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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 Krüppel homolog 1 (Kr-h1) across castes of B. terrestris. Kr-h1 is a transcription factor downstream of juvenile hormone receptors. It is downregulated in virgin queens, and upregulated in males and diapausing 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 linear scale (B) and log-transformed scale (C). Significantly different expression levels are indicated by different letters (p < 0.05).
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Figure 2: qRT-PCR analysis of tissue-specific relative expression levels of Krüppel homolog 1 (Kr-h1) across castes of B. terrestris. Kr-h1 is a transcription factor downstream of juvenile hormone receptors. It is downregulated in virgin queens, and upregulated in males and diapausing 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 linear scale (B) and log-transformed scale (C). Significantly different expression levels are indicated by different letters (p < 0.05).

Mentions: Our results indicate only low expression of Kr-h1 in virgin queens, except for slightly elevated values in the labial glands, and even lower expression in ovaries (Figures 2A–C, Supplementary Table S2). This is in stark contrast with the other females showing considerably higher expression levels, and to males who had the highest expression values in all tissues but labial glands. Reproducing queens were somewhat intermediary between the very low levels in virgins and the rather high levels in diapausing queens. Across all samples, particularly high expression occurred in labial and hypopharyngeal glands, ventriculus, and fat body.


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 Krüppel homolog 1 (Kr-h1) across castes of B. terrestris. Kr-h1 is a transcription factor downstream of juvenile hormone receptors. It is downregulated in virgin queens, and upregulated in males and diapausing 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 linear scale (B) and log-transformed scale (C). Significantly different expression levels are indicated by different letters (p < 0.05).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5121236&req=5

Figure 2: qRT-PCR analysis of tissue-specific relative expression levels of Krüppel homolog 1 (Kr-h1) across castes of B. terrestris. Kr-h1 is a transcription factor downstream of juvenile hormone receptors. It is downregulated in virgin queens, and upregulated in males and diapausing 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 linear scale (B) and log-transformed scale (C). Significantly different expression levels are indicated by different letters (p < 0.05).
Mentions: Our results indicate only low expression of Kr-h1 in virgin queens, except for slightly elevated values in the labial glands, and even lower expression in ovaries (Figures 2A–C, Supplementary Table S2). This is in stark contrast with the other females showing considerably higher expression levels, and to males who had the highest expression values in all tissues but labial glands. Reproducing queens were somewhat intermediary between the very low levels in virgins and the rather high levels in diapausing queens. Across all samples, particularly high expression occurred in labial and hypopharyngeal glands, ventriculus, and fat body.

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