Stochastic Temperatures Impede Rna Virus Adaptation

Alto, Barry W.; Wasik, Brian R.; Morales, Nadya M.; Turner, Paul

doi:10.1111/evo.12034

Cited by 47 publications

(80 citation statements)

References 45 publications

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“…Such observations are not limited to E. coli, because studies of the vesicular stomatitis virus also suggest that fitness tradeoffs are not universal across thermal gradients (18).…”

Section: Significancementioning

confidence: 99%

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Different tradeoffs result from alternate genetic adaptations to a common environment

Rodríguez‐Verdugo

Carrillo-Cisneros

González-González

et al. 2014

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

122

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Fitness tradeoffs are often assumed by evolutionary theory, yet little is known about the frequency of fitness tradeoffs during stress adaptation. Even less is known about the genetic factors that confer these tradeoffs and whether alternative adaptive mutations yield contrasting tradeoff dynamics. We addressed these issues using 114 clones of Escherichia coli that were evolved independently for 2,000 generations under thermal stress (42.2°C). For each clone, we measured their fitness relative to the ancestral clone at 37°C and 20°C. Tradeoffs were common at 37°C but more prevalent at 20°C, where 56% of clones were outperformed by the ancestor. We also characterized the upper and lower thermal boundaries of each clone. All clones shifted their upper boundary to at least 45°C; roughly half increased their lower niche boundary concomitantly, representing a shift of thermal niche. The remaining clones expanded their thermal niche by increasing their upper limit without a commensurate increase of lower limit. We associated these niche dynamics with genotypes and confirmed associations by engineering single mutations in the rpoB gene, which encodes the beta subunit of RNA polymerase, and the rho gene, which encodes a termination factor. Single mutations in the rpoB gene exhibit antagonistic pleiotropy, with fitness tradeoffs at 18°C and fitness benefits at 42.2°C. In contrast, a mutation within the rho transcriptional terminator, which defines an alternative adaptive pathway from that of rpoB, had no demonstrable effect on fitness at 18°C. This study suggests that two different genetic pathways toward high-temperature adaptation have contrasting effects with respect to thermal tradeoffs.RNA polymerase | Rho factor | genotype-phenotype associations | experimental evolution D espite the centrality of adaptation to evolution, surprisingly little is known about the diversity of mutations that contribute to adaptation or about their phenotypic and fitness effects (1). There are, in fact, only a few well-known examples linking genotype, phenotype, and adaptation in nature (2-4). In nature, this connection is often complicated by factors such as varying selection pressures or underlying genetic heterogeneities. Although the task is difficult, the general inability to connect phenotype to genotype in the context of environmental adaptation has been a major failing in the field of evolution (5).Experimental evolution provides a more tractable approach to study relationships among fitness, genotype, and phenotype (5, 6). Here we explore these relationships based on our recent, large-scale evolutionary experiment (7). The experiment began with an ancestral strain of Escherichia coli B that was inoculated into ∼115 independent replicates. Each replicate was grown at high temperature (42.2°C) for 2,000 generations. At the end of the experiment, fitness was measured at 42.2°C for a single clone from each of 114 lineages; on average, fitness increased ∼40% during the yearlong experiment.We sequenced the genome of these 114 clones, ...

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“…Such observations are not limited to E. coli, because studies of the vesicular stomatitis virus also suggest that fitness tradeoffs are not universal across thermal gradients (18).…”

Section: Significancementioning

confidence: 99%

“…Tradeoffs have been examined previously in the context of experimental evolution, particularly tradeoffs with respect to thermal niche (15)(16)(17)(18). Thermal niche has been a focus because temperature is a fundamental environmental property that affects physiological traits and often defines species' distributions (19,20).…”

mentioning

confidence: 99%

Different tradeoffs result from alternate genetic adaptations to a common environment

Rodríguez‐Verdugo

Carrillo-Cisneros

González-González

et al. 2014

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

122

View full text Add to dashboard Cite

show abstract

“…Mixed linear models were used to assess the effects of fixed effect of selection treatment and random effects of population and block on viral fitness (package 'nlme', R 2014) [16]. When significant selection treatment effects were found, specific hypotheses were tested using pairwise contrasts of means and corrected for multiple comparisons using the sequential Bonferroni method (package 'multcomp', R 2015).…”

Section: (F ) Statistical Analysismentioning

confidence: 99%

Rate of novel host invasion affects adaptability of evolving RNA virus lineages

Morley¹,

Mendiola²,

Turner³

2015

Proc. R. Soc. B.

