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Evolution of a mitochondrial VNTR: Population patterns and mutational dynamics in Schistosoma mansoni

Authors
Publisher
Purdue University
Publication Date
Keywords
  • Biology
  • Ecology|Biology
  • Genetics|Biology
  • Zoology

Abstract

The mitochondrial chromosome of Schistosoma mansoni carries an unstable mtVNTR, pSM750, which contributes a large amount of length polymorphism to the mtDNA of this organism. The evolution of this repetitive sequence has the potential to be affected by selection upon total mtDNA size or selection specifically upon the length of the tandem array itself. Replication slippage has previously been hypothesized to affect mtVNTRs, which predicts that the mutation process should be biased toward production of larger tandem arrays. This mechanism also predicts that mutation rate should be positively dependent upon tandem array length. Ultimately, this mtVNTR has potential to exhibit a self-reinforcing mutational process that acts in opposition to length constraint. Thus, pSM750 was studied with respect to tandem array length and heteroplasmy at different time scales. Genetically independent population samples from recent field isolates and laboratory strains demonstrated that, over decades, length and heteroplasmy have diverged in a manner suggesting differential length constraints between natural and laboratory conditions. Clonal cohorts derived from monomiracidial snail infections supported positive length dependence of the mutational process, as did a multi-generational study in which founder populations with different sets of haplotypes were followed over time. Inheritance of pSM750 haplotypes within the multi-generational experiments demonstrated clearly that paternal mitochondria sometimes invade zygotes and subsequently persist for generations. This represents an unprecedented breakdown of the normal mechanisms that prevent biparental inheritance of organelles in most eukaryotes. Nevertheless, high instability of the mtVNTR also results in frequent size homoplasy among parental and offspring haplotype sets, and this phenomenon was demonstrated separately from paternal inheritance of mitochondria. Mutation rates for mtVNTR systems are often high relative to rates of drift. Therefore, an analysis was conducted to determine the effect of heteroplasmy per se on the resolution of population structure. A simple model indicates that, as heteroplasmy increases to values well within the range of empirical observation among species, mtVNTRs will lose ability to resolve population structure. ^

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