Fitness effects of new mutations in<i>Chlamydomonas reinhardtii</i>across two stress gradients

Kraemer, Susanne A.; Morgan, Andrew D.; Ness, Robert W.; Keightley, Peter D.; Colegrave, Nick

doi:10.1101/033886

Cited by 10 publications

(19 citation statements)

References 48 publications

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“…By accommodating explicitly for individual nonheritable variation in longevity, the measurable genotype fitness becomes dependent on the strength of selection which may vary between environments. This trend is common in data (Kraemer, Morgan, Ness, Keightley, & Colegrave, 2016), but the reverse has also been observed (Kishony & Leibler, 2003) and occurs in our framework when mutants are less variable than their ancestors (Figure 4b,d,f). First, we assume that the phenotypic variance of the ancestor is negligible compared to the mutant and find this to result in measurable fitness ratios (solid colored lines in Figure 4a,c,e) that are consistently lower than those that would have resulted from the same mean effects if mutant and ancestor had the same variance (dashed lines), a discrepancy that increases with stress.…”

Section: Rel Ative Fitne Ss Defined Along S Tre Ss G R Ad Ientssupporting

confidence: 86%

The effects of individual nonheritable variation on fitness estimation and coexistence

Gomes

King

Nunes

et al. 2019

Ecology and Evolution

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Demographic theory and data have emphasized that nonheritable variation in individual frailty enables selection within cohorts, affecting the dynamics of a population while being invisible to its evolution. Here, we include the component of individual variation in longevity or viability which is nonheritable in simple bacterial growth models and explore its ecological and evolutionary impacts. First, we find that this variation produces consistent trends in longevity differences between bacterial genotypes when measured across stress gradients. Given that direct measurements of longevity are inevitably biased due to the presence of this variation and ongoing selection, we propose the use of the trend itself for obtaining more exact inferences of genotypic fitness. Second, we show how species or strain coexistence can be enabled by nonheritable variation in longevity or viability. These general conclusions are likely to extend beyond bacterial systems.

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Section: Rel Ative Fitne Ss Defined Along S Tre Ss G R Ad Ientssupporting

confidence: 86%

The effects of individual nonheritable variation on fitness estimation and coexistence

Gomes

King

Nunes

et al. 2019

Ecology and Evolution

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“…Specifically, some studies have shown that larger declines in fitness are experienced in harsher environments, while others have not (Martin and Lenormand 2006;Halligan and Keightley 2009;Kraemer et al 2015). In M9MM+CAA and M9MM, we can statistically distinguish fitness effects from s = 0 with greater precision (s , -0.03 in M9MM +CAA and s , -0.01 or s .…”

Section: Discussionmentioning

confidence: 87%

“…These lineages accumulate mutations independently over several thousand generations, and the magnitude and variance in fitness between lineages can be used to estimate several properties of the distribution of fitness effects (Halligan and Keightley 2009). MA studies have been used to characterize the fitness effects of spontaneous mutations in Drosophila melanogaster (Bateman 1959;Mukai 1964;Keightley 1994;Fry et al 1999), Arabidopsis thaliana Shaw et al 2000Shaw et al , 2002, Caenorhabditis elegans (Keightley and Caballero 1997;Vassilieva et al 2000;Estes et al 2004;Katju et al 2015), Saccharomyces cerevisiae (Wloch et al 2001;Zeyl and de Visser 2001;Dickinson 2008;Jasmin and Lenormand 2015), Escherichia coli (Kibota and Lynch 1996;Trindade et al 2010), and other microbes (Heilbron et al 2014;Kraemer et al 2015). Results from these studies have occasionally been inconsistent, but the majority of results suggest that most spontaneous mutations have mild effects (Eyre-Walker and Keightley 2007;Halligan and Keightley 2009;Agrawal and Whitlock 2012;Heilbron et al 2014), that deleterious mutations far outnumber beneficial mutations (Keightley and Lynch 2003;Eyre-Walker and Keightley 2007;Silander et al 2007), and that the distribution of effects of deleterious mutations is complex and multimodal (Zeyl and de Visser 2001;Eyre-Walker and Keightley 2007).…”

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confidence: 99%

The Fitness Effects of Spontaneous Mutations Nearly Unseen by Selection in a Bacterium with Multiple Chromosomes

