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Differential gene expression and protein abundance evince ontogenetic bias toward castes in a primitively eusocial wasp.

Hunt JH, Wolschin F, Henshaw MT, Newman TC, Toth AL, Amdam GV - PLoS ONE (2010)

Bottom Line: Even so, Polistes colonies have a temporal pattern in which most female larvae reared by the foundress become workers, and most reared by workers become future-reproductive gynes.We found that foundress-reared larvae (putative worker-destined) and worker-reared larvae (putative gyne-destined) differed in quantitative expression of sixteen genes, twelve of which were associated with caste and/or diapause in other insects, and they also differed in abundance of nine peptides/proteins.Although not conclusive, our results support hypotheses of 1) larval developmental pathway divergence that can lead to caste bias in adults and 2) nutritional differences as the foundation of the pathway divergence.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina, United States of America. jim_hunt@ncsu.edu

ABSTRACT
Polistes paper wasps are models for understanding conditions that may have characterized the origin of worker and queen castes and, therefore, the origin of paper wasp sociality. Polistes is "primitively eusocial" by virtue of having context-dependent caste determination and no morphological differences between castes. Even so, Polistes colonies have a temporal pattern in which most female larvae reared by the foundress become workers, and most reared by workers become future-reproductive gynes. This pattern is hypothesized to reflect development onto two pathways, which may utilize mechanisms that regulate diapause in other insects. Using expressed sequence tags (ESTs) for Polistes metricus we selected candidate genes differentially expressed in other insects in three categories: 1) diapause vs. non-diapause phenotypes and/or worker vs. queen differentiation, 2) behavioral subcastes of worker honey bees, and 3) no a priori expectation of a role in worker/gyne development. We also used a non-targeted proteomics screen to test for peptide/protein abundance differences that could reflect larval developmental divergence. We found that foundress-reared larvae (putative worker-destined) and worker-reared larvae (putative gyne-destined) differed in quantitative expression of sixteen genes, twelve of which were associated with caste and/or diapause in other insects, and they also differed in abundance of nine peptides/proteins. Some differentially-expressed genes are involved in diapause regulation in other insects, and other differentially-expressed genes and proteins are involved in the insulin signaling pathway, nutrient metabolism, and caste determination in highly social bees. Differential expression of a gene and a peptide encoding hexameric storage proteins is especially noteworthy. Although not conclusive, our results support hypotheses of 1) larval developmental pathway divergence that can lead to caste bias in adults and 2) nutritional differences as the foundation of the pathway divergence. Finally, the differential expression in Polistes larvae of genes and proteins also differentially expressed during queen vs. worker caste development in honey bees may indicate that regulatory mechanisms of caste outcomes share similarities between primitively eusocial and advanced eusocial Hymenoptera.

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Quantities of four peptides/proteins significantly differentially expressed in foundress-reared vs. worker-reared P. metricus fifth-instar larvae.Quantities of four peptides/proteins significantly differentially expressed in foundress-reared (FR; putative worker-destined) vs. worker-reared (WR; putative gyne-destined) P. metricus fifth-instar larvae: median (dark squares), 25th-75 th percentiles (brackets), and outliers (open circles). Stars denote significant differences (Mann Whitney U-test, p≤0.05, n = 5 per group). Y-axis: spectral count for individual peptides/proteins corrected for overall spectral count. Sequences are homologous to: (a) arylphorin of the boll weevil (NCBI accession AAN63347); (b) serpin (contig 46732, rf 18257); (c) imaginal disc growth factor 4 (contig 46769); (d) shrub (contig 32130).
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pone-0010674-g003: Quantities of four peptides/proteins significantly differentially expressed in foundress-reared vs. worker-reared P. metricus fifth-instar larvae.Quantities of four peptides/proteins significantly differentially expressed in foundress-reared (FR; putative worker-destined) vs. worker-reared (WR; putative gyne-destined) P. metricus fifth-instar larvae: median (dark squares), 25th-75 th percentiles (brackets), and outliers (open circles). Stars denote significant differences (Mann Whitney U-test, p≤0.05, n = 5 per group). Y-axis: spectral count for individual peptides/proteins corrected for overall spectral count. Sequences are homologous to: (a) arylphorin of the boll weevil (NCBI accession AAN63347); (b) serpin (contig 46732, rf 18257); (c) imaginal disc growth factor 4 (contig 46769); (d) shrub (contig 32130).

Mentions: Quantification of expression was performed on putative proteins, as identified by database entry hits. One or more peptides of a single mature protein can belong to one or several database entry hits, thus one protein might produce more than one hit entry. Of these database entry hits, 9 were significantly quantitatively different between the two sets of larvae (Figure 1; Table S5), and 7 were supported by at least two distinct peptides (Table S5). The hits included a peptide homologous to the hexameric storage protein arylphorin from the boll weevil, Anthonomus grandis, and that protein was identified in both in-gel and in-liquid digestion samples. Other hits indicated that several peptides homologous to an imaginal disc growth factor were up-regulated in gyne-destined larvae: a nuclear ribonucleoprotein; shrub; serpin; and apolipophorin-III (Figure 1; Table S5). Figure 3 illustrates the magnitude of differences for arylphorin, serpin, imaginal disc growth factor 4, and a shrub-like protein.


