Limits...
Mutational meltdown in primary endosymbionts: selection limits Muller's ratchet.

Allen JM, Light JE, Perotti MA, Braig HR, Reed DL - PLoS ONE (2009)

Bottom Line: When comparing Riesia to other insect p-endosymbionts, we find that nucleotide substitution rates decrease dramatically as the age of endosymbiosis increases.A decrease in nucleotide substitution rates over time suggests that selection may be limiting the effects of Muller's ratchet by removing individuals with the highest mutational loads and decreasing the rate at which new mutations become fixed.This countering effect of selection could slow the overall rate of endosymbiont extinction.

View Article: PubMed Central - PubMed

Affiliation: Zoology Department and Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA. juliema@ufl.edu

ABSTRACT

Background: Primary bacterial endosymbionts of insects (p-endosymbionts) are thought to be undergoing the process of Muller's ratchet where they accrue slightly deleterious mutations due to genetic drift in small populations with negligible recombination rates. If this process were to go unchecked over time, theory predicts mutational meltdown and eventual extinction. Although genome degradation is common among p-endosymbionts, we do not observe widespread p-endosymbiont extinction, suggesting that Muller's ratchet may be slowed or even stopped over time. For example, selection may act to slow the effects of Muller's ratchet by removing slightly deleterious mutations before they go to fixation thereby causing a decrease in nucleotide substitutions rates in older p-endosymbiont lineages.

Methodology/principal findings: To determine whether selection is slowing the effects of Muller's ratchet, we determined the age of the Candidatus Riesia/sucking louse assemblage and analyzed the nucleotide substitution rates of several p-endosymbiont lineages that differ in the length of time that they have been associated with their insect hosts. We find that Riesia is the youngest p-endosymbiont known to date, and has been associated with its louse hosts for only 13-25 My. Further, it is the fastest evolving p-endosymbiont with substitution rates of 19-34% per 50 My. When comparing Riesia to other insect p-endosymbionts, we find that nucleotide substitution rates decrease dramatically as the age of endosymbiosis increases.

Conclusions/significance: A decrease in nucleotide substitution rates over time suggests that selection may be limiting the effects of Muller's ratchet by removing individuals with the highest mutational loads and decreasing the rate at which new mutations become fixed. This countering effect of selection could slow the overall rate of endosymbiont extinction.

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Primary endosymbiont nucleotide substitution rates as a function of the age of insect/p-endosymbiont association.Ages and rates were retrieved from the literature or were calculated from pairwise sequence divergences and are shown as percent per 50 My. Point estimates (diamonds) represent the median value between the upper and lower estimates (bars show the full range of dates). The dotted line indicates a rate of 2% per 50 My. It has been suggested that the tse-tse fly and aphid p-endosymbionts (Wigglesworthia and Buchnera, respectively) are closely related to each other and are the result of a more ancient endosymbiosis event than represented here [68], [69]. Using an older date to calculate rates, however, does not change the results (data available upon request).
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pone-0004969-g003: Primary endosymbiont nucleotide substitution rates as a function of the age of insect/p-endosymbiont association.Ages and rates were retrieved from the literature or were calculated from pairwise sequence divergences and are shown as percent per 50 My. Point estimates (diamonds) represent the median value between the upper and lower estimates (bars show the full range of dates). The dotted line indicates a rate of 2% per 50 My. It has been suggested that the tse-tse fly and aphid p-endosymbionts (Wigglesworthia and Buchnera, respectively) are closely related to each other and are the result of a more ancient endosymbiosis event than represented here [68], [69]. Using an older date to calculate rates, however, does not change the results (data available upon request).

Mentions: When the rates of nucleotide substitution for Riesia are compared to other known insect/p-endosymbiont systems, we find that the rate of substitutions in 16S rDNA decreases with age of association and levels off after 100 My (Figure 3). Although the majority of the systems are evolving at a rate similar to what was reported for Buchnera (1–2% per 50 MY), the younger systems are evolving much faster (3–34% per 50 MY; Figure 3). Reduced major axis regression of the log-transformed data indicates that 78% of the variation in rates of nucleotide evolution can be explained by the age of the association (Figure 4) and that the decrease in rates is exponential. The pairwise sequence divergence in Riesia calculated here (18.56–34.24% per 50 My) were corrected with a best-fit model of nucleotide substitution. Some previous studies did not use the best-fit evolutionary model to correct for multiple substitutions. Therefore, to test the impact of the substitution model, we also evaluated the same pairwise divergences using the Jukes-Cantor model. The Jukes-Cantor distances still provide a much faster rate of nucleotide substitution in Riesia (12.9–23.9% per 50 My), and it is important to note that this more simplistic model of molecular evolution underestimates the substitution rate by 30%.


