Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

Abstract

Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA from male and female whole abdomens and sequence female ovary and gut tissue to identify sex‐ and tissue‐specific gene expression profiles in H. melpomene. Using these expression profiles, we compare (a) sequence divergence and polymorphism; (b) the strength of positive and negative selection; and (c) rates of adaptive evolution, for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato. We show that the rate of adaptive substitutions is higher for Z than autosomal genes, but contrary to expectation, it is also higher for male‐biased than female‐biased genes. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic‐specific tissue. Our results contribute to a growing body of literature from other ZW systems that also provide mixed evidence for a fast‐Z effect where hemizygosity influences the rate of adaptive substitutions.

Absence of a faster-X effect in beetles (Tribolium, Coleoptera)

“…We suggest that this may give rise to weak phenotypic effects of such genes [1], potentially limiting fixation of recessive beneficial mutations when transcribed in male gonads, thereby impeding a faster-X effect. Our results thus provide additional empirical support [7, 14] for a notion that has previously been proposed theoretically [1, 2, 7, 22]. Taken together, we propose that the unusual absence of a faster-X effect in these beetles may be influenced by two major phenomena: (1) the accumulation of highly constrained ovary-biased genes on the X-chromosome, and (2) the lack of dosage compensation in the male gonads, which may act to minimize fixation of recessive beneficial mutations of genes transcribed in these tissues.…”

“…However, the prediction of higher dN/dS for female-biased genes on the Z-chromosome was not met in this study, suggesting that the faster-Z in these birds was not due to fixation of recessive beneficial mutations, and rather might be attributable to fixation of neutral or slightly deleterious mutations via genetic drift [7, 16]. Recently, similar results were reported for the W/Z chromosomes of Heliconius butterflies [14]. At present however, the study of the faster-X effect, including the role of sex-biased gene expression, remains limited to just a few model organisms, and the putative underlying mechanisms appear to be variable.…”

“…1B). Thus, the X/A dN/dS (all genes) value is considerably below 1, a result opposite to the >1 value expected under a faster-X effect [4, 14-16, 21]. Further, the mean dN/dS on the X-chromosome was about half (ratio of 0.54) that observed on autosomes (Fig.…”

“…In other organisms, however, a faster-X effect is more ambiguous. For example, signals of this effect have sometimes, but not always, been observed in studies of fruit flies [2, 11, 12], and variable results on the presence or strength of the faster-X effect have been reported in butterflies [13, 14].…”

“…This could make beneficial mutations exposed on the single male X-chromosome unlikely to be fixed any more frequently than they would be if they were autosomal, possibly resulting in evolutionary rates of X-linked genes that are not significantly faster than those of autosomal genes [1, 7]. Support for the notion that dosage compensation may impact the rates of X-(or Z-) linked gene evolution is provided by the observation that certain butterflies display incomplete dosage compensation [24]; this correlates with, and thus may contribute towards, the observed lack of an elevated faster-Z effect in female-biased genes in those organisms [14, 24]. Similar patterns have been described in birds [7].…”