Dataset Information

Mitochondrial-Nuclear Epistasis Impacts Fitness and Mitochondrial Physiology of Interpopulation Caenorhabditis briggsae Hybrids.

ABSTRACT: In order to identify the earliest genetic changes that precipitate species formation, it is useful to study genetic incompatibilities that cause only mild dysfunction when incompatible alleles are combined in an interpopulation hybrid. Such hybridization within the nematode species Caenorhabditis briggsae has been suggested to result in selection against certain combinations of nuclear and mitochondrial alleles, raising the possibility that mitochondrial-nuclear (mitonuclear) epistasis reduces hybrid fitness. To test this hypothesis, cytoplasmic-nuclear hybrids (cybrids) were created to purposefully disrupt any epistatic interactions. Experimental analysis of the cybrids suggests that mitonuclear discord can result in decreased fecundity, increased lipid content, and increased mitochondrial reactive oxygen species levels. Many of these effects were asymmetric with respect to cross direction, as expected if cytoplasmic-nuclear Dobzhansky-Muller incompatibilities exist. One such effect is consistent with the interpretation that disrupting coevolved mitochondrial and nuclear loci impacts mitochondrial function and organismal fitness. These findings enhance efforts to study the genesis, identity, and maintenance of genetic incompatibilities that precipitate the speciation process.

SUBMITTER: Chang CC

PROVIDER: S-EPMC4704720 | biostudies-literature | 2015 Nov

REPOSITORIES: biostudies-literature

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Mitochondrial-Nuclear Epistasis Impacts Fitness and Mitochondrial Physiology of Interpopulation Caenorhabditis briggsae Hybrids.

Chang Chih-Chiun CC Rodriguez Joel J Ross Joseph J

G3 (Bethesda, Md.) 20151119 1

In order to identify the earliest genetic changes that precipitate species formation, it is useful to study genetic incompatibilities that cause only mild dysfunction when incompatible alleles are combined in an interpopulation hybrid. Such hybridization within the nematode species Caenorhabditis briggsae has been suggested to result in selection against certain combinations of nuclear and mitochondrial alleles, raising the possibility that mitochondrial-nuclear (mitonuclear) epistasis reduces h ...[more]

PMID: 26585825

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Project description:Although most metazoan mitochondrial genomes are highly streamlined and encode little noncoding DNA outside of the "AT" region, the accumulation of mitochondrial pseudogenes and other types of noncoding DNA has been observed in a growing number of animal groups. The nematode species Caenorhabditis briggsae harbors two mitochondrial DNA (mtDNA) pseudogenes, named Psinad5-1 and Psinad5-2, presumably derived from the nad5 protein-coding gene. Here, we provide an in-depth analysis of mtDNA pseudogene evolution in C. briggsae natural isolates and related Caenorhabditis species. Mapping the observed presence and absence of the pseudogenes onto phylogenies suggests that Psinad5-1 originated in the ancestor to C. briggsae and its recently discovered outcrossing relative species Caenorhabditis sp. 5 and Caenorhabditis sp. 9. However, Psinad5-1 was not detected in Caenorhabditis sp. 9 natural isolates, suggesting a lineage-specific loss of this pseudogene in this species. Our results corroborated the previous finding that Psinad5-2 originated within C. briggsae. The observed pattern of mitochondrial pseudogene gain and loss in Caenorhabditis was inconsistent with predictions of the tandem duplication-random loss model of mitochondrial genome evolution and suggests that intralineage recombination-like mechanisms might play a major role in Caenorhabditis mtDNA evolution. Natural variation was analyzed at the pseudogenes and flanking mtDNA sequences in 141 geographically diverse C. briggsae natural isolates. Although phylogenetic analysis placed the majority of isolates into the three previously established major intraspecific clades of C. briggsae, two new and unexpected haplotypes fell outside of these conventional groupings. Psinad5-2 copy number variation was observed among C. briggsae isolates collected from the same geographic site. Patterns of nucleotide diversity were analyzed in Psinad5-1 and Psinad5-2, and confidence intervals were found to overlap values from synonymous sites in protein-coding genes, consistent with neutral expectations. Our findings provide new insights into the mode and tempo of mitochondrial genome and pseudogene evolution both within and between Caenorhabditis nematode species.

Dataset Information

Mitochondrial-Nuclear Epistasis Impacts Fitness and Mitochondrial Physiology of Interpopulation Caenorhabditis briggsae Hybrids.

Publications

Mitochondrial-Nuclear Epistasis Impacts Fitness and Mitochondrial Physiology of Interpopulation Caenorhabditis briggsae Hybrids.

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