The evolution of sex-biased gene expression in the <i>Drosophila</i> brain

Khodursky, Samuel; Svetec, Nicolas; Durkin, Sylvia M.; Zhao, Li

doi:10.1101/gr.259069.119

Cited by 40 publications

(54 citation statements)

References 63 publications

(60 reference statements)

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“…Although the authors conclude that this decrease is associated with the X chromosome being depauperate in genes with very high expression, even after removing overexpressed genes from the pool of analyzed genes, significant differences in the expression activity persist for intestinal tissues in males and females. The X chromosome enrichment with male-biased genes has also been shown for gene expression in the Drosophila brain [104], confirming the noted effect of selection as a factor in the evolution of sexual dimorphism.…”

Section: Discussionsupporting

confidence: 65%

The effects of the sex chromosomes on the inheritance of species-specific traits of the copulatory organ shape in Drosophila virilis and Drosophila lummei

et al. 2020

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The shape of the male genitalia in many taxa is the most rapidly evolving morphological structure, often driving reproductive isolation, and is therefore widely used in systematics as a key character to distinguish between sibling species. However, only a few studies have used the genital arch of the male copulatory organ as a model to study the genetic basis of species-specific differences in the Drosophila copulatory system. Moreover, almost nothing is known about the effects of the sex chromosomes on the shape of the male mating organ. In our study, we used a set of crosses between D. virilis and D. lummei and applied the methods of quantitative genetics to assess the variability of the shape of the male copulatory organ and the effects of the sex chromosomes and autosomes on its variance. Our results showed that the male genital shape depends on the species composition of the sex chromosomes and autosomes. Epistatic interactions of the sex chromosomes with autosomes and the species origin of the Y-chromosome in a male in interspecific crosses also influenced the expression of species-specific traits in the shape of the male copulatory system. Overall, the effects of sex chromosomes were comparable to the effects of autosomes despite the great differences in gene numbers between them. It may be reasonably considered that sexual selection for specific genes associated with the shape of the male mating organ prevents the demasculinization of the X chromosome.

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Section: Discussionsupporting

confidence: 65%

The effects of the sex chromosomes on the inheritance of species-specific traits of the copulatory organ shape in Drosophila virilis and Drosophila lummei

et al. 2020

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“…The brain comprises a major tissue type providing the neurological basis for the mating behaviors of courtship, intrasex competition, mate-choice, and post-mating male-female responses [22][23][24][25]. Sex-biased expression per se in the brain has been examined in some insects and vertebrates [3,5,22,23,[25][26][27][28][29][30][31][32]. Further, in Drosophila, analyses of a small number of neural genes have been found to be directly connected to mating functions and behaviors [33][34][35].…”

Section: Introductionmentioning

confidence: 99%

“…However, there is a striking paucity of data on the relationship between sex-biased expression in the brain and protein sequence evolution [22]. Moreover, the minimal research available from birds, humans and flies have suggested different types of male and female effects on rates of protein evolution, depending on the system [23,29,32] (see also some brain-related and composite-tissue analyses [36,37]), and the causes of those patterns remain poorly understood. It is therefore evident that additional study is needed of sex-biased brain expression and its relationship to molecular…”

Section: Introductionmentioning

confidence: 99%

“…The brain is a major tissue type providing the neurological basis for the mating behaviors of courtship, intrasex competition, mate-choice, and post-mating male-female responses (Mank et al, 2007;Dalton et al, 2010;Naurin et al, 2011;Wright & Mank, 2013). Male and female differences in gene expression per se in the brain have been examined in some insects and vertebrates (Jagadeeshan & Singh, 2005;Mank et al, 2007;Santos et al, 2008;Small et al, 2009;Naurin et al, 2011;Catalan et al, 2012;Wright & Mank, 2013;Ingleby et al, 2014;Tomchaney et al, 2014;Huylmans & Parsch, 2015;Shi et al, 2016;Yang et al, 2016;Khodursky et al, 2020). Further, in Drosophila, analyses of a small number of neural genes showed a direct connection to mating functions and behaviors (Drapeau et al, 2003;Kadener et al, 2006;Dauwalder, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary dynamics of sex-biased genes expressed in cricket brains and gonads

