Journal Article
Evolutionary rate shifts in coding and regulatory regions underpin repeated adaptation to sulfidic streams in Poeciliid fishes
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.
Record Number:
6404
Year:
2024
Journal:
Genome Biology and Evolution
Pages:
1-16
Volume:
16(5)
Notes:
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium
Abstract:
Adaptation to extreme environments often involves the evolution of dramatic physiological changes. To better understand
how organisms evolve these complex phenotypic changes, the repeatability and predictability of evolution, and possible constraints
on adapting to an extreme environment, it is important to understand how adaptive variation has evolved. Poeciliid
fishes represent a particularly fruitful study system for investigations of adaptation to extreme environments due to their repeated
colonization of toxic hydrogen sulfide–rich springs across multiple species within the clade. Previous investigations
have highlighted changes in the physiology and gene expression in specific species that are thought to facilitate adaptation
to hydrogen sulfide–rich springs. However, the presence of adaptive nucleotide variation in coding and regulatory regions
and the degree to which convergent evolution has shaped the genomic regions underpinning sulfide tolerance across
taxa are unknown. By sampling across seven independent lineages in which nonsulfidic lineages have colonized and adapted
to sulfide springs, we reveal signatures of shared evolutionary rate shifts across the genome. We found evidence of genes,
promoters, and putative enhancer regions associated with both increased and decreased convergent evolutionary rate shifts
in hydrogen sulfide–adapted lineages. Our analysis highlights convergent evolutionary rate shifts in sulfidic lineages associated
with the modulation of endogenous hydrogen sulfide production and hydrogen sulfide detoxification. We also found
that regions with shifted evolutionary rates in sulfide spring fishes more often exhibited convergent shifts in either the coding
region or the regulatory sequence of a given gene, rather than both.
Times Cited:
1
Relevent Species:
Related Records:
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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
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).
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
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
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
Palacios-Vargas, J.G., Juberthie, C. and Reddell, J. (2014-2015)Encyclopaedia Biospeologica Mexico
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
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
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).
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
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
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
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
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)
Culumber, Z.W. and Tobler, M. (2017)Sex-specific evolution during the diversification of live-bearing fishes.
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
Passow C.N., Arias-Rodriguez L. and Tobler, M. (2017)Convergent evolution of reduced energy demands in extremophile fish
Hose, L.D. and Rosales-Lagarde, L. (2017)Sulfur-rich caves of southern Tabasco, Mexico
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
Oke, K. B., Rolshausen, G., LeBlond, C. and Hendry, A. P. (2017)How parallel is parallel evolution? A comparative analysis in 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
Bierbach, D., Arias-Rodriguez, L. and Plath, M. (2018)Intrasexual competition enhances reproductive isolation between locally adapted populations
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
Torres-Dowdall, J., Karagic, N., Plath, M. and Riesch, R. (2018)Evolution in caves: selection from darkness causes spinal deformities in teleost fishes
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"
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.
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
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
Ghedotti, M.J., Davis, M.P. and Echelle, A.A. (2020)Poeciliidae: Livebearers
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
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
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