Less effective selection leads to larger genomes

  1. Christophe Jean Douady1,5
  1. 1Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5023, ENTPE, Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés, F-69622 Villeurbanne, France;
  2. 2Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne, France;
  3. 3Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5310, INSERM, Institut NeuroMyoGène, F-69622 Villeurbanne, France;
  4. 4Center for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
  5. 5Institut Universitaire de France, F-75005 Paris, France;
  6. 6Université de Toulouse, University Paul Sabatier (UPS), CNRS UMR 5288, Laboratoire AMIS, F-31073 Toulouse, France
  1. Corresponding author: Tristan.Lefebure{at}univ-lyon1.fr

Abstract

The evolutionary origin of the striking genome size variations found in eukaryotes remains enigmatic. The effective size of populations, by controlling selection efficacy, is expected to be a key parameter underlying genome size evolution. However, this hypothesis has proved difficult to investigate using empirical data sets. Here, we tested this hypothesis using 22 de novo transcriptomes and low-coverage genomes of asellid isopods, which represent 11 independent habitat shifts from surface water to resource-poor groundwater. We show that these habitat shifts are associated with higher transcriptome-wide Formula. After ruling out the role of positive selection and pseudogenization, we show that these transcriptome-wide Formula increases are the consequence of a reduction in selection efficacy imposed by the smaller effective population size of subterranean species. This reduction is paralleled by an important increase in genome size (25% increase on average), an increase also confirmed in subterranean decapods and mollusks. We also control for an adaptive impact of genome size on life history traits but find no correlation between body size, or growth rate, and genome size. We show instead that the independent increases in genome size measured in subterranean isopods are the direct consequence of increasing invasion rates by repeat elements, which are less efficiently purged out by purifying selection. Contrary to selection efficacy, polymorphism is not correlated to genome size. We propose that recent demographic fluctuations and the difficulty of observing polymorphism variation in polymorphism-poor species can obfuscate the link between effective population size and genome size when polymorphism data are used alone.

Footnotes

  • Received July 8, 2016.
  • Accepted March 30, 2017.

This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

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