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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Related in: MedlinePlus

Maximum likelihood phylogram representing phylogenetic relationships of louse p-endosymbionts, common insect p-endosymbionts, and closely related taxa as determined from a BLAST search of each louse endosymbiont sequence.Numbers at nodes indicate maximum likelihood support values greater than 60. Gray lines indicate louse p-endosymbionts. The p-endosymbiont from Pedicinus badii (the louse that parasitizes Red Colobus monkeys) is shown in red demonstrating that it does not group with the Riesia p-endosymbionts. There are now at least six distinct clades of p-endosymbionts sampled from sucking lice.
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pone-0004969-g001: Maximum likelihood phylogram representing phylogenetic relationships of louse p-endosymbionts, common insect p-endosymbionts, and closely related taxa as determined from a BLAST search of each louse endosymbiont sequence.Numbers at nodes indicate maximum likelihood support values greater than 60. Gray lines indicate louse p-endosymbionts. The p-endosymbiont from Pedicinus badii (the louse that parasitizes Red Colobus monkeys) is shown in red demonstrating that it does not group with the Riesia p-endosymbionts. There are now at least six distinct clades of p-endosymbionts sampled from sucking lice.

Mentions: The age of the association between the fast-evolving p-endosymbiont Riesia and the primate sucking lice in which it lives was previously unknown. In order to estimate this age, we examined the p-endosymbiont from a closely related louse genus, Pedicinus. The p-endosymbiont from Pedicinus badii (a louse that parasitizes Old World monkeys) does not group with the anthropoid primate louse p-endosymbionts (the Riesia lineage) in our Maximum Likelihood or Bayesian (not shown) phylogenetic analyses (Figure 1). The Maximum Likelihood analysis groups the p-endosymbiont of Pedicinus badii at the base of a clade containing the p-endosymbionts Wigglesworthia and Baumannia (p-endosymbionts of tse-tse flies and leafhoppers, respectfully), some free-living bacteria, and the p-endosymbionts of distantly related sucking lice of rodents (Figure 1). Bayesian phylogenetic trees were largely identical, and placed the p-endosymbiont of Pedicinus badii at the base of the same clade. Analyses constraining the Pedicinus p-endosymbiont to group with the Riesia lineage produced trees that were significantly worse than the best Maximum Likelihood tree according to the Kishino-Hasegawa (p = 0.004) and Shimodaira-Hasegawa (p = 0.004) tests. Furthermore, none of the suboptimal trees from the Bayesian analysis were consistent with this topological constraint (p<0.001). We can therefore formally reject the hypothesis that the p-endosymbiont sequences from Pedicinus badii are sister to or embedded within the Riesia lineage. Because Pedicinus is the closest living relative of Pediculus and Pthirus, this phylogenetic analysis demonstrates that the age of the association between Riesia and primate lice has an upper bound at 25 My for the split between Pedicinus and Pediculus and Pthirus. Thus, the age of association between Riesia and their louse hosts is between 12.95 and 25 My, making this one of the youngest insect/p-endosymbiont assemblages known.


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

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

Maximum likelihood phylogram representing phylogenetic relationships of louse p-endosymbionts, common insect p-endosymbionts, and closely related taxa as determined from a BLAST search of each louse endosymbiont sequence.Numbers at nodes indicate maximum likelihood support values greater than 60. Gray lines indicate louse p-endosymbionts. The p-endosymbiont from Pedicinus badii (the louse that parasitizes Red Colobus monkeys) is shown in red demonstrating that it does not group with the Riesia p-endosymbionts. There are now at least six distinct clades of p-endosymbionts sampled from sucking lice.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0004969-g001: Maximum likelihood phylogram representing phylogenetic relationships of louse p-endosymbionts, common insect p-endosymbionts, and closely related taxa as determined from a BLAST search of each louse endosymbiont sequence.Numbers at nodes indicate maximum likelihood support values greater than 60. Gray lines indicate louse p-endosymbionts. The p-endosymbiont from Pedicinus badii (the louse that parasitizes Red Colobus monkeys) is shown in red demonstrating that it does not group with the Riesia p-endosymbionts. There are now at least six distinct clades of p-endosymbionts sampled from sucking lice.
Mentions: The age of the association between the fast-evolving p-endosymbiont Riesia and the primate sucking lice in which it lives was previously unknown. In order to estimate this age, we examined the p-endosymbiont from a closely related louse genus, Pedicinus. The p-endosymbiont from Pedicinus badii (a louse that parasitizes Old World monkeys) does not group with the anthropoid primate louse p-endosymbionts (the Riesia lineage) in our Maximum Likelihood or Bayesian (not shown) phylogenetic analyses (Figure 1). The Maximum Likelihood analysis groups the p-endosymbiont of Pedicinus badii at the base of a clade containing the p-endosymbionts Wigglesworthia and Baumannia (p-endosymbionts of tse-tse flies and leafhoppers, respectfully), some free-living bacteria, and the p-endosymbionts of distantly related sucking lice of rodents (Figure 1). Bayesian phylogenetic trees were largely identical, and placed the p-endosymbiont of Pedicinus badii at the base of the same clade. Analyses constraining the Pedicinus p-endosymbiont to group with the Riesia lineage produced trees that were significantly worse than the best Maximum Likelihood tree according to the Kishino-Hasegawa (p = 0.004) and Shimodaira-Hasegawa (p = 0.004) tests. Furthermore, none of the suboptimal trees from the Bayesian analysis were consistent with this topological constraint (p<0.001). We can therefore formally reject the hypothesis that the p-endosymbiont sequences from Pedicinus badii are sister to or embedded within the Riesia lineage. Because Pedicinus is the closest living relative of Pediculus and Pthirus, this phylogenetic analysis demonstrates that the age of the association between Riesia and primate lice has an upper bound at 25 My for the split between Pedicinus and Pediculus and Pthirus. Thus, the age of association between Riesia and their louse hosts is between 12.95 and 25 My, making this one of the youngest insect/p-endosymbiont assemblages known.

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