Genome editing retraces the evolution of toxin resistance in the monarch butterfly

Karageorgi, Marianthi; Groen, Simon C.; Sumbul, Fidan; Peláez, Julianne; Verster, Kirsten I.; Aguilar, Jessica M; Hastings, Amy P.; Bernstein, Susan L.; Matsunaga, Teruyuki; Astourian, Michael; Guerra, Geno; Rico, Félix; Dobler, Susanne; Agrawal, Anurag A.; Whiteman, Noah K.

doi:10.1038/s41586-019-1610-8

Cited by 148 publications

(201 citation statements)

References 51 publications

(77 reference statements)

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“…The influence of chance is likely to depend on the particular function that is evolving: more determinism is expected for functions with very narrow sequence-structure-function-constraints (e.g. 13,15,25,[45][46][47] ), than those for which sequence requirements are less strict (e.g. 19,23,48,49 ).…”

Section: Discussionmentioning

confidence: 99%

Contingency and chance erase necessity in the experimental evolution of ancestral proteins

Xie

Metzger

et al. 2020

Preprint

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The extent to which evolutionary outcomes reflect the unpredictable influences of chance and contingency is a central but unanswered question in evolutionary biology 1–4. A precise characterization requires evolutionary trajectories to be repeated multiple times under identical environmental conditions from multiple starting points across history, a scenario that rarely, if ever, occurs in nature. Here we combine continuous experimental evolution 5 with ancestral protein reconstruction 6 and manipulative genetic experiments to identify the causes and consequences of chance and contingency in the genetic outcomes of molecular evolution. By repeatedly evolving ancestral proteins in the B-cell lymphoma-2 (BCL-2) family of apoptosis regulators 7 to acquire the same protein-protein interaction specificities that evolved during history, we found that contingency and chance interact to make sequence evolution increasingly unpredictable over phylogenetic timescales. Although replicates from the same starting genotype sometimes share mutations – indicating partial predictability – there are multiple alternative sets of changes that can alter specificity, and chance decides which of these paths is taken. Contingency has a stronger effect: when trajectories are initiated from different starting points, outcomes are even more divergent, because substitutions that occurred during phylogenetic history repeatedly changed the potential of other mutations to confer new binding specificities. The impact of contingency increased steadily with phylogenetic distance and magnified the effects of chance, resulting in a >3-fold increase in genetic variance among evolutionary trajectories initiated from different starting points across the timescale of metazoan evolution. Our findings show how a particular cascade of chance evolutionary steps throughout history makes the outcomes of molecular evolution increasingly idiosyncratic and unpredictable, even under strong selection.

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Section: Discussionmentioning

confidence: 99%

Contingency and chance erase necessity in the experimental evolution of ancestral proteins

Xie

Metzger

et al. 2020

Preprint

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“…The origin of land plants over 400 million years ago presented a new niche for insects (1) , ultimately producing the most diverse assemblages of animal life ever to have evolved (2,3) . Herbivory explains ~25% or more of the variation in diversification rates and species richness across insect orders (4,5) , and has resulted in convergent evolution across many levels of biological organization, from morphology and behavior to genes (6) and even single amino acids (7)(8)(9) .…”

Section: Introductionmentioning

confidence: 99%

Evolution of herbivory remodels aDrosophilagenome

Gloss

Dittrich

Lapoint

et al. 2019

Preprint

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SIGNIFICANCE STATEMENTThe origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly ( Drosophila melanogaste r), the "wasabi fly" ( Scaptomyza flava ), that evolved to consume mustard plants including Arabidopsis thaliana . The yeast-to-mustard dietary transition remodeled the fly's gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals. Gloss et al. 2019 1ABSTRACT One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, including Arabidopsis thaliana ) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila . We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species, S. flava, revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains ("blooms") were found in Phase I and Phase II detoxification gene sub-families, including glutathione S-transferase ( Gst ) and cytochrome P450 ( Cyp450 ) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1 ) and Gst (N=5 for GstE5-8 ) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in vitro . One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms, Drosophila and Arabidopsis , helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.

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“…This might be possible to do in some cases where the phenotype to fitness mapping is simple (e.g. antibiotic resistance driven by a specific enzyme or tRNA or protein folding mediating specific RNA or protein function) (Baeza-Centurion et al, 2019;Cowperthwaite et al, 2005;Diss and Lehner, 2018;Domingo et al, 2019;Harmand et al, 2017;Karageorgi et al, 2019;Li and Zhang, 2018;Otwinowski et al, 2018;Pressman et al, 2019;Sarkisyan et al, 2016;Starr et al, 2018;Weinreich, 2006) but is exceptionally difficult for complex phenotypes.…”

Section: Introductionmentioning

confidence: 99%

A genotype-phenotype-fitness map reveals local modularity and global pleiotropy of adaptation

Kinsler

Geiler-Samerotte

Petrov

2020

Preprint

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SUMMARYBuilding a genotype-phenotype-fitness map of adaptation is a central goal in evolutionary biology. It is notoriously difficult even when the adaptive mutations are known because it is hard to enumerate which phenotypes make these mutations adaptive. We address this problem by first quantifying how the fitness of hundreds of adaptive yeast mutants responds to subtle environmental shifts and then modeling the number of phenotypes they must collectively influence by decomposing these patterns of fitness variation. We find that a small number of phenotypes predicts fitness of the adaptive mutations near their original glucose-limited evolution condition. Importantly, phenotypes that matter little to fitness at or near the evolution condition can matter strongly in distant environments. This suggests that adaptive mutations are locally modular—affecting a small number of phenotypes that matter to fitness in the environment where they evolved—yet globally pleiotropic—affecting additional phenotypes that may reduce or improve fitness in new environments.

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Genome editing retraces the evolution of toxin resistance in the monarch butterfly

Cited by 148 publications

References 51 publications

Contingency and chance erase necessity in the experimental evolution of ancestral proteins

Contingency and chance erase necessity in the experimental evolution of ancestral proteins

Evolution of herbivory remodels aDrosophilagenome

A genotype-phenotype-fitness map reveals local modularity and global pleiotropy of adaptation

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