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      Convergent evolution of conserved mitochondrial pathways underlies repeated adaptation to extreme environments

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          Some organisms can tolerate environments lethal for most others, but we often do not know what adaptations allow them to persist and whether the same mechanisms underly adaptation in different lineages exposed to the same stressors. Investigating fish inhabiting springs rich in toxic H 2S, we show that tolerance is mediated by the modification of pathways that are inhibited by H 2S and those that can detoxify it. Sulfide spring fishes across multiple genera have evolved similar modifications of toxicity targets and detoxification pathways, despite abundant lineage-specific variation. Our study highlights how constraints associated with the physiological consequences of a stressor limit the number of adaptive solutions and lead to repeatable evolutionary outcomes across organizational and evolutionary scales.

          Abstract

          Extreme environments test the limits of life; yet, some organisms thrive in harsh conditions. Extremophile lineages inspire questions about how organisms can tolerate physiochemical stressors and whether the repeated colonization of extreme environments is facilitated by predictable and repeatable evolutionary innovations. We identified the mechanistic basis underlying convergent evolution of tolerance to hydrogen sulfide (H 2S)—a toxicant that impairs mitochondrial function—across evolutionarily independent lineages of a fish ( Poecilia mexicana, Poeciliidae) from H 2S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H 2S in sulfide spring P. mexicana but not ancestral lineages from nonsulfidic habitats due to convergent adaptations in the primary toxicity target and a major detoxification enzyme. Genome-wide local ancestry analyses indicated that convergent evolution of increased H 2S tolerance in different populations is likely caused by a combination of selection on standing genetic variation and de novo mutations. On a macroevolutionary scale, H 2S tolerance in 10 independent lineages of sulfide spring fishes across multiple genera of Poeciliidae is correlated with the convergent modification and expression changes in genes associated with H 2S toxicity and detoxification. Our results demonstrate that the modification of highly conserved physiological pathways associated with essential mitochondrial processes mediates tolerance to physiochemical stress. In addition, the same pathways, genes, and—in some instances—codons are implicated in H 2S adaptation in lineages that span 40 million years of evolution.

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          The genomic basis of adaptive evolution in threespine sticklebacks

          Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.
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            Convergence, adaptation, and constraint.

            Convergent evolution of similar phenotypic features in similar environmental contexts has long been taken as evidence of adaptation. Nonetheless, recent conceptual and empirical developments in many fields have led to a proliferation of ideas about the relationship between convergence and adaptation. Despite criticism from some systematically minded biologists, I reaffirm that convergence in taxa occupying similar selective environments often is the result of natural selection. However, convergent evolution of a trait in a particular environment can occur for reasons other than selection on that trait in that environment, and species can respond to similar selective pressures by evolving nonconvergent adaptations. For these reasons, studies of convergence should be coupled with other methods-such as direct measurements of selection or investigations of the functional correlates of trait evolution-to test hypotheses of adaptation. The independent acquisition of similar phenotypes by the same genetic or developmental pathway has been suggested as evidence of constraints on adaptation, a view widely repeated as genomic studies have documented phenotypic convergence resulting from change in the same genes, sometimes even by the same mutation. Contrary to some claims, convergence by changes in the same genes is not necessarily evidence of constraint, but rather suggests hypotheses that can test the relative roles of constraint and selection in directing phenotypic evolution. © 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.
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              The genetic causes of convergent evolution.

