Different Trajectories of Parallel Evolution During Viral Adaptation

Wichman, Holly A.; Badgett, M. R.; Scott, LuAnn; Boulianne, C. M.; Bull, J. J.

doi:10.1126/science.285.5426.422

Cited by 332 publications

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“…In the first of these studies, Bull et al (1997) found that 25-50% of substitutions were parallel among five exper-1 imental lines of fX174 selected for growth on two different hosts. Similarly, Wichman et al (1999) observed $50% parallel evolution in two independent lines of the same phage selected for high-temperature growth. A similar study in which two related phages were evolved on two different hosts also found a large degree of parallel evolution within species but little between species .…”

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confidence: 92%

“…Our system allows strict control over the selective environment, repeated adaptation, and the ability to determine all of the underlying genetic changes in the genome. Previous experimental evolution studies of the genetics of adaptation that addressed parallel evolution found a high incidence of convergent genetic changes in independent experimental microbial lineages (Bull et al 1997Wichman et al 1999;Riehle et al 2001). In the first of these studies, Bull et al (1997) found that 25-50% of substitutions were parallel among five exper-1 imental lines of fX174 selected for growth on two different hosts.…”

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confidence: 97%

“…Similarly, it is of great interest to know whether the genetic changes underlying parallel traits are also parallel. With few exceptions (Andreev et al 1999;Wichman et al 1999;ffrench-Constant et al 2000;Sucena et al 2003;Wood et al 2005;Colosimo et al 2005;Sugawara et al 2005), little is understood about the underlying genetic nature of parallel phenotypes.…”

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confidence: 99%

“…In addition, they observed a significant degree of convergent evolution between the species, likely reflecting host-specific adaptations. Wichman et al (1999) also looked for a parallel evolution at a different level-parallelism in the order in which mutations appeared and in the order in which they were fixed-but failed to find an effect. Finally, in the third of these studies (Holder and Bull 2001), two closely related phage species, G4 and fX174, were adapted to growth at high temperature and assayed both for parallel substitutions and for order effects as in Wichman et al (1999).…”

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confidence: 99%

“…Wichman et al (1999) also looked for a parallel evolution at a different level-parallelism in the order in which mutations appeared and in the order in which they were fixed-but failed to find an effect. Finally, in the third of these studies (Holder and Bull 2001), two closely related phage species, G4 and fX174, were adapted to growth at high temperature and assayed both for parallel substitutions and for order effects as in Wichman et al (1999). In contrast to the findings within species, there was no parallel evolution between the species at the level of nucleotide substitutions, and perhaps most surprisingly there was little overlap even in the genes experiencing beneficial substitutions.…”

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confidence: 99%

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Parallel Genetic Evolution Within and Between Bacteriophage Species of Varying Degrees of Divergence

Bollback

Huelsenbeck

2009

Genetics

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Parallel evolution is the acquisition of identical adaptive traits in independently evolving populations. Understanding whether the genetic changes underlying adaptation to a common selective environment are parallel within and between species is interesting because it sheds light on the degree of evolutionary constraints. If parallel evolution is perfect, then the implication is that forces such as functional constraints, epistasis, and pleiotropy play an important role in shaping the outcomes of adaptive evolution. In addition, population genetic theory predicts that the probability of parallel evolution will decline with an increase in the number of adaptive solutions-if a single adaptive solution exists, then parallel evolution will be observed among highly divergent species. For this reason, it is predicted that close relatives-which likely overlap more in the details of their adaptive solutions-will show more parallel evolution. By adapting three related bacteriophage species to a novel environment we find (1) a high rate of parallel genetic evolution at orthologous nucleotide and amino acid residues within species, (2) parallel beneficial mutations do not occur in a common order in which they fix or appear in an evolving population, (3) low rates of parallel evolution and convergent evolution between species, and (4) the probability of parallel and convergent evolution between species is strongly effected by divergence.

