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.
Bibliographical noteFunding 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.
- Convergent evolution
- Molecular evolution
- Sulfide springs