Plasticity, pleiotropy and fitness tradeoffs in Arabidopsis genotypes with different telomere lengths

AbstractViruses are under relentless selective pressure from host immune defenses. To study how poxviruses adapt to innate immune detection pathways, we performed serial infections of vaccinia virus in primary human cells. Independent courses of experimental evolution with a recombinant strain lacking E3L revealed several high frequency point mutations in conserved poxvirus genes, suggesting important roles for essential poxvirus proteins in innate immune subversion. Two distinct mutations were identified in the viral RNA polymerase gene A24R, which seem to act through different mechanisms to increase virus replication. Specifically, a Leu18Phe substitution in A24R conferred fitness tradeoffs, including increased activation of the antiviral factor Protein kinase R (PKR). Intriguingly, this A24R variant underwent a drastic selective sweep during passaging, despite enhanced PKR activity. We show that the sweep of this variant can be accelerated by the presence of copy number variation (CNV) at the K3L locus, which with multiple copies strongly reduces PKR activation. Therefore, adaptive cases of CNV can also facilitate the accumulation of point mutations separate from the expanded locus. This study reveals how rapid bouts of gene copy number amplification during accrual of distant point mutations can potently facilitate poxvirus adaptation to host defenses.ImportanceViruses can quickly evolve to defeat host immune functions. For poxviruses, little is known about how multiple adaptive mutations might concurrently emerge in populations. In this study, we uncovered a means of vaccinia virus adaptation involving the accumulation of distinct genetic variants within a single population. We identified adaptive point mutations in the viral RNA polymerase gene A24R, and show that these mutations can affect the activation of host nucleic acid sensing pathways through different mechanisms. We also found that structural variants within viral genomes in the form of gene copy number variation (CNV) provide dual benefits to evolving populations, including evidence that CNV facilitates the accumulation of a point mutation distant from the expanded locus. Our data suggest that transient CNV can accommodate the accumulation of mutations conferring modest benefits, or even fitness tradeoffs, and highlight how structural variation might aid poxvirus adaptation through both direct and indirect action.

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Coherent synthesis of genomic associations with phenotypes and home environments

10.1101/051110 ◽

2016 ◽

Author(s):

Jesse R. Lasky ◽

Brenna R. Forester ◽

Matthew Reimherr

Keyword(s):

Local Adaptation ◽

Environmental Gradients ◽

Common Garden ◽

Relative Fitness ◽

Home Environments ◽

Climate Gradients ◽

A Genome ◽

Fitness Tradeoffs ◽

Common Garden Experiments ◽

Diverse Data

Local adaptation is often studied via 1) multiple common garden experiments comparing performance of genotypes in different environments and 2) sequencing genotypes from multiple locations and characterizing geographic patterns in allele frequency. Both approaches aim to characterize the same pattern (local adaptation), yet the complementary information from each has not yet been coherently integrated. Here, we develop a genome-wide association model of genotype interactions with continuous environmental gradients (G×E), i.e. reaction norms. We present an approach to impute relative fitness, allowing us to coherently synthesize evidence from common garden and genome-environment associations. Our approach identifies loci exhibiting environmental clines where alleles are associated with higher fitness in home environments. Simulations show our approach can increase power to detect loci causing local adaptation. In a case study on Arabidopsis thaliana, most identified SNPs exhibited home allele advantage and fitness tradeoffs along climate gradients, suggesting selective gradients can maintain allelic clines. SNPs exhibiting G×E associations with fitness were enriched in genic regions, putative partial selective sweeps, and associations with an adaptive phenotype (flowering time plasticity). We discuss extensions for situations where only adaptive phenotypes other than fitness are available. Many types of data may point toward the loci underlying G×E and local adaptation; coherent models of diverse data provide a principled basis for synthesis.

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Does batrachotoxin autoresistance co-evolve with toxicity in Phyllobates poison-dart frogs?

