Global Dosage Compensation Is Ubiquitous in Lepidoptera, but Counteracted by the Masculinization of the Z Chromosome

Abstract

While chromosome-wide dosage compensation of the X chromosome has been found in many species, studies in ZW clades have indicated that compensation of the Z is more localized and/or incomplete. In the ZW Lepidoptera, some species show complete compensation of the Z chromosome, while others lack full equalization, but what drives these inconsistencies is unclear. Here, we compare patterns of male and female gene expression on the Z chromosome of two closely related butterfly species, Papilio xuthus and Papilio machaon, and in multiple tissues of two moths species, Plodia interpunctella and Bombyx mori, which were previously found to differ in the extent to which they equalize Z-linked gene expression between the sexes. We find that, while some species and tissues seem to have incomplete dosage compensation, this is in fact due to the accumulation of male-biased genes and the depletion of female-biased genes on the Z chromosome. Once this is accounted for, the Z chromosome is fully compensated in all four species, through the up-regulation of Z expression in females and in some cases additional down-regulation in males. We further find that both sex-biased genes and Z-linked genes have increased rates of expression divergence in this clade, and that this can lead to fast shifts in patterns of gene expression even between closely related species. Taken together, these results show that the uneven distribution of sex-biased genes on sex chromosomes can confound conclusions about dosage compensation and that Z chromosome-wide dosage compensation is not only possible but ubiquitous among Lepidoptera.

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

“…It has been recently shown that, like in other taxa, sex-biased genes can experience rapid turnovers in butterflies (e.g., Papilio) (Huylmans et al, 2017 (Kozak et al, 2015) compared to 35MYA for P. xuthus and P. machaon (Zakharov, Caterino, & Sperling, 2004). Regardless, any gene that is sex biased in H. erato but not in H. melpomene is categorized as unbiased in our data.…”

“…It has been recently shown that, like in other taxa, sex‐biased genes can experience rapid turnovers in butterflies (e.g., Papilio ) (Huylmans et al., ). Consequently, it is possible for H. melpomene and H. erato to have different sex‐biased genes.…”

“…Heliconius males, expression of Z genes is reduced below autosomal levels, but this dosage compensation mechanism is imperfect, with males showing increased expression relative to females on Z chromosome genes (Walters et al, 2015). However, the apparent incomplete dosage compensation could be a consequence of an uneven distribution of sex-biased genes on sex chromosomes (Gu & Walters, 2017, Huylmans, Macon, & Vicoso, 2017. Regardless, when we compare rates of divergence and adaptation for genes with sex-biased expression, the expectations of fast-Z evolution are not clearly met.…”

RADSex: a computational workflow to study sex determination using Restriction Site-Associated DNA Sequencing data

“…These findings have spawned both theoretical and empirical interest in sex chromosomes as models to study the consequences of recombination suppression and associated processes (Bachtrog, 2008;Charlesworth & Charlesworth, 2000;Corcoran et al, 2016;Doorn & Kirkpatrick, 2007; L. Gu, Walters, & Knipple, 2017;Huylmans, Macon, & Vicoso, 2017;Muyle et al, 2012;Peichel et al, 2004) . More recent studies investigating sex chromosomes in insects (Blackmon, Ross, & Bachtrog, 2017) , non-avian reptilia (Modi & Crews, 2005) , amphibians (Miura, 2017) , and fishes (Kikuchi & Hamaguchi, 2013) have found many homomorphic sex chromosomes displaying varying levels of differentiation, with the extreme case of a sex locus restricted to allelic variation of a single nucleotide as reported in the Japanese pufferfish (Kamiya et al, 2012) .…”

Sexually dimorphic gene expression and transcriptome evolution provides mixed evidence for a fast-Z effect inHeliconius

“…In Heliconius males expression of Z genes is reduced below autosomal levels, but this dosage compensation mechanism is imperfect, with males showing increased expression relative to females on the Z chromosome (Walters et al ., 2015). However, alternative processes, such as the masculinization of the Z chromosome, may explain the apparent lack of complete dosage compensation (Gu & Walters, 2017, Huylmans et al . 2017).…”