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confidence: 92%

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confidence: 97%

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confidence: 99%

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Parallel Genetic Evolution Within and Between Bacteriophage Species of Varying Degrees of Divergence

Bollback

Huelsenbeck

2009

Genetics

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Microviridae: Microviruses and Gokushoviruses

Cherwa

Fane

2011

Encyclopedia of Life Sciences

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Members of the Microviridae comprise two subfamilies. The microviruses (Greek for small), which infect free‐living bacteria, are among the fastest known replicating viruses. Gokushoviruses (Japanese for very small) occupy a unique niche, infecting obligate intracellular bacteria, such as Chlamydia and Bdellovibrio , or mollicutes, bacteria without a cell wall. All members of the family contain small (4000–6000 bases), circular, single‐stranded deoxyribonucleic acid (ssDNA) genomes of positive polarity, which are packaged inside small (∼25 nm diameter) T=1 icosahedral capsids. The other icosahedral, ssDNA virus families: Parvoviridae , Circoviridae , Nanoviridae and Geminiviridae ; share most of these properties, suggesting a large super family spanning several domains of life. The most well known member of the Microviridae , ϕX174, has been extensively used to study the fundamental mechanisms of DNA replication and capsid assembly. The latter is uniquely dependent on two scaffolding proteins, and has become a model system for experimental evolution. Key Concepts: Whilst overlapping reading frames increase the amount of genetic information encoded in small genomes, they do not appear to significantly impact the ability of the virus to genetically adapt to selective pressures. Due to the genome's positive polarity, DNA replication must commence before viral genes can be transcribed. Microvirus DNA replication occurs in three distinct stages: (1) ssDNA is first converted to a double‐stranded molecule, (2) amplification of the double‐stranded molecule, (3) single‐stranded genomic DNA synthesis and packaging. Genomic DNA synthesis and packaging are concurrent processes; thus, a genome is not synthesised unless there exists a capsid in which to package it. Gene expression is controlled by the finely tuned interplay of cis ‐acting genetic elements: promoters, ribosome binding sites, mRNA stability sequences and transcription terminators. Microviruses are distinguished by their two scaffolding protein system, whereas Gokushoviruses utilise a single scaffolding protein. Capsid assembly is mediated by scaffolding proteins, which induce conformational switches in the viral coat protein to control the timing and fidelity of morphogenesis. Cell lysis is achieved by inhibiting host cell wall biosynthesis, a mechanism reminiscent of some antibiotics.

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Experimental Evolution in Viruses

Sanjuán

Domingo‐Calap

2011

Encyclopedia of Life Sciences

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Experiments in which evolution takes place in real time can help us establish cause–effect relationships that are difficult to infer from the analysis of natural populations. The simplicity, rapid evolution and biomedical relevance of viruses make them a particularly interesting model system for experimental evolution. Bacterial, animal and plant viruses can be passaged under a variety of conditions, either in simple cell culture systems or in vivo to test population biology hypotheses, study the genetic basis of evolution, or predict evolutionary change in nature. Experimental evolution is a conceptually simple and flexible tool which allows us to address issues ranging from the molecular to the ecosystem level. In addition to studying basic processes such as mutation, adaptation, or random genetic drift, viruses can be experimentally evolved to better understand the emergence of drug resistance, explore new antiviral strategies such as lethal mutagenesis, create better attenuated vaccines, or target cancerous cells. Key Concepts: Experimental evolution can be done with many different model organisms, but microorganisms and viruses offer a series of advantages including their easy manipulation, storability and biomedical relevance. The setup of an evolutionary experiment is conceptually simple and essentially consists of serially transferring viruses from flask to flask or, in vivo , from host to host. However, a careful experimental design is needed to be able to demonstrate which factors are responsible for the evolutionary changes observed in the laboratory. Molecular biology is a powerful tool in virus experimental evolution because it allows us to manipulate viral genomes and to study the molecular basis of evolution. Viruses can adapt to many different laboratory environments, but these adaptations often come at the cost of decreased performance in alternative environments, demonstrating the existence of certain limits to adaptation, or fitness tradeoffs. Viral experimental evolution has both stochastic and deterministic components. Therefore, although viral evolution is not easy to predict, it shows some regular patterns. The role played by population–genetic factors such as the population size or the mutation rate have been extensively studied in viruses, and several important generalisations have been established. Experimental evolution has inspired new strategies to combat viral disease, including the use of selective mutagens to damage viral genomes or the use of less evolvable strains to create more effective and safer vaccines.

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Different Trajectories of Parallel Evolution During Viral Adaptation

Cited by 332 publications

References 23 publications

Parallel Genetic Evolution Within and Between Bacteriophage Species of Varying Degrees of Divergence

Parallel Genetic Evolution Within and Between Bacteriophage Species of Varying Degrees of Divergence

Microviridae: Microviruses and Gokushoviruses

Experimental Evolution in Viruses

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