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Muller's Ratchet and compensatory mutation in Caenorhabditis briggsae mitochondrial genome evolution.

Howe DK, Denver DR - BMC Evol. Biol. (2008)

Bottom Line: However, putative compensatory mutations were also observed that are predicted to reduce heteroplasmy levels of deleterious deletions.Paradoxically, compensatory mutations were observed in one major intraspecific C. briggsae clade where population sizes are estimated to be very small (and selection is predicted to be relatively weak), but not in a second major clade where population size estimates are much larger and selection is expected to be more efficient.This study provides evidence that the mitochondrial genomes of animals evolving in nature are susceptible to Muller's Ratchet, suggests that context-dependent compensatory mutations can accumulate in small populations, and predicts that Muller's Ratchet can affect fundamental evolutionary forces such as the rate of mutation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, 97331, USA. howed@science.oregonstate.edu

ABSTRACT

Background: The theory of Muller' Ratchet predicts that small asexual populations are doomed to accumulate ever-increasing deleterious mutation loads as a consequence of the magnified power of genetic drift and mutation that accompanies small population size. Evidence for Muller's Ratchet and knowledge on its underlying molecular mechanisms, however, are lacking for natural populations.

Results: We characterized mitochondrial genome evolutionary processes in Caenorhabditis briggsae natural isolates to show that numerous lineages experience a high incidence of nonsynonymous substitutions in protein-coding genes and accumulate unusual deleterious noncoding DNA stretches with associated heteroplasmic function-disrupting genome deletions. Isolate-specific deletion proportions correlated negatively with nematode fecundity, suggesting that these deletions might negatively affect C. briggsae fitness. However, putative compensatory mutations were also observed that are predicted to reduce heteroplasmy levels of deleterious deletions. Paradoxically, compensatory mutations were observed in one major intraspecific C. briggsae clade where population sizes are estimated to be very small (and selection is predicted to be relatively weak), but not in a second major clade where population size estimates are much larger and selection is expected to be more efficient.

Conclusion: This study provides evidence that the mitochondrial genomes of animals evolving in nature are susceptible to Muller's Ratchet, suggests that context-dependent compensatory mutations can accumulate in small populations, and predicts that Muller's Ratchet can affect fundamental evolutionary forces such as the rate of mutation.

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Evolutionary origins of ψND5 elements. Intraspecific phylogeny of C. briggsae natural isolates based on neighbor-joining analysis of mtDNA sequences is shown. Neighbor-joining and maximum parsimony analyses of nearly complete mtDNA sequences yielded trees with identical topologies. GL indicates the global intraspecific C. briggsae superclade; KE indicates the Kenya clade; TE and TR indicate the temperate and tropical subclades of GL, respectively. Bootstrap support of 100% for both analysis approaches was observed for all selected nodes indicated by asterisks – for the node supporting monophyly of C. briggsae and Caenorhabditis sp. n. 5, neighbor-joining values are on top of maximum parsimony values. The scale bar represents 0.01 substitutions per site. Bolts indicate branches where ψND5 elements are predicted to have originated based on the phylogeny and the presence of ψND5-1 and ψND5-2 in specific Caenorhabditis species and strains. The distributions of isolates into temperate and tropical clades in our analyses were consistent with their distributions based on previous analyses of nuclear loci [17].
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Figure 2: Evolutionary origins of ψND5 elements. Intraspecific phylogeny of C. briggsae natural isolates based on neighbor-joining analysis of mtDNA sequences is shown. Neighbor-joining and maximum parsimony analyses of nearly complete mtDNA sequences yielded trees with identical topologies. GL indicates the global intraspecific C. briggsae superclade; KE indicates the Kenya clade; TE and TR indicate the temperate and tropical subclades of GL, respectively. Bootstrap support of 100% for both analysis approaches was observed for all selected nodes indicated by asterisks – for the node supporting monophyly of C. briggsae and Caenorhabditis sp. n. 5, neighbor-joining values are on top of maximum parsimony values. The scale bar represents 0.01 substitutions per site. Bolts indicate branches where ψND5 elements are predicted to have originated based on the phylogeny and the presence of ψND5-1 and ψND5-2 in specific Caenorhabditis species and strains. The distributions of isolates into temperate and tropical clades in our analyses were consistent with their distributions based on previous analyses of nuclear loci [17].

