Sex-biased Expression of Genes and Transposable Elements in Hybrids from <i>Drosophila mojavensis</i> and <i>Drosophila arizonae</i>

Sex-biased gene expression is one of the main forces driving differences between sexes. Transposable elements (TEs) have also been shown to display sex-specific expression, mainly in the gonads. Despite this clear sexual dimorphism in the transcriptome, their contribution to postzygotic isolation remains poorly understood. Here, we tested whether the balance of gene and TE expression between ovaries and testes is disrupted in hybrids, potentially contributing to reproductive barriers. We analyzed Drosophila mojavensis and Drosophila arizonae, sibling species that produce sterile hybrids with differences in sperm motility. We found that genes and TEs exhibit testis-biased expression in both parental species and their hybrids. Hybrid sterility appears to be driven by a few deregulated genes rather than global transcriptome disruption. Our results demonstrated that seven candidate genes, including dyneins (Dhc98D, Dhc16F, Dic61B, Dhc36c, and Dnah3), an ATPase (Vha100-3), and a fatty acyl-CoA reductase (FAR), may underlie sterility, with Dic61B and FAR potentially linked to sperm immobility in H♀ari♂mwri hybrids. In addition, we found a subset of testis-biased genes under positive selection. The majority appear to evolve under relaxed purifying selection, in contrast to ovary-biased genes. We also identified that 22% of TE families in the parental genomes have different evolutionary dynamics, with some families remaining potentially active in one genome while becoming silenced or fragmented in the other. However, these TEs do not support the genome-mismatch hypothesis, as most are not sex-biased or deregulated in hybrids. Overall, our results highlight the role of sex-biased gene and TE expression in reproductive isolation.

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Journal
Genome Biology and Evolution
Published
2025-12-19
DOI
https://doi.org/10.1093/gbe/evaf247
Primary Topic
Chromosomal and Genetic Variations
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article
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article

Sex-biased Expression of Genes and Transposable Elements in Hybrids from Drosophila mojavensis and Drosophila arizonae

Claudia M A Carareto, Mariana Galvão Ferrarini, Cristina P. Vieira, Maryanna Simão et al.
Genome Biology and Evolution
Chromosomal and Genetic Variations
article

Sex-biased Expression of Genes and Transposable Elements in Hybrids from Drosophila mojavensis and Drosophila arizonae

Claudia M A Carareto, Mariana Galvão Ferrarini, Cristina P. Vieira, Maryanna Simão, Cecília Artico Banho, William V B Nunes, Daniel S Oliveira
article en

Abstract

Sex-biased gene expression is one of the main forces driving differences between sexes. Transposable elements (TEs) have also been shown to display sex-specific expression, mainly in the gonads. Despite this clear sexual dimorphism in the transcriptome, their contribution to postzygotic isolation remains poorly understood. Here, we tested whether the balance of gene and TE expression between ovaries and testes is disrupted in hybrids, potentially contributing to reproductive barriers. We analyzed Drosophila mojavensis and Drosophila arizonae, sibling species that produce sterile hybrids with differences in sperm motility. We found that genes and TEs exhibit testis-biased expression in both parental species and their hybrids. Hybrid sterility appears to be driven by a few deregulated genes rather than global transcriptome disruption. Our results demonstrated that seven candidate genes, including dyneins (Dhc98D, Dhc16F, Dic61B, Dhc36c, and Dnah3), an ATPase (Vha100-3), and a fatty acyl-CoA reductase (FAR), may underlie sterility, with Dic61B and FAR potentially linked to sperm immobility in H♀ari♂mwri hybrids. In addition, we found a subset of testis-biased genes under positive selection. The majority appear to evolve under relaxed purifying selection, in contrast to ovary-biased genes. We also identified that 22% of TE families in the parental genomes have different evolutionary dynamics, with some families remaining potentially active in one genome while becoming silenced or fragmented in the other. However, these TEs do not support the genome-mismatch hypothesis, as most are not sex-biased or deregulated in hybrids. Overall, our results highlight the role of sex-biased gene and TE expression in reproductive isolation.

Genome Biology and EvolutionVol. 18(2)
Université Claude Bernard Lyon 1 (FR), Centre National de la Recherche Scientifique (FR), Faculdade de Medicina de São José do Rio Preto (BR), Cornell University (US), Institut de Biologia Evolutiva (ES), Laboratoire de Biométrie et Biologie Evolutive (FR), Universidade Estadual Paulista (Unesp) (BR)
Openalex Percentile: Top 25%
Chromosomal and Genetic Variations
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