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Evolution on empirical adaptive landscapes Yoav Ram Stanford University ISM, April 2017 1

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Adaptive landscapes Sewall Wright, Genetics 1931 Yoav Ram / ISM 2017 2

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Adaptive landscapes Simple or Rugged? Yoav Ram / ISM 2017 3

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Evolution on adaptive landscapes Adaptive peak shifts Yoav Ram / ISM 2017 4

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Ecology of adaptive landscapes Speciation* * Gavrilets, Evolution 2003 Yoav Ram / ISM 2017 5

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Empirical adaptive landscapes 6

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Evolution of Citrate utilization in E. coli Blount et al., Nature 2012 Yoav Ram / ISM 2017 7

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Mt. Citrate Quandt et al, PNAS 2014 Kryazhimskiy & Desai, PNAS 2014 Yoav Ram / ISM 2017 8

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Empirical adaptive landscapes How to get them? • Evolutionary experiments • Phylogeny • Random mutagenesis de Visser & Krug, Nat Rev Gen 2014 Yoav Ram / ISM 2017 9

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Example 1: E. coli TEM • β-lactamase TEM gene in E. coli • 5 point mutations • Increase resistance to cefotaxime ~100,000-fold. Weinreich et al., Science 2006 Image: Wikipedia Yoav Ram / ISM 2017 10

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Example 1: E. coli TEM Single peak landscape Yoav Ram / ISM 2017 11

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Example 2: Aspergillus niger The black mould Fungus • 5 auxotrophic mutations • 2 resistance mutations • 1 spore color mutation. de Visser et al., Evolution 1997 Image: Wikipedia Yoav Ram / ISM 2017 12

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Example 2: Aspergillus niger Yoav Ram / ISM 2017 13

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Example 3: tRNA gene • 65,000 yeast mutants in the gene • Fitness ~ biophysical properties of tRNA molecule • 1% single point mutations are beneficial • 42% are deleterious C. Li et al., Science 2016 Yoav Ram / ISM 2017 14

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Example 4: E. coli lac system • lac operator mutants • Measured expression and repression ability de Vos et al., PNAS 2015 Yoav Ram / ISM 2017 15

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Example 4: E. coli lac system • Adaptation facilitated by environmental changes • Population can escapes local peaks de Vos et al., PNAS 2015 Yoav Ram / ISM 2017 16

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Combining experiments & theory Simulations on empirical landscapes Experiments: - genotype ➡ fitness mapping Simulations: - test hypotheses - make predictions Yoav Ram / ISM 2017 17

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Simulating evolution Wright-Fisher model Yoav Ram / ISM 2017 18

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Simulating evolution Wright-Fisher model • Natural selection: • Mutation: • Random genetic drift: Yoav Ram / ISM 2017 19

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Simulations on E. coli TEM landscape Obolski, Ram & Hadany, 2017 Yoav Ram / ISM 2017 20

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Simulations on A. niger landscapes Obolski, Ram & Hadany, 2017 Yoav Ram / ISM 2017 21

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Comparison: A. niger vs. E. coli TEM Obolski, Ram & Hadany, 2017 Yoav Ram / ISM 2017 22

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Comparison: A. niger vs. E. coli TEM Obolski, Ram & Hadany, 2017 Yoav Ram / ISM 2017 23

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Applications in Microbiology • Generate testable predictions • Use predictions to intervene in evolution: • drug & pesticide resistance • virulence • conservation • Study open questions in evolution Yoav Ram / ISM 2017 24

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What's next? • Experimental side • More organisms, bigger landscapes, precise measurements • Estimates of mutation rates, population sizes, environmental changes • Theoretical side • New methods & models for communities, host-symbiont interactions... Yoav Ram / ISM 2017 25

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Thank you! • Collaborators: • Lilach Hadany, Tel-Aviv University • Uri Obolski, Univ. of Oxford • Preprint: Obolski, Ram & Hadany, bioRxiv 2017. doi: 10.1101/112177 • Source code: github.com/yoavram/ISM2017 • Homepage: www.yoavram.com • Funding: Yoav Ram / ISM 2017 26