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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 peptide receptor 2 (InR-2) across castes of B. terrestris. InR-2 is a receptor involved in insulin signaling. It is upregulated in gonads (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 7: qRT-PCR analysis of tissue-specific relative expression levels of insulin-like peptide receptor 2 (InR-2) across castes of B. terrestris. InR-2 is a receptor involved in insulin signaling. It is upregulated in gonads (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: InR-2 was expressed ubiquitously, but at low levels, in all stages, except for workers' labial glands (no transcript detected) (Figures 7A–C, Supplementary Table S2). The highest expression occurred in the ovaries of all females. The high expression levels in the gonads might point at a role in reproduction, because IIS controls synthesis of JHs and ecdysteroids, i.e., the main regulators of insect reproductive physiology (reviewed in Antonova et al., 2012; Badisco et al., 2013). Yet, it is clear that InR-2 plays not a single role, given the widespread expression across almost all tissues. If InR-2 is indeed involved in reproduction, the elevated expression in workers' gonads would suggest once again that some workers were prepared to reproduce during the competition phase (Duchateau and Velthuis, 1988).


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 peptide receptor 2 (InR-2) across castes of B. terrestris. InR-2 is a receptor involved in insulin signaling. It is upregulated in gonads (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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Related In: Results  -  Collection

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

Figure 7: qRT-PCR analysis of tissue-specific relative expression levels of insulin-like peptide receptor 2 (InR-2) across castes of B. terrestris. InR-2 is a receptor involved in insulin signaling. It is upregulated in gonads (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: InR-2 was expressed ubiquitously, but at low levels, in all stages, except for workers' labial glands (no transcript detected) (Figures 7A–C, Supplementary Table S2). The highest expression occurred in the ovaries of all females. The high expression levels in the gonads might point at a role in reproduction, because IIS controls synthesis of JHs and ecdysteroids, i.e., the main regulators of insect reproductive physiology (reviewed in Antonova et al., 2012; Badisco et al., 2013). Yet, it is clear that InR-2 plays not a single role, given the widespread expression across almost all tissues. If InR-2 is indeed involved in reproduction, the elevated expression in workers' gonads would suggest once again that some workers were prepared to reproduce during the competition phase (Duchateau and Velthuis, 1988).

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