Transcriptome Differences between Alternative Sex Determining Genotypes in the House Fly,<i>Musca domestica</i>

Meisel, Richard P; Scott, Jeffrey G.; Clark, Andrew G.

doi:10.1101/016774

Cited by 14 publications

(48 citation statements)

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“…The expression of Ago2 paralogs has previously been characterized in P. monodon and shows that one paralog has indeed specialized to the germline of both males and females, but not the testis alone (Leebonoi et al 2015). Publicly available RNAseq data from the head, gonad, and carcass of male and female M. domestica (GSE67065, Meisel et al 2015) suggest that neither M. domestica Ago2 paralog has specialized to the testis ( Figure S8). However, public data from the head, thorax, and abdomen of male and female D. willistoni (GSE31723, Meisel et al 2012) show that one D. willistoni Ago2 paralog (FBgn0212615) is expressed ubiquitously, while the other (FBgn0226485) is expressed only in the male abdomen 766 S. H. Lewis et al…”

Section: Prospects For Novel Functions During the Evolution Of Rnaimentioning

confidence: 91%

“…Transcriptome data for D. willistoni were taken from (Meisel et al 2012), and transcriptome data for M. domestica were taken from (Meisel et al 2015). For both species, we mapped reads to coding sequences using Bowtie 2.1 (Langmead et al 2009), counted reads mapping to each coding sequence using HTSeq (Anders et al 2015), and converted counts to reads per kilobase per million reads (RPKM (Mortazavi et al 2008)) to account for coding sequence length and sequencing depth.…”

Section: Supplementary Figure S2: the Expression Of D Pseudoobscura mentioning

confidence: 99%

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Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

Lewis

Webster

Salmela

et al. 2016

Preprint

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Argonaute2 (Ago2) is a rapidly evolving nuclease in the Drosophila melanogaster RNA interference (RNAi) pathway that targets viruses and transposable elements in somatic tissues. Here we reconstruct the history of Ago2 duplications across the D. obscura group and use patterns of gene expression to infer new functional specialization. We show that some duplications are old, shared by the entire species group, and that losses may be common, including previously undetected losses in the lineage leading to D. pseudoobscura. We find that while the original (syntenic) gene copy has generally retained the ancestral ubiquitous expression pattern, most of the novel Ago2 paralogs have independently specialized to testis-specific expression. Using population genetic analyses, we show that most testis-specific paralogs have significantly lower genetic diversity than the genome-wide average. This suggests recent positive selection in three different species, and model-based analyses provide strong evidence of recent hard selective sweeps in or near four of the six D. pseudoobscura Ago2 paralogs. We speculate that the repeated evolution of testis specificity in obscura group Ago2 genes, combined with their dynamic turnover and strong signatures of adaptive evolution, may be associated with highly derived roles in the suppression of transposable elements or meiotic drive. Our study highlights the lability of RNAi pathways, even within well-studied groups such as Drosophila, and suggests that strong selection may act quickly after duplication in RNAi pathways, potentially giving rise to new and unknown RNAi functions in nonmodel species. KEYWORDS Argonaute; RNAi; Drosophila; duplication; testis A RGONAUTE genes are found in almost all eukaryotes, where they play a key role in antiviral immune defense, gene regulation, and genome stability. They perform this diverse range of functions through their role in RNA interference (RNAi) mechanisms, an ancient system of nucleic acid manipulation in which small RNA (sRNA) molecules guide Argonaute proteins to nucleic acid targets through base complementarity (reviewed in Meister 2013). Gene duplication has occurred throughout the evolution of the Argonaute gene family, with ancient duplication events characteristic of some lineages-such as three duplications early in plant evolution (Singh et al. 2015) and multiple expansions and losses throughout the evolution of nematodes (reviewed in Buck and Blaxter 2013) and the Diptera . After duplication, Argonautes have often undergone functional divergence, involving changes in expression patterns and altered sRNA binding partners (Lu et al. 2011;Leebonoi et al. 2015;Miesen et al. 2015). Duplication early in eukaryotic evolution produced two distinct Argonaute subfamilies, Ago and Piwi, which have since been retained in the vast majority of Metazoa (Cerutti and Casas-Mollano 2006). Members of the Ago subfamily are expressed in both somatic and germline tissue, and variously bind sRNAs derived from host transcripts (miRNAs, endo-siRNAs) ...

