Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

Abstract

Sexually dimorphic phenotypes arise largely from sex-specific gene expression, which has mainly been characterized in sexually naïve adults. However, we expect sexual dimorphism in transcription to be dynamic and dependent on factors such as reproductive status. Mating induces many behavioral and physiological changes distinct to each sex and is therefore expected to activate regulatory changes in many sex-biased genes. Here, we first characterized sexual dimorphism in gene expression in Callosobruchus maculatus seed beetles. We then examined how females and males respond to mating and how it affects sex-biased expression, both in sex-limited (abdomen) and sex-shared (head and thorax) tissues. Mating responses were largely sex-specific and, as expected, females showed more genes responding compared with males (∼2,000 vs. ∼300 genes in the abdomen, ∼500 vs. ∼400 in the head and thorax, respectively). Of the sex-biased genes present in virgins, 16% (1,041 genes) in the abdomen and 17% (243 genes) in the head and thorax altered their relative expression between the sexes as a result of mating. Sex-bias status changed in 2% of the genes in the abdomen and 4% in the head and thorax following mating. Mating responses involved de-feminization of females and, to a lesser extent, de-masculinization of males relative to their virgin state: mating decreased rather than increased dimorphic expression of sex-biased genes. The fact that regulatory changes of both types of sex-biased genes occurred in both sexes suggests that male- and female-specific selection is not restricted to male- and female-biased genes, respectively, as is sometimes assumed.

Keywords: RNA-Seq; alternative splicing; sex-biased expression; sex-specific selection; transcriptome.

Fig. 1.—

(A) A Venn diagram of the numbers of sex-biased genes in virgins (i.e., P_adj<0.05 and at least 2-fold sex-bias) in the abdomen and the head + thorax. (B) Numbers of genes showing plasticity in sex-biased expression due to mating (i.e., sex-by-mating interaction and mating response at least in one sex with P_adj<0.05) in each tissue class. Overlap of the genes that respond to mating in each sex and show sex-bias plasticity in (C) the abdomen and (D) the head and thorax tissues.

Fig. 2.—

Sex-biased expression in virgin and mated beetles for the plastic genes in (A) the abdomen (1,041 genes) and (B) the head and thorax (243 genes). Grey dashed lines indicate a 2-fold difference in expression between the sexes (i.e., logFC = 1 or − 1. Positive values indicate female- and negative male-biased expression). Off diagonal segments show the genes that have changed sex-bias status due to mating (upper left segment: from male- to female-bias, lower right segment: from female- to male-bias).

Fig. 3.—

Expression response to mating in males and females for the genes that switch sex-biased expression in the two tissue groups (i.e., sex-biased ≥ 2-fold in both virgin and mated beetles, with FDR 5%). Two left-most columns show the degree of sex-bias in the virgin and mated beetles (positive log2FC indicates female-biased expression) and the two right-most columns the degree of mating response in males and females for the same genes (positive log2FC indicates higher expression in the mated beetles). Absence of a record (white) indicates no significant difference between mated and virgin individuals.

Fig. 4.—

Mating response in the female (A and B) and male (C and D) abdomen and the head + thorax, respectively, as a function of average expression (logCPM). Sex-biased genes in virgins (P_adj<0.05 and at least 2-fold sex-bias) are highlighted. Positive values indicate a higher expression in the mated state relative to virgin.