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Article
Selfish Mitochondrial DNA Proliferates and Diversifies in Small, but not Large, Experimental Populations of Caenorhabditis briggsae
Genome Biology and Evolution
  • Wendy S. Phillips, Oregon State University
  • Anna Luella Coleman-Hulbert, Portland State University
  • Emily S. Weiss, Oregon State University
  • Dana K. Howe, Oregon State University
  • Sita Ping, Oregon State University
  • Riana I. Wernick, Oregon State University
  • Suzanne Estes, Portland State University
  • Dee R. Denver, Oregon State University
Document Type
Article
Publication Date
6-1-2015
Subjects
  • Evolution (Biology),
  • Mitochondrial DNA,
  • Nematodes
Disciplines
Abstract

Evolutionary interactions across levels of biological organization contribute to a variety of fundamental processes including genome evolution, reproductive mode transitions, species diversification, and extinction. Evolutionary theory predicts that so-called “selfish” genetic elements will proliferate when the host effective population size (Ne) is small, but direct tests of this prediction remain few. We analyzed the evolutionary dynamics of deletion-containing mitochondrial DNA (ΔmtDNA) molecules, previously characterized as selfish elements, in six different natural strains of the nematode Caenorhabditis briggsae allowed to undergo experimental evolution in a range of population sizes (N = 1, 10, 100, and 1,000) for a maximum of 50 generations. Mitochondrial DNA (mtDNA) was analyzed for replicate lineages at each five-generation time point. Ten different ΔmtDNA molecule types were observed and characterized across generations in the experimental populations. Consistent with predictions from evolutionary theory, lab lines evolved in small-population sizes (e.g., nematode N = 1) were more susceptible to accumulation of high levels of preexisting mtDNA compared with those evolved in larger populations. New ΔmtDNA elements were observed to increase in frequency and persist across time points, but almost exclusively at small population sizes. In some cases, mtDNA levels decreased across generations when population size was large (nematode N = 1,000). Different natural strains of C. briggsae varied in their susceptibilities to mtDNA accumulation, owing in part to preexisting compensatory mtDNA alleles in some strains that prevent deletion formation. This analysis directly demonstrates that the evolutionary trajectories of ΔmtDNA elements depend upon the population-genetic environments and molecular-genetic features of their hosts.

Description

This is the publisher’s final pdf. The published article is copyrighted by the author(s) and published by Oxford University Press for the Society for Molecular Biology and Evolution. The published article can be found at: http://gbe.oxfordjournals.org/

This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Data deposition: New DNA sequences have been deposited at GenBank under accession numbers KR185945–KR185961. The Illumina data were archived with the NCBI Short Read Archive under accession numbers SRX1014084 and SRX1014093.

DOI
10.1093/gbe/evv116
Persistent Identifier
http://archives.pdx.edu/ds/psu/16083
Citation Information
Phillips, W. S., Coleman-Hulbert, A. L., Weiss, E. S., Howe, D. K., Ping, S., Wernick, R. I., … Denver, D. R. (2015). Selfish Mitochondrial DNA Proliferates and Diversifies in Small, but not Large, Experimental Populations of Caenorhabditis briggsae. Genome Biology and Evolution, 7(7), 2023–37.