10.1101/460865 ◽

2018 ◽

Author(s):

Roberto Márquez ◽

Valeria Ramírez-Castañeda ◽

Adolfo Amézquita

Keyword(s):

Natural Populations ◽

Future Research ◽

Costs And Benefits ◽

Evolutionary Mechanisms ◽

Toxin Resistance ◽

History Of ◽

Fitness Tradeoffs ◽

Living Organisms ◽

The Relationship ◽

Shed Light

AbstractToxicity is widespread among living organisms, and evolves as a multimodal phenotype. Part of this phenotype is the ability to avoid self-intoxication (autoresistance). Evolving toxin resistance can involve fitness tradeoffs, so autoresistance is often expected to evolve gradually and in tandem with toxicity, resulting in a correlation between the degrees of toxicity and autoresistance among toxic populations. We investigate this correlation in Phyllobates poison frogs, notorious for secreting batrachotoxin (BTX), a potent neurotoxin that targets sodium channels, using ancestral sequence reconstructions of BTX–sensing areas of the muscular voltage-gated sodium channel. Reconstructions suggest that BTX resistance arose at the root of Phyllobates, coinciding with the evolution of BTX secretion. After this event little or no further evolution of autoresistance seems to have occurred, despite large increases in toxicity throughout the history of these frogs. Our results therefore provide no evidence in favor of an evolutionary correlation between toxicity and autoresistance, which conflicts with previous work. Future research on the functional costs and benefits of mutations putatively involved in BTX resistance, as well as their prevalence in natural populations should shed light on the evolutionary mechanisms driving the relationship between toxicity and autoresistance in Phyllobates frogs.

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Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1424242112 ◽

2015 ◽

Vol 112 (9) ◽

pp. 2776-2781 ◽

Cited By ~ 38

Author(s):

Corina E. Tarnita ◽

Alex Washburne ◽

Ricardo Martinez-Garcia ◽

Allyson E. Sgro ◽

Simon A. Levin

Keyword(s):

Altruistic Behavior ◽

Bet Hedging ◽

Hedging Strategy ◽

Slime Molds ◽

Complex Interactions ◽

Local Environments ◽

Cellular Slime ◽

Cellular Slime Molds ◽

Fitness Tradeoffs ◽

Clear Description

Cellular slime molds, including the well-studied Dictyostelium discoideum, are amoebae whose life cycle includes both a single-cellular and a multicellular stage. To achieve the multicellular stage, individual amoebae aggregate upon starvation to form a fruiting body made of dead stalk cells and reproductive spores, a process that has been described in terms of cooperation and altruism. When amoebae aggregate they do not perfectly discriminate against nonkin, leading to chimeric fruiting bodies. Within chimeras, complex interactions among genotypes have been documented, which should theoretically reduce genetic diversity. This is however inconsistent with the great diversity of genotypes found in nature. Recent work has shown that a little-studied component of D. discoideum fitness—the loner cells that do not participate in the aggregation—can be selected for depending on environmental conditions and that, together with the spores, they could represent a bet-hedging strategy. We suggest that in all cellular slime molds the existence of loners could resolve the apparent diversity paradox in two ways. First, if loners are accounted for, then apparent genotypic skew in the spores of chimeras could simply be the result of different investments into spores versus loners. Second, in an ecosystem with multiple local environments differing in their food recovery characteristics and connected globally via weak-to-moderate dispersal, coexistence of multiple genotypes can occur. Finally, we argue that the loners make it impossible to define altruistic behavior, winners or losers, without a clear description of the ecology.

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Heterogeneous Selection in a Spatially Structured Environment Affects Fitness Tradeoffs of Plasmid Carriage in Pseudomonads

Applied and Environmental Microbiology ◽

10.1128/aem.02383-07 ◽

2008 ◽

Vol 74 (10) ◽

pp. 3189-3197 ◽

Cited By ~ 11

Author(s):

Frances R. Slater ◽

Kenneth D. Bruce ◽

Richard J. Ellis ◽

Andrew K. Lilley ◽

Sarah L. Turner

Keyword(s):

