Sex chromosome dosage compensation in<i>Heliconius</i>butterflies: global yet still incomplete?

Walters, James R.; Hardcastle, Thomas J.; Jiggins, Chris D.

doi:10.1101/016675

Cited by 14 publications

(44 citation statements)

References 80 publications

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“…Analysis of gene expression profiles in the data retrieved from Walters et al. () by principal component, the first principal component separates gene expression in whole abdomen by sex and explains 97% of variance (Supporting Information Figure S1). The 25 H. melpomene samples sequenced for this project have a median total number of reads of 34.86 M (min.…”

Section: Resultsmentioning

confidence: 99%

“…Gene expression data were calculated using (a) Illumina 100‐bp paired‐end RNA‐seq data from five Panamanian H. m. rosina whole‐male abdomens, and five Panamanian H. m. rosina whole‐female abdomens, downloaded from GenBank (BioProject PRJNA283415) (Walters et al., ) and (b) newly sequenced Illumina HiSeq 2500 150‐bp paired‐end directional (stranded) RNA‐seq data from ovary tissue of seven young (1 hr) and six old (20 days) H. m. rosina females and from gut tissue of six young (1 hr) and six old (20 days) H. m. rosina females (25 samples from 13 different individuals, Supporting Information Table S1).…”

Section: Methodsmentioning

confidence: 99%

“…We filtered the results as in Walters et al. () with FDR < 0.05 (alpha = 0.05) (Walters et al., ). Ovary‐ and gut‐biased genes have a log 2 ‐fold change significance threshold >1.5 (option: lcfThreshold < 1.5, altHypothesis = “greaterAbs”).…”

Section: Methodsmentioning

confidence: 99%

“…Sex‐biased expression is common across taxa from mammals (Rinn & Snyder, ) to Diptera (Assis, Zhou, & Bachtrog, ), reptiles (Cox et al., ), birds (Mank, Nam, & Ellegren, ; Mank, Vicoso, Berlin, & Charlesworth, ) and Lepidoptera (Rousselle, Faivre, Ballenghien, Galtier, & Nabholz, ). For example, in Drosophila melanogaster , 57% of genes have been categorized as sex biased (Assis et al., ), and, in Heliconius melpomene , analysis of two different tissues identified up to 29% of expressed genes as sex biased (Walters, Hardcastle, & Jiggins, ). The vast majority of genes that exhibit sexually dimorphic expression are active in reproductive tissues and tend to also have distinctive rates of molecular evolution compared to genes without dimorphic expression (Avila, Campos, & Charlesworth, ; Parisi et al., , ).…”

Section: Introductionmentioning

confidence: 99%

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

Pinharanda

Rousselle

Martin

et al. 2019

J of Evolutionary Biology

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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.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Pinharanda

Rousselle

Martin

et al. 2019

J of Evolutionary Biology

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“…e Rumex hastatulus and Rumex bucephalophorus (Hough et al, 2014). f Heliconius melpomene and Heliconius cydno (Walters et al, 2015). g Gallus gallus (Mank, 2013;Wright et al, 2012), Charadrius alexandrinus (Mank, 2013), Taeniopygia guttata (Mank, 2013), Sylvia communis (Mank, 2013), Corvus brachyrhynchos (Mank, 2013) and Ficedula albicollis (Uebbing et al, 2013).…”

Section: Evolutionary Implicationsmentioning

confidence: 99%

X ‐Chromosome Dosage Compensation

Zhang

2016

Encyclopedia of Life Sciences

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The X and Y chromosomes of placental and marsupial mammals originated from a pair of autosomes. Ohno hypothesised nearly 50 years ago that the expression levels of X‐linked genes should be doubled to compensate for the degeneration of their Y‐linked homologues during sex chromosome evolution. The advent of microarray and RNA (ribonucleic acid) sequencing technologies in the past decade prompted a series of empirical tests of Ohno's hypothesis. Surprisingly, X‐chromosome dosage compensation is found to be largely absent in mammals. Studies of multiple independently evolved sex chromosome systems from a variety of species revealed a large variation in sex‐chromosome dosage compensation, ranging from absence of compensation to complete compensation, although further scrutiny is required because of the high heterogeneities in expression data acquisition and analysis methods among studies. The lack of sex chromosome dosage compensation in at least some lineages has important implications for understanding gene expression evolution and sex chromosome evolution. Key Concepts Ohno proposed that the expression levels of mammalian X‐linked genes should be doubled to compensate for the degeneration of their Y‐linked homologues during sex chromosome evolution. Initial microarray studies of genome‐wide gene expression levels found an X : AA ratio of ∼1, consistent with Ohno's hypothesis. Subsequent analysis of transcriptomic data generated by the more sensitive RNA sequencing method found an X : AA ratio of ∼0.5, inconsistent with Ohno's hypothesis. Some argued that Ohno's hypothesis is supported because X : AA is about 1 for actively expressed genes, but this assertion is caused by a common misunderstanding of Ohno's hypothesis. A direct comparison between human X‐linked genes and their one‐to‐one orthologues located in chicken autosomes that are homologous to the mammalian proto‐X found no upregulation in mammalian X‐linked gene expression, refuting Ohno's hypothesis. A human proteomic analysis found no evidence for a twofold upregulation of protein concentrations of X‐linked genes. Transcriptome analyses of multiple species with independently evolved sex chromosomes revealed a large variation in the presence/absence and degree of sex chromosome dosage compensation, but further scrutiny is required due to the high heterogeneities in the data and methods used in the published studies. The lack of sex chromosome dosage compensation in at least some lineages suggests that halving the expression level of a gene usually has no appreciable fitness consequences.

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A de novo transcriptional atlas in Danaus plexippus reveals variability in dosage compensation across tissues

et al. 2021

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A detailed knowledge of gene function in the monarch butterfly is still lacking. Here we generate a genome assembly from a Mexican nonmigratory population and used RNA-seq data from 14 biological samples for gene annotation and to construct an atlas portraying the breadth of gene expression during most of the monarch life cycle. Two thirds of the genes show expression changes, with long noncoding RNAs being particularly finely regulated during adulthood, and male-biased expression being four times more common than female-biased. The two portions of the monarch heterochromosome Z, one ancestral to the Lepidoptera and the other resulting from a chromosomal fusion, display distinct association with sex-biased expression, reflecting sample-dependent incompleteness or absence of dosage compensation in the ancestral but not the novel portion of the Z. This study presents extended genomic and transcriptomic resources that will facilitate a better understanding of the monarch’s adaptation to a changing environment.

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Sex chromosome dosage compensation inHeliconiusbutterflies: global yet still incomplete?

Abstract: 19

Cited by 14 publications

References 80 publications

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

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

X ‐Chromosome Dosage Compensation

A de novo transcriptional atlas in Danaus plexippus reveals variability in dosage compensation across tissues

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