Repeatability and Contingency in the Evolution of a Key Innovation in Phage Lambda

Meyer, Justin R.; Dobias, Devin T.; Weitz, Joshua S.; Barrick, Jeffrey E.; Quick, Ryan T.; Lenski, Richard E.

doi:10.1126/science.1214449

Cited by 436 publications

(638 citation statements)

References 63 publications

(57 reference statements)

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“…The improved growth rate likely occurs before the reduced resistance range due to the greater competitive advantage conferred by the former. However, it is also feasible that the first mutation primes the cell for the second mutation, as was found for evolution of phage lambda (59). Unfortunately, the lack of a genetic system for Prochlorococcus prevents us from introducing the different mutations in a controlled manner to test this latter hypothesis.…”

Section: Discussionmentioning

confidence: 99%

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Avrani

Lindell

2015

Proc. Natl. Acad. Sci. U.S.A.

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Prochlorococcus is an abundant marine cyanobacterium that grows rapidly in the environment and contributes significantly to global primary production. This cyanobacterium coexists with many cyanophages in the oceans, likely aided by resistance to numerous co-occurring phages. Spontaneous resistance occurs frequently in Prochlorococcus and is often accompanied by a pleiotropic fitness cost manifested as either a reduced growth rate or enhanced infection by other phages. Here, we assessed the fate of a number of phage-resistant Prochlorococcus strains, focusing on those with a high fitness cost. We found that phage-resistant strains continued evolving toward an improved growth rate and a narrower resistance range, resulting in lineages with phenotypes intermediate between those of ancestral susceptible wild-type and initial resistant substrains. Changes in growth rate and resistance range often occurred in independent events, leading to a decoupling of the selection pressures acting on these phenotypes. These changes were largely the result of additional, compensatory mutations in noncore genes located in genomic islands, although genetic reversions were also observed. Additionally, a mutator strain was identified. The similarity of the evolutionary pathway followed by multiple independent resistant cultures and clones suggests they undergo a predictable evolutionary pathway. This process serves to increase both genetic diversity and infection permutations in Prochlorococcus populations, further augmenting the complexity of the interaction network between Prochlorococcus and its phages in nature. Last, our findings provide an explanation for the apparent paradox of a multitude of resistant Prochlorococcus cells in nature that are growing close to their maximal intrinsic growth rates.cyanobacteria | cyanophage | resistance | Prochlorococcus | virus

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Section: Discussionmentioning

confidence: 99%

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Avrani

Lindell

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…In this regard sufficiently rich data can reveal macroevolutionary patterns through, for example, ancient DNA analysis [166]. At the other extreme, the recent explosion of experimental evolution [104,167,168] and ever-increasing sophistication in behavioural studies [18] have important roles to play in scientifically evaluating competing hypotheses-depending on the system-over time scales amenable to many research programmes. Mathematical and computational models will be central in evaluating candidate processes driving innovation, regardless of time scales.…”

Section: Resultsmentioning

confidence: 99%

Innovation: an emerging focus from cells to societies

Hochberg

Marquet

Boyd

et al. 2017

Phil. Trans. R. Soc. B

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Innovations are generally unexpected, often spectacular changes in phenotypes and ecological functions. The contributions to this theme issue are the latest conceptual, theoretical and experimental developments, addressing how ecology, environment, ontogeny and evolution are central to understanding the complexity of the processes underlying innovations. Here, we set the stage by introducing and defining key terms relating to innovation and discuss their relevance to biological, cultural and technological change. Discovering how the generation and transmission of novel biological information, environmental interactions and selective evolutionary processes contribute to innovation as an ecosystem will shed light on how the dominant features across life come to be, generalize to social, cultural and technological evolution, and have applications in the health sciences and sustainability. This article is part of the theme issue ‘Process and pattern in innovations from cells to societies’.

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“…Both of these classes have been shown to play important roles across a wide range of taxa, from vertebrates (1, 2) to bacteria (3, 4), and their relative importance has been the topic of considerable discussion (5-12). Significantly, many previous studies have addressed these questions by focusing on single instances of functional innovation (13-16) or selective regimes (17)(18)(19)(20)(21)(22). However, to identify general principles, it is necessary to study evolutionary innovation for a large number of different functions in parallel.…”

mentioning

confidence: 99%

The predictability of molecular evolution during functional innovation

Blank

Wolf

Ackermann

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Determining the molecular changes that give rise to functional innovations is a major unresolved problem in biology. The paucity of examples has served as a significant hindrance in furthering our understanding of this process. Here we used experimental evolution with the bacterium Escherichia coli to quantify the molecular changes underlying functional innovation in 68 independent instances ranging over 22 different metabolic functions. Using whole-genome sequencing, we show that the relative contribution of regulatory and structural mutations depends on the cellular context of the metabolic function. In addition, we find that regulatory mutations affect genes that act in pathways relevant to the novel function, whereas structural mutations affect genes that act in unrelated pathways. Finally, we use population genetic modeling to show that the relative contributions of regulatory and structural mutations during functional innovation may be affected by population size. These results provide a predictive framework for the molecular basis of evolutionary innovation, which is essential for anticipating future evolutionary trajectories in the face of rapid environmental change.adaptation | transcription | compensatory mutation | biosynthesis O ne of the most important questions in evolutionary biology concerns the molecular mechanisms that underlie functional innovations. These changes are often polarized into two classes: those that affect protein structure and those that affect protein expression level. Both of these classes have been shown to play important roles across a wide range of taxa, from vertebrates (1, 2) to bacteria (3, 4), and their relative importance has been the topic of considerable discussion (5-12). Significantly, many previous studies have addressed these questions by focusing on single instances of functional innovation (13-16) or selective regimes (17)(18)(19)(20)(21)(22). However, to identify general principles, it is necessary to study evolutionary innovation for a large number of different functions in parallel. Indeed, the fact that only a small number of examples exist has resulted in few hypotheses being put forth that identify general characteristics of the molecular changes underlying functional innovation. One prominent hypothesis states that if the development of a novel trait is spatially or temporally limited, then innovation frequently occurs through changes in regulation (23,24). Whether there are general patterns beyond this is not well-established.Here we used an experimental system that allows the analysis of a large number of independent cases of evolutionary innovation and investigation of the underlying genetic changes. We worked with a collection of 87 strains of Escherichia coli that each had a deletion of one gene encoding a different metabolic function (SI Appendix, Table S1). Each of these deletions resulted in an inability to grow in minimal glucose media. Then, for each of these 87 deleted metabolic functions, we used experimental evolution to select for novel func...

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Repeatability and Contingency in the Evolution of a Key Innovation in Phage Lambda

Cited by 436 publications

References 63 publications

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Innovation: an emerging focus from cells to societies

The predictability of molecular evolution during functional innovation

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