Behavioral genomics of honeybee foraging and nest defense

Hunt, Greg J.; Amdam, Gro V.; Schlipalius, David I.; Emore, Christine; Sardesai, Nagesh; Williams, Christie E.; Rueppell, Olav; Guzmán-Novoa, Ernesto; Arechavaleta-Velasco, Miguel E.; Chandra, Sanjeev; Fondrk, M. Kim; Beye, Martin; Page, Robert E.

doi:10.1007/s00114-006-0183-1

Cited by 190 publications

(216 citation statements)

References 72 publications

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“…Third, seven of the genes on the alarm pheromone list are located within previously identified quantitative trait loci for AHB aggression, as are 12 from the AHB list (21) ( Table S3). Among them, 14-3-3 , a gene up-regulated in the brains of human suicide victims (22), was up-regulated in AHB soldier brains in this study and also in a relatively aggressive EHB strain (21). These and other genes that appear on one or more of our gene lists are good candidates for effectors of honey bee aggression.…”

Section: Common Brain Transcriptional Network Associated With Inherimentioning

confidence: 52%

“…In addition, the extent to which the three gene lists share the same motif association(s) is statistically significant (P Ͻ 0.001, see SI Text, Extreme Value Distribution). The motifs included Deaf1, which targets a transcription factor associated with biogenic amine signaling (27) that has been implicated in aggression in vertebrates (19) and invertebrates (20,21), and Trl (GAGA-binding factor), a motif previously found to be associated with differences in brain gene expression between young and old bees (28). Remarkably, these same results occurred even when all genes common to the three gene lists were removed (Table 4).…”

Section: Common Brain Transcriptional Network Associated With Inherimentioning

confidence: 70%

“…Consistent with these results, exposing EHB to alarm pheromone at the hive entrance for 1 min affected brain expression of hundreds of genes, measured 1 h later (Table 1). Among the genes significantly up-regulated were several involved in biogenic amine signaling (Dopa decarboxylase, Tyramine receptor, and Octopamine receptor beta-2), which have been implicated in the regulation of aggression in both vertebrates (19) and invertebrates (20,21). c-Jun was also up-regulated again [false discovery rate (FDR) adjusted P value ϭ 0.1].…”

Section: Resultsmentioning

confidence: 99%

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Honey bee aggression supports a link between gene regulation and behavioral evolution

Alaux

Sinha²,

Hasadsri

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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246

387

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A prominent theory states that animal phenotypes arise by evolutionary changes in gene regulation, but the extent to which this theory holds true for behavioral evolution is not known. Because ''nature and nurture'' are now understood to involve hereditary and environmental influences on gene expression, we studied whether environmental influences on a behavioral phenotype, i.e., aggression, could have evolved into inherited differences via changes in gene expression. Here, with microarray analysis of honey bees, we show that aggression-related genes with inherited patterns of brain expression are also environmentally regulated. There were expression differences in the brain for hundreds of genes between the highly aggressive Africanized honey bee compared with European honey bee (EHB) subspecies. Similar results were obtained for EHB in response to exposure to alarm pheromone (which provokes aggression) and when comparing old and young bees (aggressive tendencies increase with age). There was significant overlap of the gene lists generated from these three microarray experiments. Moreover, there was statistical enrichment of several of the same cis regulatory motifs in promoters of genes on all three gene lists. Aggression shows a remarkably robust brain molecular signature regardless of whether it occurs because of inherited, age-related, or environmental (social) factors. It appears that one element in the evolution of different degrees of aggressive behavior in honey bees involved changes in regulation of genes that mediate the response to alarm pheromone.

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Section: Common Brain Transcriptional Network Associated With Inherimentioning

confidence: 52%

Section: Common Brain Transcriptional Network Associated With Inherimentioning

confidence: 70%

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Honey bee aggression supports a link between gene regulation and behavioral evolution

Alaux

Sinha²,

Hasadsri

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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246

387

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“…Insulin signaling has been implicated in the regulation of caste (queen vs. worker) determination in honey bees (27,54), and insulin-signaling genes are among the more promising candidate genes located in quantitative trait loci associated with genetic variation for honey bee foraging behavior (55). Several models have been proposed to explain how insulin signaling can influence diverse aspects of phenotypic plasticity in honey bees (22,55,56). Our experiments confirm a specific prediction of Corona et al (22) by showing that low nutrient stores can increase insulin signaling.…”