Variable Selection ◽

Community Dynamics ◽

Experimental System ◽

Epifluorescence Microscopy ◽

Spatial And Temporal Variation ◽

Natural Environments ◽

Selection Pressures ◽

Selection For ◽

Fitness Tradeoffs ◽

Plasmid Carriage

ABSTRACT Environmental conditions under which fitness tradeoffs of plasmid carriage are balanced to facilitate plasmid persistence remain elusive. Periodic selection for plasmid-encoded traits due to the spatial and temporal variation typical in most natural environments (such as soil particles, plant leaf and root surfaces, gut linings, and the skin) may play a role. However, quantification of selection pressures and their effects is difficult at a scale relevant to the bacterium in situ. The present work describes a novel experimental system for such fine-scale quantification, with conditions designed to mimic the mosaic of spatially variable selection pressures present in natural surface environments. The effects of uniform and spatially heterogeneous mercuric chloride (HgCl2) on the dynamics of a model community of plasmid-carrying, mercury-resistant (Hgr) and plasmid-free, mercury-sensitive (Hgs) pseudomonads were compared. Hg resulted in an increase in the surface area occupied by, and therefore an increase in the fitness of, Hgr bacteria relative to Hgs bacteria. Uniform and heterogeneous Hg distributions were demonstrated to result in different community structures by epifluorescence microscopy, with heterogeneous Hg producing spatially variable selection landscapes. The effects of heterogeneous Hg were only apparent at scales of a few hundred micrometers, emphasizing the importance of using appropriate analysis methods to detect effects of environmental heterogeneity on community dynamics. Heterogeneous Hg resulted in negative frequency-dependent selection for Hgr cells, suggesting that sporadic selection may facilitate the discontinuous distribution of plasmids through host populations in complex, structured environments.

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Lazarus effects: the frequency and genetic causes of Escherichia coli population recovery under lethal heat stress

10.1101/058479 ◽

2016 ◽

Author(s):

Shaun M. Hug ◽

Brandon S. Gaut

Keyword(s):

Escherichia Coli ◽

Antagonistic Pleiotropy ◽

Lethal Temperature ◽

Epistatic Interactions ◽

Genetic Changes ◽

E Coli ◽

Evolutionary Innovation ◽

Fitness Benefits ◽

Fitness Tradeoffs ◽

Lazarus Effect

ABSTRACTSometimes populations crash and yet recover before being lost completely. Such recoveries have been observed incidentally in evolution experiments using Escherichia coli, and this phenomenon has been termed the “Lazarus effect.” To investigate how often recovery occurs and the genetic changes that drive it, we evolved ~300 populations of E. coli at lethally high temperatures (43.0°) for five days and sequenced the genomes of recovered populations. Our results revealed that the Lazarus effect is uncommon, but frequent enough, at ~9% of populations, to be a potent source of evolutionary innovation. Population sequencing uncovered a set of mutations adaptive to lethal 43.0°C that were mostly distinct from those that were beneficial at a high but nonlethal temperature (42.2°). Mutations within two operons—the heat shock hslUV operon and the RNA polymerase rpoBC operon—drove adaptation to lethal temperature. Mutations in hslUV exhibited little antagonistic pleiotropy at 37.0°C and may have arisen neutrally prior to subjection to lethal temperature. In contrast, rpoBC mutations provided greater fitness benefits than hslUV mutants, but were less prevalent and caused stronger fitness tradeoffs at lower temperatures. Recovered populations fixed mutations in only one operon or the other, but not both, indicating that epistatic interactions between beneficial mutations were important even at the earliest stages of adaptation.

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Immune Loss as a Driver of Coexistence During Host-Phage Coevolution

10.1101/105908 ◽

2017 ◽

Cited By ~ 3

Author(s):

Jake L Weissman ◽

Rayshawn Holmes ◽

Rodolphe Barrangou ◽

Sylvain Moineau ◽

William F Fagan ◽

...

Keyword(s):

Immune System ◽

Constant Pressure ◽

Arms Race ◽

Bacterial Host ◽

Viral Pathogens ◽

Fitness Tradeoffs ◽

Parameter Ranges ◽

Selective Regime ◽

Mixed Systems

AbstractBacteria and their viral pathogens face constant pressure for augmented immune and infective capabilities, respectively. Under this reciprocally imposed selective regime, we expect to see a runaway evolutionary arms race, ultimately leading to the extinction of one species. Despite this prediction, in many systems host and pathogen coexist with minimal coevolution even when well-mixed. Previous work explained this puzzling phenomenon by invoking fitness tradeoffs, which can diminish an arms race dynamic. Here we propose that the regular loss of immunity by the bacterial host can also produce host-phage coexistence. We pair a general model of immunity with an experimental and theoretical case study of the CRISPR-Cas immune system to contrast the behavior of tradeoff and loss mechanisms in well-mixed systems. We find that, while both mechanisms can produce stable coexistence, only immune loss does so robustly within realistic parameter ranges.

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