Less effective selection leads to larger genomes

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: see text] After ruling out the role of positive selection and pseudogenization, we show that these transcriptome-wide [Formula: see text] 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.

Figure 1.

Selection efficacy (d_N/d_S), polymorphism (${\hat{\theta }}_w$ and p_N/p_S), and haploid genome size measurements for 11 pairs of surface and subterranean asellid species. Vertical bars next to the tree indicate species pairs with their surface (black circles) and subterranean (white circles) species. Numbers along branches of the tree are the numbers of single-copy genes used to estimate the d_N/d_S. Color boxes indicate statistical support (P-value <0.05) in favor of (dark brown) or against (light brown) a decrease in selection efficacy or population size, or an increase in genome size in subterranean species. No box indicates no statistical differences between species of a pair. Error bars represent 95% bootstrap confidence intervals, except for genome size where it represents the range around the mean for five individuals. The percentage change from surface water to subterranean species is shown for each species pair.

Figure 2.

Variation in haploid genome size associated with the ecological transition from surface water to groundwater in 47 species, including isopods (top) and decapods and gastropods (bottom). The 18 independent pairs of surface and subterranean species are delimited with boxes. Legends as in Figure 1. Identical species names followed by locality names within brackets refer to cryptic species (Morvan et al. 2013).

Figure 3.

Repeatome size estimates and composition using low coverage genome sequencing. (A) Size of the non-repetitive genome (blue) and repeatome (orange) for the 22 species (tree symbols as in Figure 1). (B) Repeat family frequency spectrum. (C) Number of shared repeats between two species as a function of divergence time. Relationship between GS and repeatome size (D), the number of repeat families (E), and the total genomic size of the 10 biggest repeat families (F). In D, E, and F, surface (black circles) and subterranean (white circles) species of a pair are joined by a gray line.