              The evolution of phenotypic similarities between species, known as convergence, illustrates that populations can respond predictably to ecological challenges. Convergence often results from similar genetic changes, which can emerge in two ways: the evolution of similar or identical mutations in independent lineages, which is termed parallel evolution; and the evolution in independent lineages of alleles that are shared among populations, which I call collateral genetic evolution. Evidence for parallel and collateral evolution has been found in many taxa, and an emerging hypothesis is that they result from the fact that mutations in some genetic targets minimize pleiotropic effects while simultaneously maximizing adaptation. If this proves correct, then the molecular changes underlying adaptation might be more predictable than has been appreciated previously.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                14 July 2020
                25 June 2020
                25 June 2020
                : 117
                : 28
                : 16424-16430
                Affiliations
                [1] aDivision of Biology, Kansas State University , Manhattan, KS 66506;
                [2] bDepartment of Integrative Biology, Oklahoma State University , Stillwater, OK 74078;
                [3] cSchool of Biological Sciences, Washington State University , Pullman, WA 99163;
                [4] dDivisión Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco , Villahermosa, Tabasco, 86150, Mexico;
                [5] eInstituto de Investigaciones Botánicas y Zoológicas, Universidad Autónoma de Santo Domingo , Santo Domingo, 10105, Dominican Republic;
                [6] fMedical Research Council - Mitochondrial Biology Unit, University of Cambridge , Cambridge, CB2 0XY, United Kingdom;
                [7] gDepartment of Biosciences, University of Oslo , 0315 Oslo, Norway;
                [8] hDepartment of Nutritional Sciences, Oklahoma State University , Stillwater, OK 74078
                Author notes
                2To whom correspondence may be addressed. Email: tobler@ 123456ksu.edu , joanna.l.kelley@ 123456wsu.edu , or jennifer.shaw@ 123456pcom.edu .

                Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved May 21, 2020 (received for review March 9, 2020)

                Author contributions: R.G., N.B., C.H., M.T., J.L.K., and J.H.S. designed research; R.G., N.B., 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. contributed new reagents/analytic tools; R.G., N.B., C.H., A.P.B., M.T., J.L.K., and J.H.S. analyzed data; and R.G., N.B., M.T., and J.L.K. wrote the paper.

                1R.G., N.B., and C.H. contributed equally to this work.

                3Present address: Department of Biomedical Sciences, PCOM South Georgia, Moultrie, GA 31768.

                Author information
                https://orcid.org/0000-0002-7182-7932
                https://orcid.org/0000-0003-4641-3647
                https://orcid.org/0000-0002-7610-1380
                https://orcid.org/0000-0001-6100-2470
                https://orcid.org/0000-0002-8025-5569
                https://orcid.org/0000-0003-0472-1350
                https://orcid.org/0000-0002-7441-8210
                https://orcid.org/0000-0002-0326-0890
                https://orcid.org/0000-0002-7731-605X
                https://orcid.org/0000-0003-0670-9291
                Article
                202004223
                10.1073/pnas.2004223117
                7368198
                32586956
                c3122b12-0eee-4efe-92c9-812d99afb678
                Copyright © 2020 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 7
                Funding
                Funded by: NSF | BIO | Division of Integrative Organismal Systems (IOS) 100000154
                Award ID: IOS-1463720
                Award Recipient : Joanna L Kelley Award Recipient : Michael Tobler
                Funded by: NSF | BIO | Division of Integrative Organismal Systems (IOS) 100000154
                Award ID: IOS-1557795
                Award Recipient : Joanna L Kelley Award Recipient : Michael Tobler
                Funded by: NSF | BIO | Division of Integrative Organismal Systems (IOS) 100000154
                Award ID: IOS-1557860
                Award Recipient : Joanna L Kelley Award Recipient : Michael Tobler
                Funded by: NSF | BIO | Division of Integrative Organismal Systems (IOS) 100000154
                Award ID: IOS-1931657
                Award Recipient : Joanna L Kelley Award Recipient : Michael Tobler
                Funded by: DOD | United States Army | RDECOM | Army Research Office (ARO) 100000183
                Award ID: W911NF-15-1-0175
                Award Recipient : Joanna L Kelley Award Recipient : Michael Tobler
                Funded by: DOD | United States Army | RDECOM | Army Research Office (ARO) 100000183
                Award ID: W911NF-16-1-0225
                Award Recipient : Joanna L Kelley Award Recipient : Michael Tobler
                Funded by: RCUK | Medical Research Council (MRC) 501100000265
                Award ID: MC_U105663142
                Award Recipient : Michael P. Murphy
                Funded by: Wellcome Trust
                Award ID: 110159/Z/15/Z
                Award Recipient : Michael P. Murphy
                Categories
                Biological Sciences
                Evolution

                adaptive evolution,comparative physiology,ecological genomics,hydrogen sulfide,phylogenetic comparative analysis

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