Whittle

Kulkarni

Extavour

2020

Preprint

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AbstractBackgroundSex-biased gene expression, particularly male-biased expression in the gonad, has often been linked to rapid protein sequence evolution (dN/dS) in animals. This evolutionary trend may arise from one or both of sexual selection pressures during mating or low pleiotropy. In insects, research on sex-biased transcription and dN/dS remains largely focused on a few holometabolous species, with variable findings on male and female gonadal effects. The brain is central to the mating process, and provides neurological foundation for mating behaviors, such as courtship, intrasex competition and mate choice. However, there is a striking paucity of research on sex-biased expression of genes in the brain and the rate of protein sequence evolution in such genes.ResultsHere, we studied sex-biased gene expression in a hemimetabolous insect, the cricket Gryllus bimaculatus. We generated novel RNA-seq data for two sexual tissue types, the gonad and somatic reproductive system, and for two core components of the nervous system, the brain and ventral nerve cord. From a genome-wide analysis of genes expressed in these tissues, we report the accelerated evolution of testis-biased genes and seminal fluid proteins (SFPs) genes, as compared to ovary-biased and unbiased genes in this cricket model, which includes an elevated frequency of positive selection events. With respect to the brain, while sex-biased brain genes were much less common than for the gonads, they exhibited exceptionally rapid evolution, an effect that was stronger for the female than for the male brain. Certain sex-biased brain genes were predicted to be involved in mating or sex-related functions, which we suggest may cause exposure to sexual selection. Moreover, the sex-biased brain genes exhibited remarkably low cross-tissue expression breadth, or pleiotropy. We speculate that this feature may permit relaxed purifying selection, and allow the freedom for adaptive protein functional changes in these brain-expressed genes.ConclusionsOur results demonstrate that sex-biased expression in the male gonad, and sex-biased gene expression in the brain, especially the female brain, are associated with rapid protein sequence evolution in a cricket model system. We discuss the results with respect to our findings on pleiotropy and positive selection, and consider the potential role of the dynamic mating biology of this cricket model in shaping these patterns.

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“…Sex-biased genes are unevenly distributed on the genome among various clades, especially showing enrichment on the X or Z chromosome in the homogametic sex via a pervasive phenomenon [ 11 , 12 , 62 , 63 , 64 , 65 ]. Our results exhibited that both female- and male-biased genes in both tissues were significantly enriched on the Z chromosome.…”

Section: Discussionmentioning

confidence: 99%

Sex-Biased Gene Expression and Evolution in the Cerebrum and Syrinx of Chinese Hwamei (Garrulax canorus)

Jiang

Lin

Sun

et al. 2021

Genes

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It is common that males and females display sexual dimorphisms, which usually result from sex-biased gene expression. Chinese hwamei (Garrulax canorus) is a good model for studying sex-biased gene expression because the song between the sexes is quite different. In this study, we analyze cerebrum and syrinx sex-biased gene expression and evolution using the de novo assembled Chinese hwamei transcriptome. In both the cerebrum and syrinx, our study revealed that most female-biased genes were actively expressed in females only, while most male-biased genes were actively expressed in both sexes. In addition, both male- and female-biased genes were enriched on the putative Z chromosome, suggesting the existence of sexually antagonistic genes and the insufficient dosage compensation of the Z-linked genes. We also identified a 9 Mb sex linkage region on the putative 4A chromosome which enriched more than 20% of female-biased genes. Resultantly, male-biased genes in both tissues had significantly higher Ka/Ks and effective number of codons (ENCs) than unbiased genes, and this suggested that male-biased genes which exhibit accelerated divergence may have resulted from positive selection. Taken together, our results initially revealed the reasons for the differences in singing behavior between males and females of Chinese hwamei.

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The evolution of sex-biased gene expression in the Drosophila brain

Cited by 40 publications

References 63 publications

The effects of the sex chromosomes on the inheritance of species-specific traits of the copulatory organ shape in Drosophila virilis and Drosophila lummei

The effects of the sex chromosomes on the inheritance of species-specific traits of the copulatory organ shape in Drosophila virilis and Drosophila lummei

Evolutionary dynamics of sex-biased genes expressed in cricket brains and gonads

Sex-Biased Gene Expression and Evolution in the Cerebrum and Syrinx of Chinese Hwamei (Garrulax canorus)

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