Dataset Information

Sex-Specific Co-expression Networks and Sex-Biased Gene Expression in the Salmonid Brook Charr Salvelinus fontinalis.

ABSTRACT: Networks of co-expressed genes produce complex phenotypes associated with functional novelty. Sex differences in gene expression levels or in the structure of gene co-expression networks can cause sexual dimorphism and may resolve sexually antagonistic selection. Here we used RNA-sequencing in the salmonid Brook Charr Salvelinus fontinalis to characterize sex-specific co-expression networks in the liver of 47 female and 53 male offspring. In both networks, modules were characterized for functional enrichment, hub gene identification, and associations with 15 growth, reproduction, and stress-related phenotypes. Modules were then evaluated for preservation in the opposite sex, and in the congener Arctic Charr Salvelinus alpinus Overall, more transcripts were assigned to a module in the female network than in the male network, which coincided with higher inter-individual gene expression and phenotype variation in the females. Most modules were preserved between sexes and species, including those involved in conserved cellular processes (e.g., translation, immune pathways). However, two sex-specific male modules were identified, and these may contribute to sexual dimorphism. To compare with the network analysis, differentially expressed transcripts were identified between the sexes, revealing a total of 16% of expressed transcripts as sex-biased. For both sexes, there was no overrepresentation of sex-biased genes or sex-specific modules on the putative sex chromosome. Sex-biased transcripts were also not overrepresented in sex-specific modules, and in fact highly male-biased transcripts were enriched in preserved modules. Comparative network analysis and differential expression analyses identified different aspects of sex differences in gene expression, and both provided new insights on the genes underlying sexual dimorphism in the salmonid Brook Charr.

SUBMITTER: Sutherland BJG

PROVIDER: S-EPMC6404618 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Publications

Sex-Specific Co-expression Networks and Sex-Biased Gene Expression in the Salmonid Brook Charr <i>Salvelinus fontinalis</i>.

Sutherland Ben J G BJG Prokkola Jenni M JM Audet Céline C Bernatchez Louis L

G3 (Bethesda, Md.) 20190307 3

Networks of co-expressed genes produce complex phenotypes associated with functional novelty. Sex differences in gene expression levels or in the structure of gene co-expression networks can cause sexual dimorphism and may resolve sexually antagonistic selection. Here we used RNA-sequencing in the salmonid Brook Charr <i>Salvelinus fontinalis</i> to characterize sex-specific co-expression networks in the liver of 47 female and 53 male offspring. In both networks, modules were characterized for f ...[more]

PMID: 30692150

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Project description:Whole-genome duplication (WGD) can have large impacts on genome evolution, and much remains unknown about these impacts. This includes the mechanisms of coping with a duplicated sex determination system and whether this has an impact on increasing the diversity of sex determination mechanisms. Other impacts include sexual conflict, where alleles having different optimums in each sex can result in sequestration of genes into nonrecombining sex chromosomes. Sex chromosome development itself may involve sex-specific recombination rate (i.e., heterochiasmy), which is also poorly understood. The family Salmonidae is a model system for these phenomena, having undergone autotetraploidization and subsequent rediploidization in most of the genome at the base of the lineage. The salmonid master sex determining gene is known, and many species have nonhomologous sex chromosomes, putatively due to transposition of this gene. In this study, we identify the sex chromosome of Brook Charr Salvelinus fontinalis and compare sex chromosome identities across the lineage (eight species and four genera). Although nonhomology is frequent, homologous sex chromosomes and other consistencies are present in distantly related species, indicating probable convergence on specific sex and neo-sex chromosomes. We also characterize strong heterochiasmy with 2.7-fold more crossovers in maternal than paternal haplotypes with paternal crossovers biased to chromosome ends. When considering only rediploidized chromosomes, the overall heterochiasmy trend remains, although with only 1.9-fold more recombination in the female than the male. Y chromosome crossovers are restricted to a single end of the chromosome, and this chromosome contains a large interspecific inversion, although its status between males and females remains unknown. Finally, we identify quantitative trait loci (QTL) for 21 unique growth, reproductive, and stress-related phenotypes to improve knowledge of the genetic architecture of these traits important to aquaculture and evolution.

