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Gene Expression Dynamics in Major Endocrine Regulatory Pathways along the Transition from Solitary to Social Life in a Bumblebee, Bombus terrestris

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ABSTRACT

Understanding the social evolution leading to insect eusociality requires, among other, a detailed insight into endocrine regulatory mechanisms that have been co-opted from solitary ancestors to play new roles in the complex life histories of eusocial species. Bumblebees represent well-suited models of a relatively primitive social organization standing on the mid-way to highly advanced eusociality and their queens undergo both, a solitary and a social phase, separated by winter diapause. In the present paper, we characterize the gene expression levels of major endocrine regulatory pathways across tissues, sexes, and life-stages of the buff-tailed bumblebee, Bombus terrestris, with special emphasis on critical stages of the queen's transition from solitary to social life. We focused on fundamental genes of three pathways: (1) Forkhead box protein O and insulin/insulin-like signaling, (2) Juvenile hormone (JH) signaling, and (3) Adipokinetic hormone signaling. Virgin queens were distinguished by higher expression of forkhead box protein O and downregulated insulin-like peptides and JH signaling, indicated by low expression of methyl farnesoate epoxidase (MFE) and transcription factor Krüppel homolog 1 (Kr-h1). Diapausing queens showed the expected downregulation of JH signaling in terms of low MFE and vitellogenin (Vg) expressions, but an unexpectedly high expression of Kr-h1. By contrast, reproducing queens revealed an upregulation of MFE and Vg together with insulin signaling. Surprisingly, the insulin growth factor 1 (IGF-1) turned out to be a queen-specific hormone. Workers exhibited an expression pattern of MFE and Vg similar to that of reproducing queens. Males were characterized by high Kr-h1 expression and low Vg level. The tissue comparison unveiled an unexpected resemblance between the fat body and hypopharyngeal glands across all investigated genes, sexes, and life stages.

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qRT-PCR analysis of tissue-specific relative expression levels of insulin-like growth factor 1 (IGF-1) across castes of B. terrestris. IGF-1 is part of the IIS signaling involved in reproduction and diapause. It is queen-specific (i.e., absent in workers and males) and lowest in virgin queens (see main text). Data represent mean ± SEM (n = 3–5) of normalized and rescaled expression levels. (A) Heatmap: Log-scale. Bar graphs: Relative transcript levels in (B) linear scale; and (C) log-transformed scale. Significantly different expression levels are indicated by different letters (p < 0.05).
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Figure 4: qRT-PCR analysis of tissue-specific relative expression levels of insulin-like growth factor 1 (IGF-1) across castes of B. terrestris. IGF-1 is part of the IIS signaling involved in reproduction and diapause. It is queen-specific (i.e., absent in workers and males) and lowest in virgin queens (see main text). Data represent mean ± SEM (n = 3–5) of normalized and rescaled expression levels. (A) Heatmap: Log-scale. Bar graphs: Relative transcript levels in (B) linear scale; and (C) log-transformed scale. Significantly different expression levels are indicated by different letters (p < 0.05).

Mentions: IGF-1 was expressed exclusively in queens (Figures 4A–C). In virgins, only spurious expression was detected in brain, hypopharyngeal glands, fat body, and ovaries. Higher expression values were observed in diapausing queens, where the ventriculus also contained IGF-1 transcripts. The highest expression occurred in brain, hypopharyngeal glands and fat body tissues of reproducing queens (~2 to 3 times higher than in diapausing queens and 4 to 10 times higher than in virgins; Figures 4A–C, Supplementary Table S2). Here, IGF-1 was present in all investigated tissues except for the digestive tract.


Gene Expression Dynamics in Major Endocrine Regulatory Pathways along the Transition from Solitary to Social Life in a Bumblebee, Bombus terrestris
qRT-PCR analysis of tissue-specific relative expression levels of insulin-like growth factor 1 (IGF-1) across castes of B. terrestris. IGF-1 is part of the IIS signaling involved in reproduction and diapause. It is queen-specific (i.e., absent in workers and males) and lowest in virgin queens (see main text). Data represent mean ± SEM (n = 3–5) of normalized and rescaled expression levels. (A) Heatmap: Log-scale. Bar graphs: Relative transcript levels in (B) linear scale; and (C) log-transformed scale. Significantly different expression levels are indicated by different letters (p < 0.05).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5121236&req=5

Figure 4: qRT-PCR analysis of tissue-specific relative expression levels of insulin-like growth factor 1 (IGF-1) across castes of B. terrestris. IGF-1 is part of the IIS signaling involved in reproduction and diapause. It is queen-specific (i.e., absent in workers and males) and lowest in virgin queens (see main text). Data represent mean ± SEM (n = 3–5) of normalized and rescaled expression levels. (A) Heatmap: Log-scale. Bar graphs: Relative transcript levels in (B) linear scale; and (C) log-transformed scale. Significantly different expression levels are indicated by different letters (p < 0.05).
Mentions: IGF-1 was expressed exclusively in queens (Figures 4A–C). In virgins, only spurious expression was detected in brain, hypopharyngeal glands, fat body, and ovaries. Higher expression values were observed in diapausing queens, where the ventriculus also contained IGF-1 transcripts. The highest expression occurred in brain, hypopharyngeal glands and fat body tissues of reproducing queens (~2 to 3 times higher than in diapausing queens and 4 to 10 times higher than in virgins; Figures 4A–C, Supplementary Table S2). Here, IGF-1 was present in all investigated tissues except for the digestive tract.

View Article: PubMed Central - PubMed

ABSTRACT

Understanding the social evolution leading to insect eusociality requires, among other, a detailed insight into endocrine regulatory mechanisms that have been co-opted from solitary ancestors to play new roles in the complex life histories of eusocial species. Bumblebees represent well-suited models of a relatively primitive social organization standing on the mid-way to highly advanced eusociality and their queens undergo both, a solitary and a social phase, separated by winter diapause. In the present paper, we characterize the gene expression levels of major endocrine regulatory pathways across tissues, sexes, and life-stages of the buff-tailed bumblebee, Bombus terrestris, with special emphasis on critical stages of the queen's transition from solitary to social life. We focused on fundamental genes of three pathways: (1) Forkhead box protein O and insulin/insulin-like signaling, (2) Juvenile hormone (JH) signaling, and (3) Adipokinetic hormone signaling. Virgin queens were distinguished by higher expression of forkhead box protein O and downregulated insulin-like peptides and JH signaling, indicated by low expression of methyl farnesoate epoxidase (MFE) and transcription factor Kr&uuml;ppel homolog 1 (Kr-h1). Diapausing queens showed the expected downregulation of JH signaling in terms of low MFE and vitellogenin (Vg) expressions, but an unexpectedly high expression of Kr-h1. By contrast, reproducing queens revealed an upregulation of MFE and Vg together with insulin signaling. Surprisingly, the insulin growth factor 1 (IGF-1) turned out to be a queen-specific hormone. Workers exhibited an expression pattern of MFE and Vg similar to that of reproducing queens. Males were characterized by high Kr-h1 expression and low Vg level. The tissue comparison unveiled an unexpected resemblance between the fat body and hypopharyngeal glands across all investigated genes, sexes, and life stages.

No MeSH data available.


Related in: MedlinePlus