Hemizygosity Enhances Purifying Selection: Lack of Fast-Z Evolution in Two Satyrine Butterflies

Abstract

The fixation probability of a recessive beneficial mutation is increased on the X or Z chromosome, relative to autosomes, because recessive alleles carried by X or Z are exposed to selection in the heterogametic sex. This leads to an increased dN/dS ratio on sex chromosomes relative to autosomes, a pattern called the "fast-X" or "fast-Z" effect. Besides positive selection, the strength of genetic drift and the efficacy of purifying selection, which affect the rate of molecular evolution, might differ between sex chromosomes and autosomes. Disentangling the complex effects of these distinct forces requires the genome-wide analysis of polymorphism, divergence and gene expression data in a variety of taxa. Here we study the influence of hemizygosity of the Z chromosome in Maniola jurtina and Pyronia tithonus, two species of butterflies (Lepidoptera, Nymphalidae, Satyrinae). Using transcriptome data, we compare the strength of positive and negative selection between Z and autosomes accounting for sex-specific gene expression. We show that M. jurtina and P. tithonus do not experience a faster, but rather a slightly slower evolutionary rate on the Z than on autosomes. Our analysis failed to detect a significant difference in adaptive evolutionary rate between Z and autosomes, but comparison of male-biased, unbiased and female-biased Z-linked genes revealed an increased efficacy of purifying selection against recessive deleterious mutations in female-biased Z-linked genes. This probably contributes to the lack of fast-Z evolution of satyrines. We suggest that the effect of hemizygosity on the fate of recessive deleterious mutations should be taken into account when interpreting patterns of molecular evolution in sex chromosomes vs. autosomes.

Keywords: Lepidoptera; Nymphalidae; fast-Z effect; sex-biased expression; sex-chromosome evolution; transcriptomics.

Fig. 1.—

Distribution of the dN/dS ratio obtained by resampling without replacement of 90 autosomal pairwise alignments (1000 replicates). dN/dS ratio of the Z-linked pairwise alignments is indicated in red.

Fig. 2.—

Distribution of the π_n/π_s ratio obtained by resampling without replacement of 151 and 144 autosomal genes (1000 replicates). π_n/π_s ratio of the Z-linked genes are indicated in red. (A) M. jurtina and (B) P. tithonus.

Fig. 3.—

π_n/π_s ratios of Z-linked genes of the following categories: female-biased expression, unbiased expression and male-biased expression. Error bars represent ninety-five percent confidence intervals obtained by bootstrapping genes (1000 replicates). (A) M. jurtina and (B): P. tithonus.

Fig. 4.—

Distribution of α, ω_a, and ω_na obtained by resampling without replacement 90 autosomal genes (1000 replicates). α, ω_a, and ω_na values of the Z-linked genes (obtained with 90 genes for divergence and 151 and 144 genes for polymorphism for M. jurtina and P. tithonus, respectively) are indicated in red. (a) α in M. jurtina, (b) ω_a in M. jurtina, (c) ω_na in M. jurtina, (d) α in P. tithonus, (e) ω_a in P. tithonus, and (f) ω_na in P. tithonus.