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Evolution on empirical adaptive landscapes

Yoav Ram
April 06, 2017

Evolution on empirical adaptive landscapes

The increasing availability of empirical adaptive landscapes in microbes pro- vides an opportunity, for the rst time, to study evolutionary theory on real- istic adaptive landscapes. We demonstrate this new approach by simulating adaptive evolution of a haploid, asexual population on the A. nigeri and the E. coli TEM empirical landscapes. Our results demonstrate some interesting evolutionary phenomena. First, adaptation starts with a big leap forward, but additional tness increases become smaller and further apart. Second, in the smooth E. coli TEM landscape, every genotype along the evolutionary trajec- tory reached high frequency before the next genotype emerged and increased in frequency. In contrast, in the rugged A. niger landscape, only four genotypes reach a high frequency, although adaptation proceeds through seven di erent genotypes. These di erences have profound e ects on our ability to predict the trajectory and pace of adaptation. We consider this new approach critical for our understanding of many biological phenomena, from emergence of drug resistance to formation of microbial communities.

Yoav Ram

April 06, 2017
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  1. Evolution on empirical adaptive
    landscapes
    Yoav Ram
    Stanford University
    ISM, April 2017
    1

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

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

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

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

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  6. Empirical adaptive landscapes
    6

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

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

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  9. 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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  10. 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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  11. Example 1: E. coli TEM
    Single peak landscape
    Yoav Ram / ISM 2017 11

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  12. 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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  13. Example 2: Aspergillus niger
    Yoav Ram / ISM 2017 13

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  14. 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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  15. 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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  16. 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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  17. 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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  18. Simulating evolution
    Wright-Fisher model
    Yoav Ram / ISM 2017 18

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

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

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

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

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

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  24. 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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  25. 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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  26. 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

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