Section: Nursing) (E) Expression Of Ilp1 In Brains Of Nurses and Formentioning

confidence: 99%

Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies

Ament

Corona

Pollock

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

310

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It has been proposed that one route of behavioral evolution involves novel regulation of conserved genes. Age-related division of labor in honey bee colonies, a highly derived behavioral system, involves the performance of different feeding-related tasks by different groups of individuals. Older bees acquire the colony's food by foraging for nectar and pollen, and the younger ''nurse'' bees feed larvae processed foods. The transition from hive work to foraging has been shown to be socially regulated and associated both with decreases in abdominal lipid stores and with increases in brain expression of genes implicated in feeding behavior in Drosophila melanogaster. Here we show that division of labor is influenced by a canonical regulator of food intake and energy balance in solitary species, the insulin/insulin-like growth factor signaling (IIS) pathway. Foragers had higher levels of IIS gene expression in the brain and abdomen than did nurses, despite their low lipid stores. These differences are likely nutritionally mediated because manipulations that induced low lipid stores in young bees also up-regulated these genes. Changes in IIS also causally influenced the timing of behavioral maturation: inhibition of the insulin-related target of rapamycin pathway delayed the onset of foraging in a seasonally dependent manner. In addition, pathway analyses of microarray data revealed that nurses and foragers differ in brain energy metabolism gene expression, but the differences are opposite predictions based on their insulin-signaling status. These results suggest that changes in the regulation of the IIS pathway are associated with social behavior.Apis mellifera ͉ behavioral maturation ͉ social insect ͉ nutrition ͉ foraging A n important problem in biology is to understand the molecular basis for complex behavior. It has been proposed that one route of behavioral evolution involves novel regulation of conserved genes (1). It is well established that orthologous sets of genes regulate the development of body plans across taxa (2), but this idea has only recently begun to be tested for behavior (3,4).Age-related division of labor in honey bee colonies involves the performance of different food-related tasks by different groups of individuals. Nurse bees feed brood for the first 1-2 weeks of adult life, process and store food for another week, and then shift to foraging for nectar and pollen at Ϸ2-3 weeks of age (5). This division of labor is socially regulated; bees speed up, slow down, or reverse their maturation in response to colony needs (6). Although the mechanics of foraging in honey bees are similar to food-gathering in solitary bees, there are fundamental differences. Honey bees forage to improve the fitness of the colony rather than their own; they collect food when their colony needs it. Honey bees feed on honey before exiting the hive to fuel their foraging flights, and most of the food obtained on a foraging trip is not for their own sustenance.We hypothesized that the regulation of honey bee behavioral mat...

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“…Whereas octopamine has been studied in detail and has been shown to affect age-dependent division of labour between nurse bees and foragers, tyramine has received little attention (for review, see Scheiner et al, 2006). However, the tyramine receptor gene Amtyr1 is a candidate gene in a quantitative trait locus correlating with different aspects of foraging behaviour (Hunt et al, 2007) and tyramine can increase the sucrose responsiveness of nectar foragers to the level of pollen foragers (Scheiner et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

The honey bee tyramine receptor AmTYR1 and division of foraging labor

Scheiner

Kulikovskaja

Thamm

2013

Journal of Experimental Biology

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Honey bees display a fascinating division of labour among foragers. While some bees solely collect pollen, others only collect nectar. It is assumed that individual differences in sensory response thresholds are at the basis of this division of labour. Biogenic amines and their receptors are important candidates for regulating the division of labour, because they can modulate sensory response thresholds. Here, we investigated the role of the honey bee tyramine receptor AmTYR1 in regulating the division of foraging labour. We report differential splicing of the Amtyr1 gene and show differential gene expression of one isoform in the suboesophageal ganglion of pollen and nectar foragers. This ganglion mediates gustatory inputs. These findings imply a role for the honey bee tyramine receptor in regulating the division of foraging labour, possibly through the suboesophageal ganglion.

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Behavioral genomics of honeybee foraging and nest defense

Cited by 190 publications

References 72 publications

Honey bee aggression supports a link between gene regulation and behavioral evolution

Honey bee aggression supports a link between gene regulation and behavioral evolution

Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies

The honey bee tyramine receptor AmTYR1 and division of foraging labor

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