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

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 (H2S)-a toxicant that impairs mitochondrial function-across evolutionarily independent lineages of a fish (Poecilia mexicana, Poeciliidae) from H2S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H2S 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 H2S tolerance in different populations is likely caused by a combination of selection on standing genetic variation and de novo mutations. On a macroevolutionary scale, H2S 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 H2S 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 H2S adaptation in lineages that span 40 million years of evolution

Comparative physiology and the predictability of evolution in extreme environments

Doctor of PhilosophyDivision of BiologyMichael ToblerThe physiological mechanisms underlying adaptation, and how physiological differences observed in natural populations relate to underlying genetic variation, remain largely unknown for many natural systems. My dissertation seeks to close these gaps in knowledge by addressing three major questions: 1) How does variation across levels of biological organization integrate to explain divergence in organismal phenotypes? 2) Are patterns of physiological adaptation predictable across populations experiencing similar sources of selection? 3) What are the evolutionary origins of physiological traits facilitating adaptation to novel environmental conditions? Organisms inhabiting extreme environments are ideal systems to investigate questions about the mechanisms underlying adaptation and the predictability of evolution at molecular scales. These habitats are characterized by harsh physiochemical stressors that often target specific biochemical and physiological pathways, allowing for hypothesis-driven tests of the effects of the stressor on organismal function and trait evolution. Additionally, powerful comparisons can be made between closely related lineages inhabiting extreme and ancestral habitats, which allows for investigations into the predictability of evolution in response to similar sources of selection. In my research, I leveraged a unique study system of fishes that have independently colonized extreme aquatic habitats rich in hydrogen sulfide (H₂S), a naturally occurring toxin that is known to interfere with oxygen transport and mitochondrial function address four objectives: 1) I determined the predictability and repeatability of molecular evolution and changes in gene expression of oxygen transport genes in ten lineages of sulfide-tolerant fishes, 2) I assessed the convergence in biochemical, physiological, and organismal function in pathways exhibiting evidence of molecular evolution and gene expression variation, 3) I measured the functional consequences of genetic variation on the metabolic function of enzymes, mitochondria, and whole organisms to identify the predictability of metabolic evolution across levels of organization and between sulfide-tolerant and -intolerant lineages of fish, and 4) I identified potential adaptive plasticity in gene expression in ancestral freshwater species that may represent pre-adaptations for the colonization of H₂S-rich springs. Through the integration of genomic, biochemical, and organismal data, I found that (1) oxygen transport genes are predictable targets of natural selection in sulfide spring fishes, but the modifications in gene expression and sequence variation were not repeatable across groups, (2) both H₂S detoxification and oxidative phosphorylation are predictable targets of natural selection in H₂S-rich environments, and modification of these integral pathways results in functional differences at the biochemical, physiological, and organismal levels, (3) the degree to which metabolic physiology varies between sulfide-tolerant and -intolerant fish differs depending on the level of organization observed, suggesting that researchers must be cautious when making inferences about function solely from genetic data, and (4) genes exhibiting adaptive plasticity in H₂S detoxification, metabolic pathways, and oxygen sensing may have been pre-adaptations that facilitated colonization of sulfide-rich springs. The research detailed in this dissertation has important implications for how scientists perceive the predictability of both evolution and phenotype, highlighting the role environmental and physiological constraints play in our ability to predict the outcomes of natural variation across habitats and within organisms

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

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 ten lineages of fish of the family Poeciliidae that have colonized freshwater springs rich in H2S â along with related lineages from non-sulfidic environments â 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.The accepted manuscript in pdf format is listed with the files at the bottom of this page. The presentation of the authors' names and (or) special characters in the title of the manuscript may differ slightly between what is listed on this page and what is listed in the pdf file of the accepted manuscript; that in the pdf file of the accepted manuscript is what was submitted by the author

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

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 (H2S)-a toxicant that impairs mitochondrial function-across evolutionarily independent lineages of a fish (Poecilia mexicana, Poeciliidae) from H2S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H2S 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 H2S tolerance in different populations is likely caused by a combination of selection on standing genetic variation and de novo mutations. On a macroevolutionary scale, H2S 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 H2S 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 H2S adaptation in lineages that span 40 million years of evolution

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

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 2 S)—a toxicant that impairs mitochondrial function—across evolutionarily independent lineages of a fish ( Poecilia mexicana , Poeciliidae) from H 2 S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H 2 S 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 2 S 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 2 S 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 2 S 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 2 S adaptation in lineages that span 40 million years of evolution

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

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 (H2S)-a toxicant that impairs mitochondrial function-across evolutionarily independent lineages of a fish (Poecilia mexicana, Poeciliidae) from H2S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H2S 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 H2S tolerance in different populations is likely caused by a combination of selection on standing genetic variation and de novo mutations. On a macroevolutionary scale, H2S 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 H2S 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 H2S adaptation in lineages that span 40 million years of evolution