Project description:Growth performance and reduced stress response are traits of major interest in fish production. Growth and stress-related quantitative trait loci (QTL) have been already identified in several salmonid species, but little effort has been devoted to charrs (genus Salvelinus). Moreover, most QTL studies to date focused on one or very few traits, and little investigation has been devoted to QTL identification for gene expression. Here, our objective was to identify QTL for 27 phenotypes related to growth and stress responses in brook charr (Salvelinus fontinalis), which is one of the most economically important freshwater aquaculture species in Canada. Phenotypes included 12 growth parameters, six blood and plasma variables, three hepatic variables, and one plasma hormone level as well as the relative expression measurements of five genes of interest linked to growth regulation. QTL analysis relied on a linkage map recently built from S. fontinalis consisting of both single-nucleotide polymorphism (SNP, n = 266) and microsatellite (n =81) markers in an F(2) interstrain hybrid population (n = 171). We identified 63 growth-related QTL and four stress-related QTL across 18 of the 40 linkage groups of the brook charr linkage map. Percent variance explained, confidence interval, and allelic QTL effects also were investigated to provide insight into the genetic architecture of growth- and stress-related QTL. QTL related to growth performance and stress response that were identified could be classified into two groups: (1) a group composed of the numerous, small-effect QTL associated with some traits related to growth (i.e., weight) that may be under the control of a large number of genes or pleiotropic genes, and (2) a group of less numerous QTL associated with growth (i.e., gene expression) and with stress-related QTL that display a larger effect, suggesting that these QTL are under the control of a limited number of genes of major effect. This study represents a first step toward the identification of genes potentially linked to phenotypic variation of growth and stress response in brook charr. The ultimate goal is to provide new tools for developing Molecular Assisted Selection for this species.

Project description:A linkage map of 40 linkage groups (LGs) was developed for brook charr, Salvelinus fontinalis, using an F(2) interstrain hybrid progeny (n = 171) and 256 coding gene SNP developed specifically for brook charr and validated from a large (>1000) subset of putative SNP, as well as 81 microsatellite markers. To identify quantitative trait loci (QTL) related to reproduction functions, these fish were also phenotyped at six physiological traits, including spermatozoid head diameter, sperm concentration, plasma testosterone, plasma 11-keto-testosterone, egg diameter, and plasma 17?-estradiol. Five significant QTL were detected over four LGs for egg diameter and plasma 17?-estradiol concentration in females, and sperm concentration as well as spermatozoid head diameter in males. In females, two different QTLs located on LG 11 and LG 34 were associated with the egg number, whereas one QTL was associated with plasma 17?-estradiol concentration (LG 8). Their total percent variance explained (PVE) was 26.7% and 27.6%, respectively. In males, two QTL were also detected for the sperm concentration, and their PVE were estimated at 18.58% and 14.95%, respectively. The low QTL number, associated with the high PVE, suggests that the variance in these reproductive physiological traits was either under the control of one major gene or a small number of genes. The QTL associated with sperm concentration, plasma 17?-estradiol, and egg diameter appeared to be under a dominance effect, whereas the two others were under a negative additive effect. These results show that genes underlying the phenotypic variance of these traits are under different modes of action (additive vs. dominance) and may be used to predict an increase or a decrease in their phenotypic values in subsequent generations of selective breeding. Moreover, this newly developed panel of mapped SNP located in coding gene regions will be useful for screening wild populations, especially in the context of investigating the genetic impact of massive stocking of domestic brook charr to support the angling industry throughout eastern North America.

Dataset Information

Sex-Specific Co-expression Networks and Sex-Biased Gene Expression in the Salmonid Brook Charr Salvelinus fontinalis.

Publications

Sex-Specific Co-expression Networks and Sex-Biased Gene Expression in the Salmonid Brook Charr <i>Salvelinus fontinalis</i>.

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