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Convergent Evolution of Conserved Mitochondrial Pathways Underlies Repeated Adaptation to Extreme Environments

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Convergent Evolution of Conserved Mitochondrial Pathways Underlies Repeated Adaptation to Extreme Environments Correction EVOLUTION Correction for “Convergent evolution of conserved mitochon- drial pathways underlies repeated adaptation to extreme envi- ronments,” by Ryan Greenway, Nick Barts, Chathurika Henpita, Anthony P. Brown, Lenin Arias Rodriguez, Carlos M. Rodríguez Peña, Sabine Arndt, Gigi Y. Lau, Michael P. Murphy, Lei Wu, Dingbo Lin, Michael Tobler, Joanna L. Kelley, and Jennifer H. Shaw, which was first published June 25, 2020; 10.1073/ pnas.2004223117 (Proc. Natl. Acad. Sci. U.S.A. 117, 16424– 16430). The authors note that, due to a printer’s error, the author line appeared incorrectly. The authors Michael Tobler, Joanna L. Kelley, and Jennifer H. Shaw should appear in the author line as Jennifer H. Shaw, Joanna L. Kelley, and Michael Tobler. The corrected author line appears below. The online version has been updated. Ryan Greenway, Nick Barts, Chathurika Henpita, Anthony P. Brown, Lenin Arias Rodriguez, Carlos M. Rodríguez Peña, Sabine Arndt, Gigi Y. Lau, Michael P. Murphy, Lei Wu, Dingbo Lin, Jennifer H. Shaw, Joanna L. Kelley, and Michael Tobler Published under the PNAS license. First published August 17, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2016076117 21822 | PNAS | September 1, 2020 | vol. 117 | no. 35 www.pnas.org Downloaded by guest on September 28, 2021 Convergent evolution of conserved mitochondrial pathways underlies repeated adaptation to extreme environments Ryan Greenwaya,1, Nick Bartsa,1, Chathurika Henpitab,1, Anthony P. Brownc, Lenin Arias Rodriguezd, Carlos M. Rodríguez Peñae, Sabine Arndtf, Gigi Y. Laug, Michael P. Murphyf, Lei Wuh, Dingbo Linh, Michael Toblera,2, Joanna L. Kelleyc,2, and Jennifer H. Shawb,2,3 aDivision of Biology, Kansas State University, Manhattan, KS 66506; bDepartment of Integrative Biology, Oklahoma State University, Stillwater, OK 74078; cSchool of Biological Sciences, Washington State University, Pullman, WA 99163; dDivisión Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, Villahermosa, Tabasco, 86150, Mexico; eInstituto de Investigaciones Botánicas y Zoológicas, Universidad Autónoma de Santo Domingo, Santo Domingo, 10105, Dominican Republic; fMedical Research Council - Mitochondrial Biology Unit, University of Cambridge, Cambridge, CB2 0XY, United Kingdom; gDepartment of Biosciences, University of Oslo, 0315 Oslo, Norway; and hDepartment of Nutritional Sciences, Oklahoma State University, Stillwater, OK 74078 Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved May 21, 2020 (received for review March 9, 2020) Extreme environments test the limits of life; yet, some organisms genetic variants were assumed to be selectively neutral (5). This thrive in harsh conditions. Extremophile lineages inspire questions paradigm has been shifting though, with mounting evidence that about how organisms can tolerate physiochemical stressors and mitochondria—and genes encoded in the mitochondrial genome— whether the repeated colonization of extreme environments is can play important roles in adaptation, especially in the context facilitated by predictable and repeatable evolutionary innova- of physiochemical stress (6). 2) Mitochondria are critical for the tions. We identified the mechanistic basis underlying convergent cellular function of eukaryotes (7). Their function is dependent evolution of tolerance to hydrogen sulfide (H2S)—a toxicant that on the gene products from two genomes, the mitochondrial and impairs mitochondrial function—across evolutionarily indepen- the nuclear (8), which interact to ultimately shape whole-organism dent lineages of a fish (Poecilia mexicana, Poeciliidae) from performance. Despite extensive characterization of allelic variation EVOLUTION H2S-rich springs. Using comparative biochemical and physiological in mitochondrial genomes, it often remains unclear how variation in analyses, we found that mitochondrial function is maintained in genes that contribute to mitochondrial function translates to the presence of H2S in sulfide spring P. mexicana but not ancestral lineages from nonsulfidic habitats due to convergent adaptations Significance in the primary toxicity target and a major detoxification enzyme. Genome-wide local ancestry analyses indicated that convergent Some organisms can tolerate environments lethal for most evolution of increased H S tolerance in different populations is 2 others, but we often do not know what adaptations allow likely caused by a combination of selection on standing genetic them to persist and whether the same mechanisms underly variation and de novo mutations. On a macroevolutionary scale, adaptation in different lineages exposed to the same