Surviving the Bottleneck: Transmission Mutants and the Evolution of Microbial Populations

Handel, Andreas; Bennett, Matthew R.

doi:10.1534/genetics.108.093013

Cited by 32 publications

(44 citation statements)

References 53 publications

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“…Within an infected host, efficient replication and immune evasion are central. At the population level, efficient transmission between hosts, potentially with good environmental persistence as an intermediate stage, is a critical component of overall pathogen fitness [22][23][24][25][26]. It is plausible, then, that different constraints act at different parts of this cycle and that potential conflicts between optimizing fitness for one component versus another may lead to trade-offs.…”

Section: Introductionmentioning

confidence: 99%

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

et al. 2014

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Trade-offs between different components of a pathogen's replication and transmission cycle are thought to be common. A number of studies have identified trade-offs that emerge across scales, reflecting the tension between strategies that optimize within-host proliferation and large-scale population spread. Most of these studies are theoretical in nature, with direct experimental tests of such cross-scale trade-offs still rare. Here, we report an analysis of avian influenza A viruses across scales, focusing on the phenotype of temperaturedependent viral persistence. Taking advantage of a unique dataset that reports both environmental virus decay rates and strain-specific viral kinetics from duck challenge experiments, we show that the temperature-dependent environmental decay rate of a strain does not impact within-host virus load. Hence, for this phenotype, the scales of within-host infection dynamics and between-host environmental persistence do not seem to interact: viral fitness may be optimized on each scale without cross-scale trade-offs. Instead, we confirm the existence of a temperature-dependent persistence trade-off on a single scale, with some strains favouring environmental persistence in water at low temperatures while others reduce sensitivity to increasing temperatures. We show that this temperature-dependent trade-off is a robust phenomenon and does not depend on the details of data analysis. Our findings suggest that viruses might employ different environmental persistence strategies, which facilitates the coexistence of diverse strains in ecological niches. We conclude that a better understanding of the transmission and evolutionary dynamics of influenza A viruses probably requires empirical information regarding both within-host dynamics and environmental traits, integrated within a combined ecological and within-host framework.

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Section: Introductionmentioning

confidence: 99%

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

et al. 2014

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“…As mentioned above, the depletion of a finite resource is a clear avenue for future investigation. The influence of cell size in sequestering this resource (Vasi et al 1994), in survival through stationary phase, or in survival through the bottleneck (Handel and Bennett 2008) could then also be addressed. and, usefully, points along a trajectory in s have the same values of G i .…”

Section: Discussionmentioning

confidence: 99%

Survival Probability of Beneficial Mutations in Bacterial Batch Culture

Wahl

Zhu²

2015

Genetics

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The survival of rare beneficial mutations can be extremely sensitive to the organism's life history and the trait affected by the mutation. Given the tremendous impact of bacteria in batch culture as a model system for the study of adaptation, it is important to understand the survival probability of beneficial mutations in these populations. Here we develop a life-history model for bacterial populations in batch culture and predict the survival of mutations that increase fitness through their effects on specific traits: lag time, fission time, viability, and the timing of stationary phase. We find that if beneficial mutations are present in the founding population at the beginning of culture growth, mutations that reduce the mortality of daughter cells are the most likely to survive drift. In contrast, of mutations that occur de novo during growth, those that delay the onset of stationary phase are the most likely to survive. Our model predicts that approximately fivefold population growth between bottlenecks will optimize the occurrence and survival of beneficial mutations of all four types. This prediction is relatively insensitive to other model parameters, such as the lag time, fission time, or mortality rate of the population. We further estimate that bottlenecks that are more severe than this optimal prediction substantially reduce the occurrence and survival of adaptive mutations.KEYWORDS fixation probability; serial passaging; adaptation; experimental evolution; life history I T is well understood that most de novo mutations, even if they confer a substantial fitness advantage to the organism, do not survive the vicissitudes of genetic drift when initially rare (Fisher 1922;Haldane 1927;Wright 1929;Kimura 1964). The influences of population size, population structure, and environmental fluctuations on the fate of beneficial mutations have all been well studied, including cyclic (Otto and Whitlock 1997;Pollak 2000) or dynamically changing population sizes (Lambert 2006; Parsons and Quince 2007a,b), population subdivision (Barton 1993;Cherry 2003;Whitlock 2003) and migration (Lundy and Possingham 1998;Shpak and Proulx 2007), fluctuating selection (Haccou and Iwasa 1996;Lande 2007), or several of these factors in combination (Uecker and Hermisson 2011;Waxman 2011).A phenomenon that is perhaps less well appreciated is the sensitivity of a beneficial mutation's fate-survival or extinction-to the details of the organism's life history and the trait affected by the mutation. Studies of the extinction process in a population of changing size have demonstrated that extinction probabilities sensitively depend on whether mutations increase birth rates or reduce death rates (Parsons and Quince 2007a,b) or if mutations affect other life-history traits (Lambert 2006). Previous work has also compared the fate of mutations that reduce generation times with those that increase offspring survival (Wahl and Dehaan 2004). From these studies a clear picture is emerging: beneficial mutations that confer the same ...

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“…During this second stage of the regime, we subjected populations to either extreme heat or low pH. Overall fitness was measured as a linear combination of the growth and decay rates weighted by the time spent under each condition (Handel and Bennett 2008). We varied the strength of selection by altering the time exposed to the secondary selective pressure to determine whether the starting point of the population relative to the phenotypic optimum determined whether pleiotropic mutations were observed.…”

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Synergistic Pleiotropy Overrides the Costs of Complexity in Viral Adaptation

McGee¹,

Sackman²,

Morrison³

et al. 2015

Genetics

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Adaptive evolution progresses as a series of steps toward a multidimensional phenotypic optimum, and organismal or environmental complexity determines the number of phenotypic dimensions, or traits, under selection. Populations evolving in complex environments may experience costs of complexity such that improvement in one or more traits is impeded by selection on others. We compared the fitness effects of the first fixed mutations for populations of single-stranded DNA bacteriophage evolving under simple selection for growth rate to those of populations evolving under more complex selection for growth rate as well as capsid stability. We detected a cost of complexity manifested as a smaller growth rate improvement for mutations fixed under complex conditions. We found that, despite imposing a cost for growth rate improvement, strong complex selection resulted in the greatest overall fitness improvement, even for single mutations. Under weaker secondary selective pressures, tradeoffs between growth rate and stability were pervasive, but strong selection on the secondary trait resulted largely in mutations beneficial to both traits. Strength of selection therefore determined the nature of pleiotropy governing observed trait evolution, and strong positive selection forced populations to find mutations that improved multiple traits, thereby overriding costs incurred as a result of a more complex selective environment. The costs of complexity, however, remained substantial when considering the effects on a single trait in the context of selection on multiple traits.

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Surviving the Bottleneck: Transmission Mutants and the Evolution of Microbial Populations

Cited by 32 publications

References 53 publications

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

Survival Probability of Beneficial Mutations in Bacterial Batch Culture

Synergistic Pleiotropy Overrides the Costs of Complexity in Viral Adaptation

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