Molecular evolution and expression of oxygen transport genes in livebearing fishes (Poeciliidae) from hydrogen sulfide rich springs

Nicholas Barts; Ryan Greenway; Courtney N. Passow; Lenin Arias-Rodriguez; Joanna L. Kelley; Michael Tobler

doi:10.1139/gen-2017-0051

Molecular evolution and expression of oxygen transport genes in livebearing fishes (Poeciliidae) from hydrogen sulfide rich springs

Nicholas Barts, Ryan Greenway, Courtney N. Passow, Lenin Arias-Rodriguez, Joanna L. Kelley, Michael Tobler

Genomics Center

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

Hydrogen sulfide (H₂S) is a natural toxicant in some aquatic environments that has diverse molecular targets. It binds to oxygen transport proteins, rendering them non-functional by reducing oxygen-binding affinity. Hence, organisms permanently inhabiting H₂S-rich environments are predicted to exhibit adaptive modifications to compensate for the reduced capacity to transport oxygen. We investigated 10 lineages of fish of the family Poeciliidae that have colonized freshwater springs rich in H₂S-along with related lineages from non-sulfidic environments-to test hypotheses about the expression and evolution of oxygen transport genes in a phylogenetic context. We predicted shifts in the expression of and signatures of positive selection on oxygen transport genes upon colonization of H₂S-rich habitats. Our analyses indicated significant shifts in gene expression for multiple hemoglobin genes in lineages that have colonized H₂S-rich environments, and three hemoglobin genes exhibited relaxed selection in sulfidic compared to non-sulfidic lineages. However, neither changes in gene expression nor signatures of selection were consistent among all lineages in H₂S-rich environments. Oxygen transport genes may consequently be predictable targets of selection during adaptation to sulfidic environments, but changes in gene expression and molecular evolution of oxygen transport genes in H₂S-rich environments are not necessarily repeatable across replicated lineages.

Original language	English (US)
Pages (from-to)	273-286
Number of pages	14
Journal	Genome
Volume	61
Issue number	4
DOIs	https://doi.org/10.1139/gen-2017-0051
State	Published - 2018

Bibliographical note

Funding Information:
This work was supported by grants from the National Science Foundation (IOS-1463720, IOS-1557795, and IOS-1557860), the Army Research Office (W911NF-15-1-0175), and the Defense University Research Instrumentation Program of the U.S. Office of Naval Research (W911NF-16-1-0225) to M.T. and J.L.K. In addition, N.B. was supported by a Graduate Assistance in Areas of National Need (GAANN) Fellowship, R.G. was supported by an NSF Graduate Research Fellowship (GRFP), and C.N.P. was supported by the University of Minnesota Grand Challenges Postdoctoral Program.

Funding Information:
We thank the communities of Teapa and Tapijulapa, as well as local landowners and Villa Luz Nature Park, for providing access to study sites. We are indebted to Centro de Investigación e Inno-vación para la Enseñanza y Aprendizaje (CIIEA) and Universidad Juárez Autónoma de Tabasco (UJAT) for their hospitality and support over many years of research. We thank I. Schlupp and J.B. Johnson for providing samples of Limia, and Rori Rohlfs for advice during the analysis of gene expression data. Permits were provided by the Mexican Federal Agencies SEMARNAT and CONAPESCA (DGOPA.09004.041111.3088, SGPA/DGVS/04315/11, PRMN/DGOPA-003/2014, PRMN/DGOPA-009/2015). This work was supported by grants from the National Science Foundation (IOS-1463720, IOS-1557795, and IOS-1557860), the Army Research Office (W911NF-15-1-0175), and the Defense University Research Instrumentation Program of the U.S. Office of Naval Research (W911NF-16-1-0225) to M.T. and J.L.K. In addition, N.B. was supported by a Graduate Assistance in Areas of National Need (GAANN) Fellowship, R.G. was supported by an NSF Graduate Research Fellowship (GRFP), and C.N.P. was supported by the University of Minnesota Grand Challenges Postdoctoral Program.

Publisher Copyright:
© 2018 Published by NRC Research Press.