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Section: Prospects For Novel Functions During the Evolution Of Rnaimentioning

confidence: 91%

Section: Supplementary Figure S2: the Expression Of D Pseudoobscura mentioning

confidence: 99%

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

Lewis

Webster

Salmela

et al. 2016

Preprint

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“…One strain, Cornell susceptible (CS), has X/X; III M /III males (Scott et al 1996;Hamm et al 2005;Meisel et al 2015). The other four strains have previously been characterized as having males with the XY karyotype: aabys, A3, LPR, and CSaY.…”

Section: Fly Strainsmentioning

confidence: 99%

The house fly Y Chromosome is young and minimally differentiated from its ancient X Chromosome partner

2017

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Canonical ancient sex chromosome pairs consist of a gene rich X (or Z) Chromosome and a male-limited (or female-limited) Y (or W) Chromosome that is gene poor. In contrast to highly differentiated sex chromosomes, nascent sex chromosome pairs are homomorphic or very similar in sequence content. Nascent sex chromosomes can arise if an existing sex chromosome fuses to an autosome or an autosome acquires a new sex-determining locus/allele. Sex chromosomes often differ between closely related species and can even be polymorphic within species, suggesting that nascent sex chromosomes arise frequently over the course of evolution. Previously documented sex chromosome transitions involve changes to both members of the sex chromosome pair (X and Y, or Z and W). The house fly has sex chromosomes that resemble the ancestral fly karyotype that originated ∼100 million yr ago; therefore, the house fly is expected to have X and Y Chromosomes with different gene content. We tested this hypothesis using whole-genome sequencing and transcriptomic data, and we discovered little evidence for genetic differentiation between the X and Y in house fly. We propose that the house fly has retained the ancient X Chromosome, but the ancestral Y was replaced by an X Chromosome carrying a new male determining gene. Our proposed hypothesis provides a mechanism for how one member of a sex chromosome pair can experience evolutionary turnover while the other member remains unaffected.

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“…We examined gene expression in four house fly strains that each have a different naturally 108 occurring proto-Y chromosome (either Y M or III M ) on a common genetic background (Figure 1). 109 We used a previously described backcrossing method to move each proto-Y chromosome onto 110 the Cornell Susceptible (CS) genetic background (Meisel et al 2015). CS is an inbred III M strain 111 produced by mixing strains collected from throughout the United States (Scott et al 1996).…”

Section: Introduction 36 37mentioning

confidence: 99%

Minimal effects of proto-Y chromosomes on house fly gene expression in spite of evidence that selection maintains stable polygenic sex determination

Son

Kohlbrenner

Heinze

et al. 2019

Preprint

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14 15 Sex determination, the developmental process by which organismal sex is established, evolves 16 fast, often due to changes in the master regulators at the top of the pathway. Additionally, in 17 species with polygenic sex determination, multiple different master regulators segregate as 18 polymorphisms. Understanding the forces that maintain polygenic sex determination can be 19informative of the factors that drive the evolution of sex determination. The house fly, Musca 20 domestica, is a well-suited model to those ends because natural populations harbor male-21 determining loci on each of the six chromosomes and a bi-allelic female-determiner. To 22 investigate how natural selection maintains polygenic sex determination in house fly, we assayed 23 the phenotypic effects of proto-Y chromosomes by performing RNA-seq experiments to measure 24 gene expression in house fly males carrying different proto-Y chromosomes. We find that the 25 proto-Y chromosomes have similar effects as a non-sex-

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Transcriptome Differences between Alternative Sex Determining Genotypes in the House Fly,Musca domestica

Cited by 14 publications

References 84 publications

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

The house fly Y Chromosome is young and minimally differentiated from its ancient X Chromosome partner

Minimal effects of proto-Y chromosomes on house fly gene expression in spite of evidence that selection maintains stable polygenic sex determination

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