-specific evolution during the diversification of live-bearing fishes.
Bierbach, D., Lukas. J.A., Bergmann, A., Elsner, K., Höhne, L., Weber, C., Weimar, N., Redriguez, L.A., Mönck, H.J., Nguyen, H., Romanczuk, P., Landgraf, T. and Krause, J. (2018)
Insights into the social behavior of surface and cave-dwelling fish (Poecilia mexicana) in light and darkness through the use of a biomimetic robot
Tobler, M., Kelley, J.L., Plath, M., and Riesch, R. (2018)
Extreme environments and the origins of biodiversity: Adaptation and speciation in sulphide spring fishes
Bierbach, D., Arias-Rodriguez, L. and Plath, M. (2018)
Intrasexual competition enhances reproductive isolation between locally adapted populations
Torres-Dowdall, J., Karagic, N., Plath, M. and Riesch, R. (2018)
Evolution in caves: selection from darkness causes spinal deformities in teleost fishes
Lau, G.Y., Barts, N., Hartley, R.C., Tobler, M., Richards, J.G., Murphy, M.P. and Arndt, S. (2019)
Detection of changes in mitochondrial hydrogen sulfide in vivo in the fish model Poecilia mexicana (Poeciliidae)
Torres-Martínez, A., Ruiz de Dios, L., Hernández-Franyutti, A., Uribe, M.C., and Sánchez, W.C. (2019)
Structure of the testis and spermatogenesis of the viviparous teleost Poecilia mexicana (Poeciliidae) from an active sulfur spring cave in Southern Mexico
McGowan, K.L., Passow, C.N., Arias-Rodriguez, L., Tobler, M. and Kelley, J.L. (2019)
Expression analyses of cave mollies (Poecilia mexicana) reveal key genes involved in the early evolution of eye regression.
McGowan, K.L., Passow, C.N., Arias-Rodriguez, L., Tobler, M and Kelley, J.L. (2019)
Supplementary material for "Expression analyses of cave mollies (Poecilia mexicana) reveal key genes involved in the early evolution of eye regression"
Riesch, R., Morley, N.J., Jourdan, J., Arias-Rodriguez, L. and Plath, M. (2020)
Sulphide-toxic habitats are not refuges from parasite infections in an extremophile fish
Warren, M.L. and Burr, B.M. (2020)
Freshwater fishes of North America. Volume 2 Characidae to Poeciliidae
Camarillo, H., Arias-Rodriguez, L. and Tobler, M. (2020)
Functional consequences of phenotypic variation between locally adapted populations: swimming performance and ventilation in extremophile fish
Ghedotti, M.J., Davis, M.P. and Echelle, A.A. (2020)
Poeciliidae: Livebearers
Owens, G.L., Veen, T., Moxley, D.R., Arias-Rodriguez, L., Tobler, M. and Rennison, D.J. (2021)
Parallel shifts of visual sensitivity and body coloration in replicate populations of extremophile fish
Kelley J.L., Desvignes T., McGowan K.L., Perez M., Rodriguez L. A., Brown A.P., . . . and Tobler M. (2021)
microRNA expression variation as a potential molecular mechanism contributing to adaptation to hydrogen sulphide
Riesch, R., Curtis, A., Jourdan, J., Schlupp, I. Arias-Rodriguez, L. and Plath, M. (2022)
Two ecological gradients drive phenotypic differentiation of a cave fish over a few hundred metres
Riesch, R. Arriaga, L.R. and Schlupp, I. (2023)
Sex-specific life-history trait expression in hybrids of a cave- and surface-dwelling fish (Poecilia mexicana, Poeciliidae)
Wilkens, H. (2023)
The general significance of variability in cave regressive traits for evolution
Nobrega, M.D. (2023)
Adaptation in sulfide spring fishes: experimental approaches
Johnson, E.S., Johnson, S.D., McNemee, R., Greenway, R., Rodriguez, L.A. and Tobler, M. (2024)
Genital evolution in the dark: characterization of male and female genitalia in cave mollies and their surface ancestors (Poecilia mexicana, Poeciliidae)
De-Kayne, R., Perry, B.W., McGowan, K.L., Landers, J., Arias-Rodriguez, L., Greenway, R., Rodríguez Peña, C.M., Tobler, M. and Kelley, J.L. (2024)
Evolutionary rate shifts in coding and regulatory regions underpin repeated adaptation to sulfidic streams in Poeciliid fishes
Nobrega, M., Greenway, R., Passow, C.N., Rodriguez, L.A. and Tobler, M. (2024)
Effects of plasticity and genetic divergence in phenotypic trait expression of sulfide spring fishes