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Genome-wide analysis of alternative reproductive phenotypes in honeybee workers

Dries Cardoen, Tom Wenseleers, Ulrich R Ernst, Ellen Danneels UGent, Dries Laget UGent, Dirk de Graaf UGent, Liliane Schoofs and Peter Verleyen (2011) MOLECULAR ECOLOGY. 20(19). p.4070-4084
abstract
A defining feature of social insects is the reproductive division of labour, in which workers usually forego all reproduction to help their mother queen to reproduce. However, little is known about the molecular basis of this spectacular form of altruism. Here, we compared gene expression patterns between nonreproductive, altruistic workers and reproductive, non-altruistic workers in queenless honeybee colonies using a whole-genome microarray analysis. Our results demonstrate massive differences in gene expression patterns between these two sets of workers, with a total of 1292 genes being differentially expressed. In nonreproductive workers, genes associated with energy metabolism and respiration, flight and foraging behaviour, detection of visible light, flight and heart muscle contraction and synaptic transmission were overexpressed relative to reproductive workers. This implies they probably had a higher whole-body energy metabolism and activity rate and were most likely actively foraging, whereas same-aged reproductive workers were not. This pattern is predicted from evolutionary theory, given that reproductive workers should be less willing to compromise their reproductive futures by carrying out high-risk tasks such as foraging or other energetically expensive tasks. By contrast, reproductive workers mainly overexpressed oogenesis-related genes compared to nonreproductive ones. With respect to key switches for ovary activation, several genes involved in steroid biosynthesis were upregulated in reproductive workers, as well as genes known to respond to queen and brood pheromones, genes involved in TOR and insulin signalling pathways and genes located within quantitative trait loci associated with reproductive capacity in honeybees. Overall, our results provide unique insight into the molecular mechanisms underlying alternative reproductive phenotypes in honeybee workers.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
BEE APIS-MELLIFERA, microarray, JUVENILE-HORMONE TITERS, reproductive division of labour, Altruism, Apis mellifera, BRAIN GENE-EXPRESSION, CASTE DEVELOPMENT, OVARY DEVELOPMENT, EUSOCIAL HYMENOPTERA, SOCIAL INSECT, HYPOPHARYNGEAL-GLAND, HEMOLYMPH TITERS, DNA METHYLATION
journal title
MOLECULAR ECOLOGY
Mol. Ecol.
volume
20
issue
19
pages
4070 - 4084
Web of Science type
Article
Web of Science id
000295230000011
JCR category
ECOLOGY
JCR impact factor
5.522 (2011)
JCR rank
8/130 (2011)
JCR quartile
1 (2011)
ISSN
0962-1083
DOI
10.1111/j.1365-294X.2011.05254.x
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
2059324
handle
http://hdl.handle.net/1854/LU-2059324
date created
2012-03-05 12:40:17
date last changed
2012-03-26 15:53:02
@article{2059324,
  abstract     = {A defining feature of social insects is the reproductive division of labour, in which workers usually forego all reproduction to help their mother queen to reproduce. However, little is known about the molecular basis of this spectacular form of altruism. Here, we compared gene expression patterns between nonreproductive, altruistic workers and reproductive, non-altruistic workers in queenless honeybee colonies using a whole-genome microarray analysis. Our results demonstrate massive differences in gene expression patterns between these two sets of workers, with a total of 1292 genes being differentially expressed. In nonreproductive workers, genes associated with energy metabolism and respiration, flight and foraging behaviour, detection of visible light, flight and heart muscle contraction and synaptic transmission were overexpressed relative to reproductive workers. This implies they probably had a higher whole-body energy metabolism and activity rate and were most likely actively foraging, whereas same-aged reproductive workers were not. This pattern is predicted from evolutionary theory, given that reproductive workers should be less willing to compromise their reproductive futures by carrying out high-risk tasks such as foraging or other energetically expensive tasks. By contrast, reproductive workers mainly overexpressed oogenesis-related genes compared to nonreproductive ones. With respect to key switches for ovary activation, several genes involved in steroid biosynthesis were upregulated in reproductive workers, as well as genes known to respond to queen and brood pheromones, genes involved in TOR and insulin signalling pathways and genes located within quantitative trait loci associated with reproductive capacity in honeybees. Overall, our results provide unique insight into the molecular mechanisms underlying alternative reproductive phenotypes in honeybee workers.},
  author       = {Cardoen, Dries and Wenseleers, Tom and Ernst, Ulrich R and Danneels, Ellen and Laget, Dries and de Graaf, Dirk and Schoofs, Liliane and Verleyen, Peter},
  issn         = {0962-1083},
  journal      = {MOLECULAR ECOLOGY},
  keyword      = {BEE APIS-MELLIFERA,microarray,JUVENILE-HORMONE TITERS,reproductive division of labour,Altruism,Apis mellifera,BRAIN GENE-EXPRESSION,CASTE DEVELOPMENT,OVARY DEVELOPMENT,EUSOCIAL HYMENOPTERA,SOCIAL INSECT,HYPOPHARYNGEAL-GLAND,HEMOLYMPH TITERS,DNA METHYLATION},
  language     = {eng},
  number       = {19},
  pages        = {4070--4084},
  title        = {Genome-wide analysis of alternative reproductive phenotypes in honeybee workers},
  url          = {http://dx.doi.org/10.1111/j.1365-294X.2011.05254.x},
  volume       = {20},
  year         = {2011},
}

Chicago
Cardoen, Dries, Tom Wenseleers, Ulrich R Ernst, Ellen Danneels, Dries Laget, Dirk de Graaf, Liliane Schoofs, and Peter Verleyen. 2011. “Genome-wide Analysis of Alternative Reproductive Phenotypes in Honeybee Workers.” Molecular Ecology 20 (19): 4070–4084.
APA
Cardoen, D., Wenseleers, T., Ernst, U. R., Danneels, E., Laget, D., de Graaf, D., Schoofs, L., et al. (2011). Genome-wide analysis of alternative reproductive phenotypes in honeybee workers. MOLECULAR ECOLOGY, 20(19), 4070–4084.
Vancouver
1.
Cardoen D, Wenseleers T, Ernst UR, Danneels E, Laget D, de Graaf D, et al. Genome-wide analysis of alternative reproductive phenotypes in honeybee workers. MOLECULAR ECOLOGY. 2011;20(19):4070–84.
MLA
Cardoen, Dries, Tom Wenseleers, Ulrich R Ernst, et al. “Genome-wide Analysis of Alternative Reproductive Phenotypes in Honeybee Workers.” MOLECULAR ECOLOGY 20.19 (2011): 4070–4084. Print.