Mutational meltdown in primary endosymbionts: selection limits Muller's ratchet.

Allen JM, Light JE, Perotti MA, Braig HR, Reed DL - PLoS ONE (2009)

Primary endosymbiont nucleotide substitution rates as a function of the age of insect/p-endosymbiont association.Ages and rates were retrieved from the literature or were calculated from pairwise sequence divergences and are shown as percent per 50 My. Point estimates (diamonds) represent the median value between the upper and lower estimates (bars show the full range of dates). The dotted line indicates a rate of 2% per 50 My. It has been suggested that the tse-tse fly and aphid p-endosymbionts (Wigglesworthia and Buchnera, respectively) are closely related to each other and are the result of a more ancient endosymbiosis event than represented here [68], [69]. Using an older date to calculate rates, however, does not change the results (data available upon request).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2654755&req=5

pone-0004969-g003: Primary endosymbiont nucleotide substitution rates as a function of the age of insect/p-endosymbiont association.Ages and rates were retrieved from the literature or were calculated from pairwise sequence divergences and are shown as percent per 50 My. Point estimates (diamonds) represent the median value between the upper and lower estimates (bars show the full range of dates). The dotted line indicates a rate of 2% per 50 My. It has been suggested that the tse-tse fly and aphid p-endosymbionts (Wigglesworthia and Buchnera, respectively) are closely related to each other and are the result of a more ancient endosymbiosis event than represented here [68], [69]. Using an older date to calculate rates, however, does not change the results (data available upon request).
Mentions: When the rates of nucleotide substitution for Riesia are compared to other known insect/p-endosymbiont systems, we find that the rate of substitutions in 16S rDNA decreases with age of association and levels off after 100 My (Figure 3). Although the majority of the systems are evolving at a rate similar to what was reported for Buchnera (1–2% per 50 MY), the younger systems are evolving much faster (3–34% per 50 MY; Figure 3). Reduced major axis regression of the log-transformed data indicates that 78% of the variation in rates of nucleotide evolution can be explained by the age of the association (Figure 4) and that the decrease in rates is exponential. The pairwise sequence divergence in Riesia calculated here (18.56–34.24% per 50 My) were corrected with a best-fit model of nucleotide substitution. Some previous studies did not use the best-fit evolutionary model to correct for multiple substitutions. Therefore, to test the impact of the substitution model, we also evaluated the same pairwise divergences using the Jukes-Cantor model. The Jukes-Cantor distances still provide a much faster rate of nucleotide substitution in Riesia (12.9–23.9% per 50 My), and it is important to note that this more simplistic model of molecular evolution underestimates the substitution rate by 30%.

Bottom Line: When comparing Riesia to other insect p-endosymbionts, we find that nucleotide substitution rates decrease dramatically as the age of endosymbiosis increases.A decrease in nucleotide substitution rates over time suggests that selection may be limiting the effects of Muller's ratchet by removing individuals with the highest mutational loads and decreasing the rate at which new mutations become fixed.This countering effect of selection could slow the overall rate of endosymbiont extinction.

View Article: PubMed Central - PubMed

Affiliation: Zoology Department and Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA. juliema@ufl.edu

ABSTRACT

Background: Primary bacterial endosymbionts of insects (p-endosymbionts) are thought to be undergoing the process of Muller's ratchet where they accrue slightly deleterious mutations due to genetic drift in small populations with negligible recombination rates. If this process were to go unchecked over time, theory predicts mutational meltdown and eventual extinction. Although genome degradation is common among p-endosymbionts, we do not observe widespread p-endosymbiont extinction, suggesting that Muller's ratchet may be slowed or even stopped over time. For example, selection may act to slow the effects of Muller's ratchet by removing slightly deleterious mutations before they go to fixation thereby causing a decrease in nucleotide substitutions rates in older p-endosymbiont lineages.

Methodology/principal findings: To determine whether selection is slowing the effects of Muller's ratchet, we determined the age of the Candidatus Riesia/sucking louse assemblage and analyzed the nucleotide substitution rates of several p-endosymbiont lineages that differ in the length of time that they have been associated with their insect hosts. We find that Riesia is the youngest p-endosymbiont known to date, and has been associated with its louse hosts for only 13-25 My. Further, it is the fastest evolving p-endosymbiont with substitution rates of 19-34% per 50 My. When comparing Riesia to other insect p-endosymbionts, we find that nucleotide substitution rates decrease dramatically as the age of endosymbiosis increases.

Conclusions/significance: A decrease in nucleotide substitution rates over time suggests that selection may be limiting the effects of Muller's ratchet by removing individuals with the highest mutational loads and decreasing the rate at which new mutations become fixed. This countering effect of selection could slow the overall rate of endosymbiont extinction.

Show MeSH
Related in: MedlinePlus