Mentions: To investigate the evolutionary relationships of C. briggsae natural isolate hermaphrodite lineages and the origins of ψND5-1 and ψND5-2, we subjected the mtDNA sequences to phylogenetic analyses using MEGA4 [23]. Mitochondrial genome sequences from C. elegans (accession # NC_001328), Caenorhabditis remanei (W. K. Thomas, unpublished data) and Caenorhabditis sp. n. 5 (a recently-discovered gonochoristic sister species to C. briggsae – sequences collected here for isolate JU727) were used as outgroups. All mtDNA sequences were used for phylogenetic analyses, with the exception of ψND5-1 and ψND5-2 regions since determining their origins was one aim of the phylogenetic studies. Maximum parsimony and neighbor-joining analyses yielded trees with identical topologies. The phylogenies revealed the presence of three major, well-supported intraspecific C. briggsae clades that we refer to as the temperate, tropical and Kenya clades (Figure 2). The temperate and tropical clades form a monophyletic superclade, referred to as the global superclade, to the exclusion of the divergent Kenya clade. The phylogenetic distributions of isolates into these clades are highly congruent with previous phylogenetic analyses based on nuclear intron and protein-coding gene sequences [17]. The absence of ψND5-2 in the mitochondrial genomes of the two Kenya clade C. briggsae isolates and other Caenorhabditis species suggests that this element originated in the lineage leading to the C. briggsae global superclade. The presence of ψND5-1 in all C. briggsae isolates and Caenorhabditis sp. n. 5, but not other Caenorhabditis species, suggests that this element originated in the common ancestor of C. briggsae and Caenorhabditis sp. n. 5 (Figure 2).


Muller's Ratchet and compensatory mutation in Caenorhabditis briggsae mitochondrial genome evolution.

Howe DK, Denver DR - BMC Evol. Biol. (2008)

Evolutionary origins of ψND5 elements. Intraspecific phylogeny of C. briggsae natural isolates based on neighbor-joining analysis of mtDNA sequences is shown. Neighbor-joining and maximum parsimony analyses of nearly complete mtDNA sequences yielded trees with identical topologies. GL indicates the global intraspecific C. briggsae superclade; KE indicates the Kenya clade; TE and TR indicate the temperate and tropical subclades of GL, respectively. Bootstrap support of 100% for both analysis approaches was observed for all selected nodes indicated by asterisks – for the node supporting monophyly of C. briggsae and Caenorhabditis sp. n. 5, neighbor-joining values are on top of maximum parsimony values. The scale bar represents 0.01 substitutions per site. Bolts indicate branches where ψND5 elements are predicted to have originated based on the phylogeny and the presence of ψND5-1 and ψND5-2 in specific Caenorhabditis species and strains. The distributions of isolates into temperate and tropical clades in our analyses were consistent with their distributions based on previous analyses of nuclear loci [17].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2279117&req=5