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Although differing rates of environmental turnover should be consequential for the dynamics of adaptive change, this idea has been rarely examined outside of theory. In particular, the importance of RNA viruses in disease emergence warrants experiments testing how differing rates of novel host invasion may impact the ability of viruses to adaptively shift onto a novel host. To test whether the rate of environmental turnover influences adaptation, we experimentally evolved 144 Sindbis virus lineages in replicated tissue-culture environments, which transitioned from being dominated by a permissive host cell type to a novel host cell type. The rate at which the novel host 'invaded' the environment varied by treatment. The fitness (growth rate) of evolved virus populations was measured on each host type, and molecular substitutions were mapped via whole genome consensus sequencing. Results showed that virus populations more consistently reached high fitness levels on the novel host when the novel host 'invaded' the environment more gradually, and gradual invasion resulted in less variable genomic outcomes. Moreover, virus populations that experienced a rapid shift onto the novel host converged upon different genotypes than populations that experienced a gradual shift onto the novel host, suggesting a strong effect of historical contingency.

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“…Nevertheless, many types of abiotic perturbations can cause viral mortality, i.e., the inability of a viral particle to successfully complete within-host replication after experiencing an environmental challenge (56). A wide variety of environmental stressors are known to somehow compromise a virus's subsequent ability to productively infect a host; examples include changes in ambient temperature, ionic strength (saltiness), UV radiation, acidity, atmospheric pressure, and moisture (2,49,56,58). Although capsids function to protect viral nucleic acid from degradation by these and other environmental stressors, the protection is not absolute, and some viruses may experience very short half-lives outside of the host under these harsh conditions.…”

Section: Biotic and Abiotic Challenges Faced By Virusesmentioning

confidence: 99%

“…These radical widespread changes would be experienced by viruses, just as they would by other biological populations. However, only a few studies have examined the effects on viral mortality of abiotic challenges associated with proposed ecosystem changes, such as increased acidity of marine water (48) or stochastic temperature fluctuations predicted by some climate change models (2). More research is needed to identify how the survival of viruses may be compromised under radical ecosystem changes.…”

Section: Biotic and Abiotic Challenges Faced By Virusesmentioning

confidence: 99%

On the Biological Success of Viruses

Wasik

Turner

2013

Annu. Rev. Microbiol.

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Are viruses more biologically successful than cellular life? Here we examine many ways of gauging biological success, including numerical abundance, environmental tolerance, type biodiversity, reproductive potential, and widespread impact on other organisms. We especially focus on successful ability to evolutionarily adapt in the face of environmental change. Viruses are often challenged by dynamic environments, such as host immune function and evolved resistance as well as abiotic fluctuations in temperature, moisture, and other stressors that reduce virion stability. Despite these challenges, our experimental evolution studies show that viruses can often readily adapt, and novel virus emergence in humans and other hosts is increasingly problematic. We additionally consider whether viruses are advantaged in evolvability-the capacity to evolve-and in avoidance of extinction. On the basis of these different ways of gauging biological success, we conclude that viruses are the most successful inhabitants of the biosphere.

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Stochastic Temperatures Impede Rna Virus Adaptation

Cited by 47 publications

References 45 publications

Different tradeoffs result from alternate genetic adaptations to a common environment

Different tradeoffs result from alternate genetic adaptations to a common environment

Rate of novel host invasion affects adaptability of evolving RNA virus lineages

On the Biological Success of Viruses

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