Dillon

Cooper

2016

Genetics

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Mutation accumulation (MA) experiments employ the strategy of minimizing the population size of evolving lineages to greatly reduce effects of selection on newly arising mutations. Thus, most mutations fix within MA lines independently of their fitness effects. This approach, more recently combined with genome sequencing, has detailed the rates, spectra, and biases of different mutational processes. However, a quantitative understanding of the fitness effects of mutations virtually unseen by selection has remained an untapped opportunity. Here, we analyzed the fitness of 43 sequenced MA lines of the multi-chromosome bacterium Burkholderia cenocepacia that had each undergone 5554 generations of MA and accumulated an average of 6.73 spontaneous mutations. Most lineages exhibited either neutral or deleterious fitness in three different environments in comparison with their common ancestor. The only mutational class that was significantly overrepresented in lineages with reduced fitness was the loss of the plasmid, though nonsense mutations, missense mutations, and coding insertion-deletions were also overrepresented in MA lineages whose fitness had significantly declined. Although the overall distribution of fitness effects was similar between the three environments, the magnitude and even the sign of the fitness of a number of lineages changed with the environment, demonstrating that the fitness of some genotypes was environmentally dependent. These results present an unprecedented picture of the fitness effects of spontaneous mutations in a bacterium with multiple chromosomes and provide greater quantitative support for the theory that the vast majority of spontaneous mutations are neutral or deleterious.KEYWORDS fitness effects; deleterious mutation; pleiotropy; genetic drift; Burkholderia cenocepacia T HE extent to which spontaneous mutations contribute to evolutionary change largely depends on their rates and fitness effects. Both parameters are fundamental to several evolutionary problems, including the maintenance of genetic variation (Charlesworth et al. 1993(Charlesworth et al. , 2009Charlesworth and Charlesworth 1998), the evolution of recombination (Muller 1964;Kondrashov 1988;Otto and Lenormand 2002;Roze and Blanckaert 2014), the evolution of mutator alleles (Sniegowski et al. 1997;Tenaillon et al. 1999), and deleterious mutation accumulation (MA) in small populations (Lande 1994;Lynch et al. 1995Lynch et al. , 1999Schwander and Crespi 2009). Many studies have now obtained direct and robust estimates of mutation rates and spectra across diverse organisms, but our understanding of the fitness effects of spontaneous mutations remains limited to mostly indirect estimates in classic model organisms (Eyre-Walker and Keightley 2007).MA experiments provide the opportunity to quantify properties of the fitness of spontaneous mutations that have not been exposed to the sieve of natural selection. Specifically, MA experiments limit the efficiency of natural selection by passaging replicate lineages throu...

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“…To further investigate the effect of stress on mutational effects, we conducted competitive fitness assays in medium supplemented with 2.5 g/L NaCl, representing moderate stress (Kraemer et al. ). Moderately stressful conditions represent a more realistic scenario for environmental conditions that might be encountered by new mutants, in contrast to nearly lethal conditions.…”

Section: Resultsmentioning

confidence: 99%

Fitness change in relation to mutation number in spontaneous mutation accumulation lines ofChlamydomonas reinhardtii

et al. 2017

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Although all genetic variation ultimately stems from mutations, their properties are difficult to study directly. Here, we used multiple mutation accumulation (MA) lines derived from five genetic backgrounds of the green algae Chlamydomonas reinhardtii that have been previously subjected to whole genome sequencing to investigate the relationship between the number of spontaneous mutations and change in fitness from a nonevolved ancestor. MA lines were on average less fit than their ancestors and we detected a significantly negative correlation between the change in fitness and the total number of accumulated mutations in the genome. Likewise, the number of mutations located within coding regions significantly and negatively impacted MA line fitness. We used the fitness data to parameterize a maximum likelihood model to estimate discrete categories of mutational effects, and found that models containing one to two mutational effect categories (one neutral and one deleterious category) fitted the data best. However, the best‐fitting mutational effects models were highly dependent on the genetic background of the ancestral strain.

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Fitness effects of new mutations inChlamydomonas reinhardtiiacross two stress gradients

Cited by 10 publications

References 48 publications

The effects of individual nonheritable variation on fitness estimation and coexistence

The effects of individual nonheritable variation on fitness estimation and coexistence

The Fitness Effects of Spontaneous Mutations Nearly Unseen by Selection in a Bacterium with Multiple Chromosomes

Fitness change in relation to mutation number in spontaneous mutation accumulation lines ofChlamydomonas reinhardtii

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