Keywords

Adaptation
Convergent evolution
Hemoglobin
Molecular evolution
Myoglobin
Sulfide springs

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title = "Molecular evolution and expression of oxygen transport genes in livebearing fishes (Poeciliidae) from hydrogen sulfide rich springs",

abstract = "Hydrogen sulfide (H2S) is a natural toxicant in some aquatic environments that has diverse molecular targets. It binds to oxygen transport proteins, rendering them non-functional by reducing oxygen-binding affinity. Hence, organisms permanently inhabiting H2S-rich environments are predicted to exhibit adaptive modifications to compensate for the reduced capacity to transport oxygen. We investigated 10 lineages of fish of the family Poeciliidae that have colonized freshwater springs rich in H2S-along with related lineages from non-sulfidic environments-to test hypotheses about the expression and evolution of oxygen transport genes in a phylogenetic context. We predicted shifts in the expression of and signatures of positive selection on oxygen transport genes upon colonization of H2S-rich habitats. Our analyses indicated significant shifts in gene expression for multiple hemoglobin genes in lineages that have colonized H2S-rich environments, and three hemoglobin genes exhibited relaxed selection in sulfidic compared to non-sulfidic lineages. However, neither changes in gene expression nor signatures of selection were consistent among all lineages in H2S-rich environments. Oxygen transport genes may consequently be predictable targets of selection during adaptation to sulfidic environments, but changes in gene expression and molecular evolution of oxygen transport genes in H2S-rich environments are not necessarily repeatable across replicated lineages.",

keywords = "Adaptation, Convergent evolution, Hemoglobin, Molecular evolution, Myoglobin, Sulfide springs",

author = "Nicholas Barts and Ryan Greenway and Passow, {Courtney N.} and Lenin Arias-Rodriguez and Kelley, {Joanna L.} and Michael Tobler",

note = "Funding Information: This work was supported by grants from the National Science Foundation (IOS-1463720, IOS-1557795, and IOS-1557860), the Army Research Office (W911NF-15-1-0175), and the Defense University Research Instrumentation Program of the U.S. Office of Naval Research (W911NF-16-1-0225) to M.T. and J.L.K. In addition, N.B. was supported by a Graduate Assistance in Areas of National Need (GAANN) Fellowship, R.G. was supported by an NSF Graduate Research Fellowship (GRFP), and C.N.P. was supported by the University of Minnesota Grand Challenges Postdoctoral Program. Funding Information: We thank the communities of Teapa and Tapijulapa, as well as local landowners and Villa Luz Nature Park, for providing access to study sites. We are indebted to Centro de Investigaci{\'o}n e Inno-vaci{\'o}n para la Ense{\~n}anza y Aprendizaje (CIIEA) and Universidad Ju{\'a}rez Aut{\'o}noma de Tabasco (UJAT) for their hospitality and support over many years of research. We thank I. Schlupp and J.B. Johnson for providing samples of Limia, and Rori Rohlfs for advice during the analysis of gene expression data. Permits were provided by the Mexican Federal Agencies SEMARNAT and CONAPESCA (DGOPA.09004.041111.3088, SGPA/DGVS/04315/11, PRMN/DGOPA-003/2014, PRMN/DGOPA-009/2015). This work was supported by grants from the National Science Foundation (IOS-1463720, IOS-1557795, and IOS-1557860), the Army Research Office (W911NF-15-1-0175), and the Defense University Research Instrumentation Program of the U.S. Office of Naval Research (W911NF-16-1-0225) to M.T. and J.L.K. In addition, N.B. was supported by a Graduate Assistance in Areas of National Need (GAANN) Fellowship, R.G. was supported by an NSF Graduate Research Fellowship (GRFP), and C.N.P. was supported by the University of Minnesota Grand Challenges Postdoctoral Program. Publisher Copyright: {\textcopyright} 2018 Published by NRC Research Press.",

year = "2018",

doi = "10.1139/gen-2017-0051",

language = "English (US)",

volume = "61",

pages = "273--286",

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T1 - Molecular evolution and expression of oxygen transport genes in livebearing fishes (Poeciliidae) from hydrogen sulfide rich springs

AU - Barts, Nicholas

AU - Greenway, Ryan

AU - Passow, Courtney N.

AU - Arias-Rodriguez, Lenin

AU - Kelley, Joanna L.

