Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera

Angel R. Barchuk, Alexandre S. Cristino, Robert Kucharski, Luciano F. Costa, Zila L. P. Simoes, Ryszard Maleszka

Research output: Contribution to journalArticle

163 Citations (Scopus)
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Abstract

Background: In honeybees, differential feeding of female larvae promotes the occurrence of two different phenotypes, a queen and a worker, from identical genotypes, through incremental alterations, which affect general growth, and character state alterations that result in the presence or absence of specific structures. Although previous studies revealed a link between incremental alterations and differential expression of physiometabolic genes, the molecular changes accompanying character state alterations remain unknown. Results: By using cDNA microarray analyses of >6,000 Apis mellifera ESTs, we found 240 differentially expressed genes (DEGs) between developing queens and workers. Many genes recorded as up-regulated in prospective workers appear to be unique to A. mellifera, suggesting that the workers' developmental pathway involves the participation of novel genes. Workers up-regulate more developmental genes than queens, whereas queens up-regulate a greater proportion of physiometabolic genes, including genes coding for metabolic enzymes and genes whose products are known to regulate the rate of mass-transforming processes and the general growth of the organism (e.g., tor). Many DEGs are likely to be involved in processes favoring the development of caste-biased structures, like brain, legs and ovaries, as well as genes that code for cytoskeleton constituents. Treatment of developing worker larvae with juvenile hormone (JH) revealed 52 JH responsive genes, specifically during the critical period of caste development. Using Gibbs sampling and Expectation Maximization algorithms, we discovered eight overrepresented cis-elements from four gene groups. Graph theory and complex networks concepts were adopted to attain powerful graphical representations of the interrelation between cis-elements and genes and objectively quantify the degree of relationship between these entities. Conclusion: We suggest that clusters of functionally related DEGs are co-regulated during caste development in honeybees. This network of interactions is activated by nutrition-driven stimuli in early larval stages. Our data are consistent with the hypothesis that JH is a key component of the developmental determination of queen-like characters. Finally, we propose a conceptual model of caste differentiation in A. mellifera based on gene-regulatory networks.
Original languageEnglish
Pages (from-to)1-19
Number of pages19
JournalBMC Developmental Biology
Volume7
DOIs
Publication statusPublished - 2007
Externally publishedYes

Cite this

Barchuk, A. R., Cristino, A. S., Kucharski, R., Costa, L. F., Simoes, Z. L. P., & Maleszka, R. (2007). Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Developmental Biology, 7, 1-19. https://doi.org/10.1186/1471-213X-7-70
Barchuk, Angel R. ; Cristino, Alexandre S. ; Kucharski, Robert ; Costa, Luciano F. ; Simoes, Zila L. P. ; Maleszka, Ryszard. / Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. In: BMC Developmental Biology. 2007 ; Vol. 7. pp. 1-19.
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Barchuk, AR, Cristino, AS, Kucharski, R, Costa, LF, Simoes, ZLP & Maleszka, R 2007, 'Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera', BMC Developmental Biology, vol. 7, pp. 1-19. https://doi.org/10.1186/1471-213X-7-70

Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. / Barchuk, Angel R.; Cristino, Alexandre S.; Kucharski, Robert; Costa, Luciano F.; Simoes, Zila L. P.; Maleszka, Ryszard.

In: BMC Developmental Biology, Vol. 7, 2007, p. 1-19.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera

AU - Barchuk, Angel R.

AU - Cristino, Alexandre S.

AU - Kucharski, Robert

AU - Costa, Luciano F.

AU - Simoes, Zila L. P.

AU - Maleszka, Ryszard

PY - 2007

Y1 - 2007

N2 - Background: In honeybees, differential feeding of female larvae promotes the occurrence of two different phenotypes, a queen and a worker, from identical genotypes, through incremental alterations, which affect general growth, and character state alterations that result in the presence or absence of specific structures. Although previous studies revealed a link between incremental alterations and differential expression of physiometabolic genes, the molecular changes accompanying character state alterations remain unknown. Results: By using cDNA microarray analyses of >6,000 Apis mellifera ESTs, we found 240 differentially expressed genes (DEGs) between developing queens and workers. Many genes recorded as up-regulated in prospective workers appear to be unique to A. mellifera, suggesting that the workers' developmental pathway involves the participation of novel genes. Workers up-regulate more developmental genes than queens, whereas queens up-regulate a greater proportion of physiometabolic genes, including genes coding for metabolic enzymes and genes whose products are known to regulate the rate of mass-transforming processes and the general growth of the organism (e.g., tor). Many DEGs are likely to be involved in processes favoring the development of caste-biased structures, like brain, legs and ovaries, as well as genes that code for cytoskeleton constituents. Treatment of developing worker larvae with juvenile hormone (JH) revealed 52 JH responsive genes, specifically during the critical period of caste development. Using Gibbs sampling and Expectation Maximization algorithms, we discovered eight overrepresented cis-elements from four gene groups. Graph theory and complex networks concepts were adopted to attain powerful graphical representations of the interrelation between cis-elements and genes and objectively quantify the degree of relationship between these entities. Conclusion: We suggest that clusters of functionally related DEGs are co-regulated during caste development in honeybees. This network of interactions is activated by nutrition-driven stimuli in early larval stages. Our data are consistent with the hypothesis that JH is a key component of the developmental determination of queen-like characters. Finally, we propose a conceptual model of caste differentiation in A. mellifera based on gene-regulatory networks.

AB - Background: In honeybees, differential feeding of female larvae promotes the occurrence of two different phenotypes, a queen and a worker, from identical genotypes, through incremental alterations, which affect general growth, and character state alterations that result in the presence or absence of specific structures. Although previous studies revealed a link between incremental alterations and differential expression of physiometabolic genes, the molecular changes accompanying character state alterations remain unknown. Results: By using cDNA microarray analyses of >6,000 Apis mellifera ESTs, we found 240 differentially expressed genes (DEGs) between developing queens and workers. Many genes recorded as up-regulated in prospective workers appear to be unique to A. mellifera, suggesting that the workers' developmental pathway involves the participation of novel genes. Workers up-regulate more developmental genes than queens, whereas queens up-regulate a greater proportion of physiometabolic genes, including genes coding for metabolic enzymes and genes whose products are known to regulate the rate of mass-transforming processes and the general growth of the organism (e.g., tor). Many DEGs are likely to be involved in processes favoring the development of caste-biased structures, like brain, legs and ovaries, as well as genes that code for cytoskeleton constituents. Treatment of developing worker larvae with juvenile hormone (JH) revealed 52 JH responsive genes, specifically during the critical period of caste development. Using Gibbs sampling and Expectation Maximization algorithms, we discovered eight overrepresented cis-elements from four gene groups. Graph theory and complex networks concepts were adopted to attain powerful graphical representations of the interrelation between cis-elements and genes and objectively quantify the degree of relationship between these entities. Conclusion: We suggest that clusters of functionally related DEGs are co-regulated during caste development in honeybees. This network of interactions is activated by nutrition-driven stimuli in early larval stages. Our data are consistent with the hypothesis that JH is a key component of the developmental determination of queen-like characters. Finally, we propose a conceptual model of caste differentiation in A. mellifera based on gene-regulatory networks.

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DO - 10.1186/1471-213X-7-70

M3 - Article

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SP - 1

EP - 19

JO - BMC Developmental Biology

JF - BMC Developmental Biology

SN - 1471-213X

ER -