Limits...
Limited sex-biased neural gene expression patterns across strains in Zebrafish (Danio rerio).

Wong RY, McLeod MM, Godwin J - BMC Genomics (2014)

Bottom Line: Surprisingly, only 61 genes (approximately 0.4% of genes analyzed) showed a significant sex effect across all four strains, and 48 of these differences were male-biased.WGCNA revealed only one module that was significantly associated with sex.Further, genes found to be sex-biased are associated with hormone biosynthesis, suggesting that sex steroid hormones may be key contributors to sexual behavioral plasticity seen in teleosts.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, W,M, Keck Center for Behavioral Biology, Box 7617, North Carolina State University, Raleigh, NC 27695-7617, USA. rwong@unomaha.edu.

ABSTRACT

Background: Male and female vertebrates typically differ in a range of characteristics, from morphology to physiology to behavior, which are influenced by factors such as the social environment and the internal hormonal and genetic milieu. However, sex differences in gene expression profiles in the brains of vertebrates are only beginning to be understood. Fishes provide a unique complement to studies of sex differences in mammals and birds given that fish show extreme plasticity and lability of sexually dimorphic characters and behaviors during development and even adulthood. Hence, teleost models can give additional insight into sexual differentiation. The goal of this study is to identify neurotranscriptomic mechanisms for sex differences in the brain.

Results: In this study we examined whole-brain sex-biased gene expression through RNA-sequencing across four strains of zebrafish. We subsequently conducted systems level analyses by examining gene network dynamics between the sexes using weighted gene coexpression network analysis. Surprisingly, only 61 genes (approximately 0.4% of genes analyzed) showed a significant sex effect across all four strains, and 48 of these differences were male-biased. Several of these genes are associated with steroid hormone biosynthesis. Despite sex differences in a display of stress-related behaviors, basal transcript levels did not predict the intensity of the behavioral display. WGCNA revealed only one module that was significantly associated with sex. Intriguingly, comparing intermodule dynamics between the sexes revealed only moderate preservation. Further we identify sex-specific gene modules.

Conclusions: Despite differences in morphology, physiology, and behavior, there is limited sex-biased neural gene expression in zebrafish. Further, genes found to be sex-biased are associated with hormone biosynthesis, suggesting that sex steroid hormones may be key contributors to sexual behavioral plasticity seen in teleosts. A possible mechanism is through regulating specific brain gene networks.

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Multidimensional scaling plot of all genes for each sample. Square, circle, star, and diamond represents the LSB, HSB, AB, and SH strains, respectively. Male and female samples are represented by open and filled symbols, respectively.
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Fig1: Multidimensional scaling plot of all genes for each sample. Square, circle, star, and diamond represents the LSB, HSB, AB, and SH strains, respectively. Male and female samples are represented by open and filled symbols, respectively.

Mentions: In this study we used RNA-sequencing and subsequent bioinformatic analyses to compare the neurotranscriptomes of four strains of zebrafish (AB, SH, HSB, LSB) to identify sex-biased gene expression patterns. Multidimensional scaling analysis revealed that the samples clearly clustered together by strain rather than sex (Figure 1). Of the 15,304 protein coding genes analyzed, 61 showed significant differences between the sexes after controlling for strain differences (Figure 2, Additional file 1). The zebrafish brain shows a substantially lower number of sex-biased genes compared to the gonads or liver [28, 29, 34, 35] and the number of differentially expressed genes in the brain in this study is consistent with other studies [28, 32, 33]. We speculate that having the majority of the genes displaying similar basal level expression between males and females may be an important factor for sexual lability in fishes. If the male and female zebrafish brain is largely similar at the basal transcript level, behavioral and physiological sex differences may be more easily facilitated by other factors such as the hormonal, ecological, or social environment.Figure 1


Limited sex-biased neural gene expression patterns across strains in Zebrafish (Danio rerio).

Wong RY, McLeod MM, Godwin J - BMC Genomics (2014)

Multidimensional scaling plot of all genes for each sample. Square, circle, star, and diamond represents the LSB, HSB, AB, and SH strains, respectively. Male and female samples are represented by open and filled symbols, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4216363&req=5

Fig1: Multidimensional scaling plot of all genes for each sample. Square, circle, star, and diamond represents the LSB, HSB, AB, and SH strains, respectively. Male and female samples are represented by open and filled symbols, respectively.
Mentions: In this study we used RNA-sequencing and subsequent bioinformatic analyses to compare the neurotranscriptomes of four strains of zebrafish (AB, SH, HSB, LSB) to identify sex-biased gene expression patterns. Multidimensional scaling analysis revealed that the samples clearly clustered together by strain rather than sex (Figure 1). Of the 15,304 protein coding genes analyzed, 61 showed significant differences between the sexes after controlling for strain differences (Figure 2, Additional file 1). The zebrafish brain shows a substantially lower number of sex-biased genes compared to the gonads or liver [28, 29, 34, 35] and the number of differentially expressed genes in the brain in this study is consistent with other studies [28, 32, 33]. We speculate that having the majority of the genes displaying similar basal level expression between males and females may be an important factor for sexual lability in fishes. If the male and female zebrafish brain is largely similar at the basal transcript level, behavioral and physiological sex differences may be more easily facilitated by other factors such as the hormonal, ecological, or social environment.Figure 1

Bottom Line: Surprisingly, only 61 genes (approximately 0.4% of genes analyzed) showed a significant sex effect across all four strains, and 48 of these differences were male-biased.WGCNA revealed only one module that was significantly associated with sex.Further, genes found to be sex-biased are associated with hormone biosynthesis, suggesting that sex steroid hormones may be key contributors to sexual behavioral plasticity seen in teleosts.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, W,M, Keck Center for Behavioral Biology, Box 7617, North Carolina State University, Raleigh, NC 27695-7617, USA. rwong@unomaha.edu.

ABSTRACT

Background: Male and female vertebrates typically differ in a range of characteristics, from morphology to physiology to behavior, which are influenced by factors such as the social environment and the internal hormonal and genetic milieu. However, sex differences in gene expression profiles in the brains of vertebrates are only beginning to be understood. Fishes provide a unique complement to studies of sex differences in mammals and birds given that fish show extreme plasticity and lability of sexually dimorphic characters and behaviors during development and even adulthood. Hence, teleost models can give additional insight into sexual differentiation. The goal of this study is to identify neurotranscriptomic mechanisms for sex differences in the brain.

Results: In this study we examined whole-brain sex-biased gene expression through RNA-sequencing across four strains of zebrafish. We subsequently conducted systems level analyses by examining gene network dynamics between the sexes using weighted gene coexpression network analysis. Surprisingly, only 61 genes (approximately 0.4% of genes analyzed) showed a significant sex effect across all four strains, and 48 of these differences were male-biased. Several of these genes are associated with steroid hormone biosynthesis. Despite sex differences in a display of stress-related behaviors, basal transcript levels did not predict the intensity of the behavioral display. WGCNA revealed only one module that was significantly associated with sex. Intriguingly, comparing intermodule dynamics between the sexes revealed only moderate preservation. Further we identify sex-specific gene modules.

Conclusions: Despite differences in morphology, physiology, and behavior, there is limited sex-biased neural gene expression in zebrafish. Further, genes found to be sex-biased are associated with hormone biosynthesis, suggesting that sex steroid hormones may be key contributors to sexual behavioral plasticity seen in teleosts. A possible mechanism is through regulating specific brain gene networks.

Show MeSH
Related in: MedlinePlus