stressors. H S tolerance in 10 independent lineages of sulfide spring fishes 2 Investigating fish inhabiting springs rich in toxic H S, we show across multiple genera of Poeciliidae is correlated with the conver- 2 that tolerance is mediated by the modification of pathways gent modification and expression changes in genes associated that are inhibited by H S and those that can detoxify it. Sulfide with H S toxicity and detoxification. Our results demonstrate 2 2 spring fishes across multiple genera have evolved similar that the modification of highly conserved physiological path- modifications of toxicity targets and detoxification pathways, ways associated with essential mitochondrial processes medi- despite abundant lineage-specific variation. Our study high- ates tolerance to physiochemical stress. In addition, the same lights how constraints associated with the physiological con- pathways, genes, and—in some instances—codons are impli- sequences of a stressor limit the number of adaptive solutions catedinHS adaptation in lineages that span 40 million years 2 and lead to repeatable evolutionary outcomes across organi- of evolution. zational and evolutionary scales. adaptive evolution | comparative physiology | ecological genomics | Author contributions: R.G., N.B., C.H., M.T., J.L.K., and J.H.S. designed research; R.G., N.B., hydrogen sulfide | phylogenetic comparative analysis C.H., L.A.R., C.M.R.P., S.A., G.Y.L., M.P.M., L.W., D.L., M.T., J.L.K., and J.H.S. performed research; L.A.R., C.M.R.P., S.A., G.Y.L., M.P.M., L.W., D.L., M.T., J.L.K., and J.H.S. contrib- uted new reagents/analytic tools; R.G., N.B., C.H., A.P.B., M.T., J.L.K., and J.H.S. analyzed tephen J. Gould made a strong case for the importance of data; and R.G., N.B., M.T., and J.L.K. wrote the paper. Scontingency in evolution, famously quipping that replaying The authors declare no competing interest. “ ” the tape of life would lead to different outcomes every time This article is a PNAS Direct Submission. (1). However, despite the unpredictability of mutations, the effects This open access article is distributed under Creative Commons Attribution-NonCommercial- of genetic drift, and other historical contingencies, convergent NoDerivatives License 4.0 (CC BY-NC-ND). evolution of phenotypic traits and their underlying genes is Data deposition: Data and code associated with biochemical and physiological analyses common, indicating that natural selection sometimes finds are available on GitHub (https://github.com/michitobler/convergent_h2s_evolution). All repeatable and predictable solutions to shared evolutionary sequence data are available at National Center for Biotechnology Information (NCBI) BioProject (accession nos. PRJNA473350 and PRJNA608180). challenges (2, 3). A major challenge that remains is the 1R.G., N.B., and C.H. contributed equally to this work. identification of the ecological, genetic, and functional factors 2To whom correspondence may be addressed. Email: [email protected], joanna.l.kelley@ that might determine the repeatability and predictability of wsu.edu, or [email protected]. evolutionary outcomes (4). 3Present address: Department of Biomedical Sciences, PCOM South Georgia, Moultrie, Mitochondria and their genomes provide a fascinating model GA 31768. to ask questions about the predictability of evolution for two This article contains supporting information online at https://www.pnas.org/lookup/suppl/ reasons: 1) Mitochondrial genomes were historically thought to doi:10.1073/pnas.2004223117/-/DCSupplemental. be a prime example of contingency evolution because alternative www.pnas.org/cgi/doi/10.1073/pnas.2004223117 PNAS Latest Articles | 1of7 variation in physiological and organismal function. Furthermore, it (Fig. 1B; habitat × H2S: P < 0.001, SI Appendix, Table S3). Even is not known whether exposure to similar selective regimes may though the drainage of origin was not retained as an explanatory cause convergent modifications of mitochondrial genomes and variable in statistical models (SI Appendix, Table S2), COX ac- emergent biochemical and physiological functions in evolutionarily tivity in one H2S-tolerant population [Tacotalpa (Tac)] declined independent lineages. just as in nonsulfidic populations (Fig. 1B). The other two P. Extreme environments that represent novel ecological niches mexicana populations from sulfidic habitats [Puyacatengo (Puy) are natural experiments to address questions about mechanisms and Pichucalco (Pich)] maintained significant COX activity even underlying mitochondrial adaptations and illuminate the pre- at the highest H2S concentrations, which should reduce the dictability of adaptive evolution of mitochondria. Among the negative impact of H2S on cellular respiration. These results are most extreme freshwater ecosystems are springs with high levels consistent with previous analyses (15) and indicate that
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