AU - Tobler, Michael

N1 - Funding Information: This work was supported by grants from the National Science Foundation (IOS-1463720, IOS-1557795, and IOS-1557860), the Army Research Office (W911NF-15-1-0175), and the Defense University Research Instrumentation Program of the U.S. Office of Naval Research (W911NF-16-1-0225) to M.T. and J.L.K. In addition, N.B. was supported by a Graduate Assistance in Areas of National Need (GAANN) Fellowship, R.G. was supported by an NSF Graduate Research Fellowship (GRFP), and C.N.P. was supported by the University of Minnesota Grand Challenges Postdoctoral Program. Funding Information: We thank the communities of Teapa and Tapijulapa, as well as local landowners and Villa Luz Nature Park, for providing access to study sites. We are indebted to Centro de Investigación e Inno-vación para la Enseñanza y Aprendizaje (CIIEA) and Universidad Juárez Autónoma de Tabasco (UJAT) for their hospitality and support over many years of research. We thank I. Schlupp and J.B. Johnson for providing samples of Limia, and Rori Rohlfs for advice during the analysis of gene expression data. Permits were provided by the Mexican Federal Agencies SEMARNAT and CONAPESCA (DGOPA.09004.041111.3088, SGPA/DGVS/04315/11, PRMN/DGOPA-003/2014, PRMN/DGOPA-009/2015). This work was supported by grants from the National Science Foundation (IOS-1463720, IOS-1557795, and IOS-1557860), the Army Research Office (W911NF-15-1-0175), and the Defense University Research Instrumentation Program of the U.S. Office of Naval Research (W911NF-16-1-0225) to M.T. and J.L.K. In addition, N.B. was supported by a Graduate Assistance in Areas of National Need (GAANN) Fellowship, R.G. was supported by an NSF Graduate Research Fellowship (GRFP), and C.N.P. was supported by the University of Minnesota Grand Challenges Postdoctoral Program. Publisher Copyright: © 2018 Published by NRC Research Press.

PY - 2018

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N2 - Hydrogen sulfide (H2S) is a natural toxicant in some aquatic environments that has diverse molecular targets. It binds to oxygen transport proteins, rendering them non-functional by reducing oxygen-binding affinity. Hence, organisms permanently inhabiting H2S-rich environments are predicted to exhibit adaptive modifications to compensate for the reduced capacity to transport oxygen. We investigated 10 lineages of fish of the family Poeciliidae that have colonized freshwater springs rich in H2S-along with related lineages from non-sulfidic environments-to test hypotheses about the expression and evolution of oxygen transport genes in a phylogenetic context. We predicted shifts in the expression of and signatures of positive selection on oxygen transport genes upon colonization of H2S-rich habitats. Our analyses indicated significant shifts in gene expression for multiple hemoglobin genes in lineages that have colonized H2S-rich environments, and three hemoglobin genes exhibited relaxed selection in sulfidic compared to non-sulfidic lineages. However, neither changes in gene expression nor signatures of selection were consistent among all lineages in H2S-rich environments. Oxygen transport genes may consequently be predictable targets of selection during adaptation to sulfidic environments, but changes in gene expression and molecular evolution of oxygen transport genes in H2S-rich environments are not necessarily repeatable across replicated lineages.

AB - Hydrogen sulfide (H2S) is a natural toxicant in some aquatic environments that has diverse molecular targets. It binds to oxygen transport proteins, rendering them non-functional by reducing oxygen-binding affinity. Hence, organisms permanently inhabiting H2S-rich environments are predicted to exhibit adaptive modifications to compensate for the reduced capacity to transport oxygen. We investigated 10 lineages of fish of the family Poeciliidae that have colonized freshwater springs rich in H2S-along with related lineages from non-sulfidic environments-to test hypotheses about the expression and evolution of oxygen transport genes in a phylogenetic context. We predicted shifts in the expression of and signatures of positive selection on oxygen transport genes upon colonization of H2S-rich habitats. Our analyses indicated significant shifts in gene expression for multiple hemoglobin genes in lineages that have colonized H2S-rich environments, and three hemoglobin genes exhibited relaxed selection in sulfidic compared to non-sulfidic lineages. However, neither changes in gene expression nor signatures of selection were consistent among all lineages in H2S-rich environments. Oxygen transport genes may consequently be predictable targets of selection during adaptation to sulfidic environments, but changes in gene expression and molecular evolution of oxygen transport genes in H2S-rich environments are not necessarily repeatable across replicated lineages.

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KW - Convergent evolution

KW - Hemoglobin

KW - Molecular evolution

KW - Myoglobin

KW - Sulfide springs

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Molecular evolution and expression of oxygen transport genes in livebearing fishes (Poeciliidae) from hydrogen sulfide rich springs

Abstract

Bibliographical note

Keywords

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