Did Genetic Drift Drive Increases in Genome Complexity?
Kenneth D. Whitney1*, Theodore Garland Jr2
1 Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas, United States of America, 2 Department of Biology, University of California Riverside, Riverside, California, United States of America
Abstract
Mechanisms underlying the dramatic patterns of genome size variation across the tree of life remain mysterious. Effective population size (Ne) has been proposed as a major driver of genome size: selection is expected to efficiently weed out deleterious mutations increasing genome size in lineages with large (but not small) Ne. Strong support for this model was claimed from a comparative analysis of Neu and genome size for ≈30 phylogenetically diverse species ranging from bacteria to vertebrates, but analyses at that scale have so far failed to account for phylogenetic nonindependence of species. In our reanalysis, accounting for phylogenetic history substantially altered the perceived strength of the relationship between Neu and genomic attributes: there were no statistically significant associations betweenNeu and gene number, intron size, intron number, the half-life of gene duplicates, transposon number, transposons as a fraction of the genome, or overall genome size. We conclude that current datasets do not support the hypothesis of a mechanistic connection between Ne and these genomic attributes, and we suggest that further progress requires larger datasets, phylogenetic comparative methods, more robust estimators of genetic drift, and a multivariate approach that accounts for correlations between putative explanatory variables.
Author Summary
Genome size (the amount of nuclear DNA) varies tremendously across organisms but is not necessarily correlated with organismal complexity. For example, genome sizes just within the grasses vary nearly 20-fold, but large-genomed grass species are not obviously more complex in terms of morphology or physiology than are the small-genomed species. Recent explanations for genome size variation have instead been dominated by the idea that population size determines genome size: mutations that increase genome size are expected to drift to fixation in species with small populations, but such mutations would be eliminated in species with large populations where natural selection operates at higher efficiency. However, inferences from previous analyses are limited because they fail to recognize that species share evolutionary histories and thus are not necessarily statistically independent. Our analysis takes a phylogenetic perspective and, contrary to previous studies, finds no evidence that genome size or any of its components (e.g., transposon number, intron number) are related to population size. We suggest that genome size evolution is unlikely to be neatly explained by a single factor such as population size.
Citation: Whitney KD, Garland T Jr (2010) Did Genetic Drift Drive Increases in Genome Complexity?
PLoS Genet 6(8): e1001080. doi:10.1371/journal.pgen.1001080
Editor: Nancy A. Moran, Yale University, United States of America
Received: March 15, 2010; Accepted: July 22, 2010; Published: August 26, 2010
Copyright: © 2010 Whitney, Garland. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: KDW was supported by NSF DEB-0716868 and TG was supported in part by NSF DEB-0416085. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: kwhitney@rice.edu
+++++
