Sex-Biased Gene Expression and Dosage Compensation on theArtemia franciscanaZ-Chromosome

Abstract

Males and females of Artemia franciscana , a crustacean commonly used in the aquarium trade, are highly dimorphic. Sex is determined by a pair of ZW chromosomes, but the nature and extent of differentiation of these chromosomes is unknown. Here, we characterize the Z chromosome by detecting genomic regions that show lower genomic coverage in female than in male samples, and regions that harbor an excess of female-specific SNPs. We detect many Z-specific genes, which no longer have homologs on the W, but also Z-linked genes that appear to have diverged very recently from their existing W-linked homolog. We assess patterns of male and female expression in two tissues with extensive morphological dimorphism, gonads, and heads. In agreement with their morphology, sex-biased expression is common in both tissues. Interestingly, the Z chromosome is not enriched for sex-biased genes, and seems to in fact have a mechanism of dosage compensation that leads to equal expression in males and in females. Both of these patterns are contrary to most ZW systems studied so far, making A. franciscana an excellent model for investigating the interplay between the evolution of sexual dimorphism and dosage compensation, as well as Z chromosome evolution in general.

How to identify sex chromosomes and their turnover

“…Due to noise in mapping reads to a genome, the male to female coverage ratio is typically a continuum, where there are two overlapping normal distributions of sex differences in coverage, one for the X or Z chromosome and the other for autosomal scaffolds (Figure a). Identifying the equidistant point between the maximum of these two peaks can help minimize the error in identifying sex‐linked regions, and has been employed successfully across a number of species (Huylmans, Toups, Macon, Gammerdinger, & Vicoso, ; Vicoso & Bachtrog, ). Lastly, the k ‐mer counting approach (Akagi, Henry, Tao, & Comai, ; Carvalho & Clark, ; Li et al, ; Morris, Darolti, Bloch, Wright, & Mank, ; Pucholt, Wright, Conze, Mank, & Berlin, ) is based on similar underlying principles.…”

“…Estimating the false positive rate using computational methods can be a complementary and alternative approach to validating sex-linked loci. Permutation tests that shuffle sex assignments among sampled individuals are essential for generating null distributions against which to assess the validity of candidate loci (Huylmans et al, 2019;Jeffries et al, 2018;Morris et al, 2018;Scharmann, Grafe, Metali, & Widmer, 2017;Wright et al, 2017). For example, in an XY system, identifying the number of loci conforming to ZW expectations is essential to estimate the false positive rate and distinguish true sex-linkage from stochastic noise.…”

“…Dosage compensation mechanisms are more frequently observed on XY relative to ZW chromosomes in the species studied so far (Gu & Walters, 2017;Mullon et al, 2015; Tables S1-S3), potentially leading to faster rates of Y chromosome decay. However, there have been several recent counter-examples to this trend (Hale, McKinney, Thrower, & Nichols, 2018;Huylmans et al, 2019), and as more sex chromosomes are identified it will be possible to test whether there is indeed a consistent relationship between dosage compensation status and sex chromosome system. Second, in several vertebrate and plant groups (Kirkpatrick & Hall, 2004;Whittle & Johnston, 2002), males have a higher mutation rate than females.…”

Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos

“…This implies that some genes are dosage sensitive (low heterozygote fitness or lethality) whereas others are less so. The lack of chromosome-wide dosage compensation and dosage balance has been documented in parasitic blood flukes, tonguefish, caenophidian snakes, birds, a trionychid turtle and the Komodo dragon, with lepidopteran insects and Artemia franciscana representing the only known exceptions here 6,11,15,16–18 and unpublished manuscript .…”

Hypersaline Lagoons from Chile, the Southern Edge of the World

“…With the advent of massive sequencing and transcriptomics, new information has been reported on the genetics of sex differentiation [54][55][56] and stress or adaptation-related genes [41]. A transcriptomic study in A. franciscana identified genes responding to salt stress by experimentally comparing Artemia individuals reared under hypersaline and marine conditions [57].…”