Corticosterone and testosterone treatment influence expression of gene pathways linked to meiotic segregation in preovulatory follicles of the domestic hen.

Elizabeth R Wrobel,Alexandra B Bentz,Kristen J Navara,Mary T Mendonça,Stephen T Gardner,W Walter Lorenz,Aneta Agnieszka Koronowicz

doi:10.1371/journal.pone.0232120

Elizabeth R Wrobel, Alexandra B Bentz + Show 5 more

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https://doi.org/10.1371/journal.pone.0232120

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Abstract

Decades of work indicate that female birds can control their offspring sex ratios in response to environmental and social cues. In laying hens, hormones administered immediately prior to sex chromosome segregation can exert sex ratio skews, indicating that these hormones may act directly on the germinal disc to influence which sex chromosome is retained in the oocyte and which is discarded into an unfertilizable polar body. We aimed to uncover the gene pathways involved in this process by testing whether treatments with testosterone or corticosterone that were previously shown to influence sex ratios elicit changes in the expression of genes and/or gene pathways involved in the process of meiotic segregation. We injected laying hens with testosterone, corticosterone, or control oil 5h prior to ovulation and collected germinal discs from the F1 preovulatory follicle in each hen 1.5h after injection. We used RNA-sequencing (RNA-seq) followed by DESeq2 and gene set enrichment analyses to identify genes and gene pathways that were differentially expressed between germinal discs of control and hormone-treated hens. Corticosterone treatment triggered downregulation of 13 individual genes, as well as enrichment of gene sets related to meiotic spindle organization and chromosome segregation, and additional gene sets that function in ion transport. Testosterone treatment triggered upregulation of one gene, and enrichment of one gene set that functions in nuclear chromosome segregation. This work indicates that corticosterone can be a potent regulator of meiotic processes and provides potential gene targets on which corticosterone and/or testosterone may act to influence offspring sex ratios in birds.

Highlights

Hundreds of scientific observations since the early 1900’s suggest that female birds are able to bias the sexes of the offspring they produce in response to external cues [1]
Testosterone’s influences appeared to be less dramatic than those triggered by corticosterone treatment
Corticosterone treatment, on the other hand, triggered downregulation of 13 differentially expressed genes (DEGs), 3 of which are interesting in terms of how they may play into an existing hypothesized mechanism for how sex ratio adjustment occurs

Summary

Introduction

Hundreds of scientific observations since the early 1900’s suggest that female birds are able to bias the sexes of the offspring they produce in response to external cues [1]. Birds bias primary offspring sex ratios in response to a variety of environmental conditions, such as territory quality [2,3], food availability [4,5], and laying date [6,7]. Both mate attractiveness [8,9] and maternal condition [10,11] exert a significant influence on offspring sex ratios. A body of research suggests that hormones are likely mediators of sex ratio adjustment during this time because they can transduce environmental and social experiences into physiological responses, and treatment with multiple hormones has biased offspring sex ratios in birds [15]

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