Multilayered Tuning of Dosage Compensation and Z-Chromosome Masculinization in the Wood White (Leptidea sinapis) Butterfly

Abstract

In species with genetic sex determination, dosage compensation can evolve to equal expression levels of sex-linked and autosomal genes. Current knowledge about dosage compensation has mainly been derived from male-heterogametic (XX/XY) model organisms, whereas less is understood about the process in female-heterogametic systems (ZZ/ZW). In moths and butterflies, downregulation of Z-linked expression in males (ZZ) to match the expression level in females (ZW) is often observed. However, little is known about the underlying regulatory mechanisms, or if dosage compensation patterns vary across ontogenetic stages. In this study, we assessed dynamics of Z-linked and autosomal expression levels across developmental stages in the wood white (Leptidea sinapis). We found that although expression of Z-linked genes in general was reduced compared with autosomal genes, dosage compensation was actually complete for some categories of genes, in particular sex-biased genes, but equalization in females was constrained to a narrower gene set. We also observed a noticeable convergence in Z-linked expression between males and females after correcting for sex-biased genes. Sex-biased expression increased successively across developmental stages, and male-biased genes were enriched on the Z-chromosome. Finally, all five core genes associated with the ribonucleoprotein dosage compensation complex male-specific lethal were detected in adult females, in correspondence with a reduction in the expression difference between autosomes and the single Z-chromosome. We show that tuning of gene dosage is multilayered in Lepidoptera and argue that expression balance across chromosomal classes may predominantly be driven by enrichment of male-biased genes on the Z-chromosome and cooption of available dosage regulators.

Host plant diet affects growth and induces altered gene expression and microbiome composition in the wood white (Leptidea sinapis) butterfly

“…The main factor affecting global expression profiles across all samples was developmental stage, whereas no effect of sex could be detected. This is in line with previous studies that found considerable differences in gene expression profiles between ontogenetic stages (Leal et al, 2018), but only a small proportion of sex-biased genes in the larval stages (Höök et al, 2019). We did not observe any obvious clustering by either population or host plant treatment, in contrast to other studies where different host plant use results in clearly distinguishable expression profiles (Celorio-Mancera et al, 2013).…”

“…Finally, fastq Screen (Wingett, 2017) with bowtie2 version 2.3.5 (Langmead & Salzberg, 2012) was used to identify and screen for contaminants. The most likely contaminants were identified based on previous gene expression studies in L. sinapis (Höök et al, 2019;Leal et al, 2018). The filtered data set was screened for contaminants of the following origin: rRNA, human, Drosophila…”

“…Filtered reads were indexed and mapped with star version 2.7.2b (Dobin et al, 2013), using previously available L. sinapis genome (Talla et al, 2017) and transcriptome (Höök et al, 2019;Leal et al, 2018) assemblies. Gene specific counts of mapped RNA-seq reads were obtained using stringtie version 1.3.6 (Pertea et al, 2015).…”

High-density linkage maps and chromosome level genome assemblies unveil direction and frequency of extensive structural rearrangements in wood white butterflies (Leptideaspp.)

“…sinapis (Höök et al, 2019), can therefore be a potential reason for the much more conserved Z chromosomes. The fact that the Z chromosome only recombines and spends relatively more time in male butterflies (Turner & Sheppard, 1975) should further strengthen this linkage.…”

“…The fact that the Z chromosome only recombines and spends relatively more time in male butterflies (Turner & Sheppard, 1975) should further strengthen this linkage. Translocation of genes from the sex chromosomes might also be selected against if it alters expression levels regulated by dosage compensation mechanisms, which has been observed in L. sinapis (Höök et al, 2019).…”