Experimental evolution

The outcome of selection for high and low oil content in the Illinois corn experiment.

William Dallinger Selected for thermotolerance of microorganisms 60 F  158 F

How experimental evolution works Batch (serial) culture Chemostat Turbidostat Static culture (liquid or solid)

Chemostat

Chemostats select for nutrient affinity

Static culture

What are the key variables? (brainstorm) Population size (N), and effective population size (Ne) Mutation rate Recombination? Parasites? Constant or fluctuating environment? Mass-action or structured environment?

Some questions addressed by experimental evolution What is the tempo and mode of evolution? (gradual or punctuated, limits, etc?) What factors promote or constrain adaptation? What are the consequences of adaptation? What are the mechanisms of adaptation? Is the mutation rate optimal or minimal? How do mutations interact?

Is evolution repeatable? “I call this experiment ‘replaying life’s tape.’ You press the rewind button and, making sure you thoroughly erase everything that actually happened, go back to any time and place in the past – say to the seas of the Burgess Shale. Then let the tape run again and see if the repetition looks at all like the original.” “The bad news is that we cannot possibly perform the experiment…” -S.J. Gould, Wonderful Life: the Burgess Shale and the nature of history (1989)

We CAN replay evolution Replicate populations evolving under identical conditions address whether evolution is repeatable. Do you predict phenotypic repeatability (parallelism)? Do you predict genetic repeatability?

Some more questions Why has sex evolved? Why do we age? How does virulence evolve? How does cooperation (or cheating) evolve? How does speciation begin? Is evolution Wrightian (many different outcomes) or Fisherian (one universal solution)? How do competitors coexist?

The most conspicuous evidence of evolution by natural selection is the fit of organisms to their environment. Yet quantifying adaptation continues to elude biologists.

Adaptation may be quantified directly Evolved Ancestor Day 0Day 1 Plate on agar to determine the ratio of 1 : 2 Determine 1 : 2 Fitness = Ln [ N 1 (Day 1) / N1 (Day 0) ] Ln [ N 2 (Day 1) / N2 (Day 0) ]

Generation Generation 20,000+  Experimental Conditions 12 replicate cultures single genotype of Escherichia coli B daily serial transfer single resource and temperature no sex + -

Mutation rate itself evolves in certain populations Non-mutator Mutator Population Sniegowski et al., Nature 387, (1997) Generations

“Part of the folk wisdom of evolutionary biology is that specialization leads to adaptive decay for environments outside the domain of specialization.” -R.D. Holt, Evol. Ecol. (1996)

Q1:Is the “folk wisdom” true?  Does specialization lead to adaptive decay? (Can we find such an association?)  Specialization: adaptation by an organism to a subset of its original environment  Adaptive decay: decay in niche breadth that is associated with adaptation

Why is this association so elusive? To determine if specialization leads to adaptive decay, we need to: quantify adaptation know the history of adaptation Both have proven challenging in most natural and experimental systems.

Is adaptation associated with loss of function? ?

Important environmental factors 37° CGlucose

Time (Generations) Fitness    I used Biolog plates to measure diet breadth

What are the consequences of adaptation?

Hypothetical curves describing loss of function: Total Catabolic Function Time (Generations)

Parallel and convergent changes across lineages are hallmarks of adaptive evolution ? evolved ancestors

Is the pattern consistent with AP?

Diet breadth decays over time 0 2,000 10,000 20,000 Time (Generations) Total Catabolic Function Red = mutators White = non-mutators Cooper and Lenski (2000) Nature 407:

Specialization in diet breadth was caused mostly by antagonistic pleiotropy Antagonistic pleiotropy: –Most losses of catabolic function occurred in replicate populations (parallelism) and when adaptation was most rapid (early in the experiment). Mutation accumulation: –Mutator populations tend to lose more catabolic functionality… –…but this additional loss is not proportional to the increase in mutation rate.

V max Generation time Evolution of thermal niche Temperature (  C) Cooper, Bennett, and Lenski. (2001) Evolution 55(5):

Adaptation to moderate temperatures leads to reduced performance at extreme temperatures Time (Generations) Relative V max Cooper, Bennett, and Lenski. (2001) Evolution 55(5):

Case study: What explains the rapid loss of D-ribose catabolism? Time (Generations) Frequency Rbs  Cooper, V. S., D. Schneider, M. Blot, and R. E. Lenski. (2001) J. Bact. 183: 2834–2841.

Ribose function is hypermutable Mutation rate for ribose loss = 5.4 X per generation. 2-5 orders of magnitude higher than mutation rates measured for other traits. Time required to reach a frequency of 50% under mutation pressure alone = 18,519 generations.

1 kb IS150 G5 G6 G76 Hinc II rbsDrbsArbsCrbsBrbsKrbsRyieO left IS150 adjacent sequence right IS150 adjacent sequence G77 Extent of the deletion Ara-1 Hyb. (bp) PCR (bp) 2,8122,071 Ara-2 3,0432,302 Ara-3 3,8547,373 Ara-4 3,3382,597 Ara-5 2,4833,378 Ara-6 3,0342,293 Ara+1 1,9722,867 Ara+3 3,3322,591 Ara+4 4,1635,058 Ara+5 2,9993,894 Ara+6 3,3292,588 2,6629,005 Ancestor Hinc II A. B. G269 G268 G266 G267 Cooper, V. S., D. Schneider, M. Blot, and R. E. Lenski. (2001) J. Bact. 183: 2834–2841.

Rbs - mutation alone improves fitness Independent Rbs - mutants of ancestor Fitness

What accounts for the rapid loss of ribose catabolism? Time to 50% of population MA alone = 18,519 generations Selection = 1,774 generations Selection plus MA = 781 generations Genetic hitchhiking = priceless (< 500 generations)

Loss of succinate, fumarate, malate function suite of functions compromised in part by IS insertion in pykF different pykF mutations found in other populations; same reversibility? suggests selection to regain succinate function and study of evolution of phenotypic plasticity

Summary Is specialization caused more by AP or MA? –Antagonistic pleiotropy explains the majority of change in diet breadth and thermal range. –Mutation accumulation is only detectable among mutator populations; may require more time? Should adaptive decay be “folk wisdom?” –Most functions were retained. –Selection in permissive environments may yield a greater frequency of specialists. –The mechanisms responsible for loss of function cannot be assumed.