Abstract
We have analyzed natural variation in mitochondrial form and function among a set of Caenorhabditis briggsae isolates known to harbor mitochondrial DNA structural variation in the form of a heteroplasmic nad5 gene deletion (nad5Δ) that correlates negatively with organismal fitness. We performed in vivo quantification of 24 mitochondrial phenotypes including reactive oxygen species level, membrane potential, and aspects of organelle morphology, and observed significant among-isolate variation in 18 traits. Although several mitochondrial phenotypes were non-linearly associated with nad5Δ levels, most of the among-isolate phenotypic variation could be accounted for by phylogeographic clade membership. In particular, isolate-specific mitochondrial membrane potential was an excellent predictor of clade membership. We interpret this result in light of recent evidence for local adaptation to temperature in C. briggsae. Analysis of mitochondrial-nuclear hybrid strains provided support for both mtDNA and nuclear genetic variation as drivers of natural mitochondrial phenotype variation. This study demonstrates that multicellular eukaryotic species are capable of extensive natural variation in organellar phenotypes and highlights the potential of integrating evolutionary and cell biology perspectives.
Highlights
Mitochondria are organelles that harbor DNA and produce most of the energy required to sustain eukaryotic life via an electron transport chain (ETC)
Among-isolate variation in nad5 gene deletion (nad5D) heteroplasmy level is controlled by the presence of compensatory sequences within the mitochondrial DNA (mtDNA) of certain isolates [47], which appear to place an upper bound on the proportion of nad5D-deletion bearing genomes able to accrue within individuals [52]. nad5D was recently shown to behave as a selfish genetic element that increases in frequency when C. briggsae isolates are maintained by singleindividual bottlenecking [48]; nad5D heteroplasmy level is stably maintained across generations when isolates are maintained in larger population sizes (N,100) where natural selection is more efficient (Estes, Coleman-Hulbert, Howe, and Denver, unpubl. data)
We have reported a novel analysis of subcellular processes in C. briggsae that, to our knowledge, provides the first explicit treatment of within-species natural variation in form and function of an organelle
Summary
Mitochondria are organelles that harbor DNA and produce most of the energy required to sustain eukaryotic life via an electron transport chain (ETC). Mutations affecting ETC genes can have a variety of detrimental consequences that manifest at cellular, tissue, and whole organism levels [1,2], and have been implicated in many complex human diseases [3,4,5,6]. Proximal effects of ETC mutations include altering mitochondrial reactive oxygen species (ROS) production [7,8], membrane potential (DYM) [8,9,10,11], and other aspects of mitochondrial physiology. ROS are generated by the ETC as a byproduct of oxidative phosphorylation and are of particular interest because, when present at high levels, they can damage cellular macromolecules including mitochondrial and nuclear DNA and the components of the ETC itself [12]. Selection on ETC-dependent mitochondrial traits has been implicated in the evolution and diversification of life-history traits [13,14], thermal tolerance [15,16,17], aging [18], reinforcement and allopatric speciation [19,20,21,22,23,24]
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