Mutation accumulation in Tetrahymena

Patricia H Brito,Helena Soares,Elsa Guilherme,Isabel Gordo

doi:10.1186/1471-2148-10-354

Abstract

BackgroundThe rate and fitness effects of mutations are key in understanding the evolution of every species. Traditionally, these parameters are estimated in mutation accumulation experiments where replicate lines are propagated in conditions that allow mutations to randomly accumulate without the purging effect of natural selection. These experiments have been performed with many model organisms but we still lack empirical estimates of the rate and effects of mutation in the protists.ResultsWe performed a mutation accumulation (MA) experiment in Tetrahymena thermophila, a species that can reproduce sexually and asexually in nature, and measured both the mean decline and variance increase in fitness of 20 lines. The results obtained with T. thermophila were compared with T. pyriformis that is an obligate asexual species. We show that MA lines of T. thermophila go to extinction at a rate of 1.25 clonal extinctions per bottleneck. In contrast, populations of T. pyriformis show a much higher resistance to extinction. Variation in gene copy number is likely to be a key factor in explaining these results, and indeed we show that T. pyriformis has a higher mean copy number per cell than T. thermophila. From fitness measurements during the MA experiment, we infer a rate of mutation to copy number variation of 0.0333 per haploid MAC genome of T. thermophila and a mean effect against copy number variation of 0.16. A strong effect of population size in the rate of fitness decline was also found, consistent with the increased power of natural selection.ConclusionsThe rate of clonal extinction measured for T. thermophila is characteristic of a mutational degradation and suggests that this species must undergo sexual reproduction to avoid the deleterious effects detected in the laboratory experiments. We also suggest that an increase in chromosomal copy number associated with the phenotypic assortment of amitotic divisions can provide an alternative mechanism to escape the deleterious effect of random chromosomal copy number variation in species like T. pyriformis that lack the resetting mechanism of sexual reproduction. Our results are relevant to the understanding of cell line longevity and senescence in ciliates.

Highlights

The rate and fitness effects of mutations are key in understanding the evolution of every species
Lynch and Gabriel [19] had previously estimated the mutation load of Paramecium caudatum this estimate was performed on data collected to determine the species maximum lifespan and replicate lines were obtained from a diverse population and initial phenotypic variability was not set to zero as it is typical of mutation accumulation (MA) studies
Due to the particular mode that characterizes the genetic segregation in the macronucleous of Tetrahymena that defies the rules of diploid Mendelian inheritance, we developed a simple simulation model to estimate both U - the rate at which copy number variation in the MAC occurs- and s - the mean effect on fitness caused by deviations of the optimum copy number

Summary

Introduction

The rate and fitness effects of mutations are key in understanding the evolution of every species These parameters are estimated in mutation accumulation experiments where replicate lines are propagated in conditions that allow mutations to randomly accumulate without the purging effect of natural selection. These experiments have been performed with many model organisms but we still lack empirical estimates of the rate and effects of mutation in the protists. Lynch and Gabriel [19] had previously estimated the mutation load of Paramecium caudatum this estimate was performed on data collected to determine the species maximum lifespan and replicate lines were obtained from a diverse population and initial phenotypic variability was not set to zero as it is typical of MA studies

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