Figure 2: Evolutionary origins of ψND5 elements. Intraspecific phylogeny of C. briggsae natural isolates based on neighbor-joining analysis of mtDNA sequences is shown. Neighbor-joining and maximum parsimony analyses of nearly complete mtDNA sequences yielded trees with identical topologies. GL indicates the global intraspecific C. briggsae superclade; KE indicates the Kenya clade; TE and TR indicate the temperate and tropical subclades of GL, respectively. Bootstrap support of 100% for both analysis approaches was observed for all selected nodes indicated by asterisks – for the node supporting monophyly of C. briggsae and Caenorhabditis sp. n. 5, neighbor-joining values are on top of maximum parsimony values. The scale bar represents 0.01 substitutions per site. Bolts indicate branches where ψND5 elements are predicted to have originated based on the phylogeny and the presence of ψND5-1 and ψND5-2 in specific Caenorhabditis species and strains. The distributions of isolates into temperate and tropical clades in our analyses were consistent with their distributions based on previous analyses of nuclear loci [17].
Mentions: To investigate the evolutionary relationships of C. briggsae natural isolate hermaphrodite lineages and the origins of ψND5-1 and ψND5-2, we subjected the mtDNA sequences to phylogenetic analyses using MEGA4 [23]. Mitochondrial genome sequences from C. elegans (accession # NC_001328), Caenorhabditis remanei (W. K. Thomas, unpublished data) and Caenorhabditis sp. n. 5 (a recently-discovered gonochoristic sister species to C. briggsae – sequences collected here for isolate JU727) were used as outgroups. All mtDNA sequences were used for phylogenetic analyses, with the exception of ψND5-1 and ψND5-2 regions since determining their origins was one aim of the phylogenetic studies. Maximum parsimony and neighbor-joining analyses yielded trees with identical topologies. The phylogenies revealed the presence of three major, well-supported intraspecific C. briggsae clades that we refer to as the temperate, tropical and Kenya clades (Figure 2). The temperate and tropical clades form a monophyletic superclade, referred to as the global superclade, to the exclusion of the divergent Kenya clade. The phylogenetic distributions of isolates into these clades are highly congruent with previous phylogenetic analyses based on nuclear intron and protein-coding gene sequences [17]. The absence of ψND5-2 in the mitochondrial genomes of the two Kenya clade C. briggsae isolates and other Caenorhabditis species suggests that this element originated in the lineage leading to the C. briggsae global superclade. The presence of ψND5-1 in all C. briggsae isolates and Caenorhabditis sp. n. 5, but not other Caenorhabditis species, suggests that this element originated in the common ancestor of C. briggsae and Caenorhabditis sp. n. 5 (Figure 2).

Bottom Line: However, putative compensatory mutations were also observed that are predicted to reduce heteroplasmy levels of deleterious deletions.Paradoxically, compensatory mutations were observed in one major intraspecific C. briggsae clade where population sizes are estimated to be very small (and selection is predicted to be relatively weak), but not in a second major clade where population size estimates are much larger and selection is expected to be more efficient.This study provides evidence that the mitochondrial genomes of animals evolving in nature are susceptible to Muller's Ratchet, suggests that context-dependent compensatory mutations can accumulate in small populations, and predicts that Muller's Ratchet can affect fundamental evolutionary forces such as the rate of mutation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, 97331, USA. howed@science.oregonstate.edu

ABSTRACT

Background: The theory of Muller' Ratchet predicts that small asexual populations are doomed to accumulate ever-increasing deleterious mutation loads as a consequence of the magnified power of genetic drift and mutation that accompanies small population size. Evidence for Muller's Ratchet and knowledge on its underlying molecular mechanisms, however, are lacking for natural populations.

Results: We characterized mitochondrial genome evolutionary processes in Caenorhabditis briggsae natural isolates to show that numerous lineages experience a high incidence of nonsynonymous substitutions in protein-coding genes and accumulate unusual deleterious noncoding DNA stretches with associated heteroplasmic function-disrupting genome deletions. Isolate-specific deletion proportions correlated negatively with nematode fecundity, suggesting that these deletions might negatively affect C. briggsae fitness. However, putative compensatory mutations were also observed that are predicted to reduce heteroplasmy levels of deleterious deletions. Paradoxically, compensatory mutations were observed in one major intraspecific C. briggsae clade where population sizes are estimated to be very small (and selection is predicted to be relatively weak), but not in a second major clade where population size estimates are much larger and selection is expected to be more efficient.

Conclusion: This study provides evidence that the mitochondrial genomes of animals evolving in nature are susceptible to Muller's Ratchet, suggests that context-dependent compensatory mutations can accumulate in small populations, and predicts that Muller's Ratchet can affect fundamental evolutionary forces such as the rate of mutation.

Show MeSH
Related in: MedlinePlus