Differential gene expression and protein abundance evince ontogenetic bias toward castes in a primitively eusocial wasp.

Hunt JH, Wolschin F, Henshaw MT, Newman TC, Toth AL, Amdam GV - PLoS ONE (2010)

Quantities of four peptides/proteins significantly differentially expressed in foundress-reared vs. worker-reared P. metricus fifth-instar larvae.Quantities of four peptides/proteins significantly differentially expressed in foundress-reared (FR; putative worker-destined) vs. worker-reared (WR; putative gyne-destined) P. metricus fifth-instar larvae: median (dark squares), 25th-75 th percentiles (brackets), and outliers (open circles). Stars denote significant differences (Mann Whitney U-test, p≤0.05, n = 5 per group). Y-axis: spectral count for individual peptides/proteins corrected for overall spectral count. Sequences are homologous to: (a) arylphorin of the boll weevil (NCBI accession AAN63347); (b) serpin (contig 46732, rf 18257); (c) imaginal disc growth factor 4 (contig 46769); (d) shrub (contig 32130).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2871793&req=5

pone-0010674-g003: Quantities of four peptides/proteins significantly differentially expressed in foundress-reared vs. worker-reared P. metricus fifth-instar larvae.Quantities of four peptides/proteins significantly differentially expressed in foundress-reared (FR; putative worker-destined) vs. worker-reared (WR; putative gyne-destined) P. metricus fifth-instar larvae: median (dark squares), 25th-75 th percentiles (brackets), and outliers (open circles). Stars denote significant differences (Mann Whitney U-test, p≤0.05, n = 5 per group). Y-axis: spectral count for individual peptides/proteins corrected for overall spectral count. Sequences are homologous to: (a) arylphorin of the boll weevil (NCBI accession AAN63347); (b) serpin (contig 46732, rf 18257); (c) imaginal disc growth factor 4 (contig 46769); (d) shrub (contig 32130).
Mentions: Quantification of expression was performed on putative proteins, as identified by database entry hits. One or more peptides of a single mature protein can belong to one or several database entry hits, thus one protein might produce more than one hit entry. Of these database entry hits, 9 were significantly quantitatively different between the two sets of larvae (Figure 1; Table S5), and 7 were supported by at least two distinct peptides (Table S5). The hits included a peptide homologous to the hexameric storage protein arylphorin from the boll weevil, Anthonomus grandis, and that protein was identified in both in-gel and in-liquid digestion samples. Other hits indicated that several peptides homologous to an imaginal disc growth factor were up-regulated in gyne-destined larvae: a nuclear ribonucleoprotein; shrub; serpin; and apolipophorin-III (Figure 1; Table S5). Figure 3 illustrates the magnitude of differences for arylphorin, serpin, imaginal disc growth factor 4, and a shrub-like protein.

Bottom Line: Even so, Polistes colonies have a temporal pattern in which most female larvae reared by the foundress become workers, and most reared by workers become future-reproductive gynes.We found that foundress-reared larvae (putative worker-destined) and worker-reared larvae (putative gyne-destined) differed in quantitative expression of sixteen genes, twelve of which were associated with caste and/or diapause in other insects, and they also differed in abundance of nine peptides/proteins.Although not conclusive, our results support hypotheses of 1) larval developmental pathway divergence that can lead to caste bias in adults and 2) nutritional differences as the foundation of the pathway divergence.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina, United States of America. jim_hunt@ncsu.edu

ABSTRACT
Polistes paper wasps are models for understanding conditions that may have characterized the origin of worker and queen castes and, therefore, the origin of paper wasp sociality. Polistes is "primitively eusocial" by virtue of having context-dependent caste determination and no morphological differences between castes. Even so, Polistes colonies have a temporal pattern in which most female larvae reared by the foundress become workers, and most reared by workers become future-reproductive gynes. This pattern is hypothesized to reflect development onto two pathways, which may utilize mechanisms that regulate diapause in other insects. Using expressed sequence tags (ESTs) for Polistes metricus we selected candidate genes differentially expressed in other insects in three categories: 1) diapause vs. non-diapause phenotypes and/or worker vs. queen differentiation, 2) behavioral subcastes of worker honey bees, and 3) no a priori expectation of a role in worker/gyne development. We also used a non-targeted proteomics screen to test for peptide/protein abundance differences that could reflect larval developmental divergence. We found that foundress-reared larvae (putative worker-destined) and worker-reared larvae (putative gyne-destined) differed in quantitative expression of sixteen genes, twelve of which were associated with caste and/or diapause in other insects, and they also differed in abundance of nine peptides/proteins. Some differentially-expressed genes are involved in diapause regulation in other insects, and other differentially-expressed genes and proteins are involved in the insulin signaling pathway, nutrient metabolism, and caste determination in highly social bees. Differential expression of a gene and a peptide encoding hexameric storage proteins is especially noteworthy. Although not conclusive, our results support hypotheses of 1) larval developmental pathway divergence that can lead to caste bias in adults and 2) nutritional differences as the foundation of the pathway divergence. Finally, the differential expression in Polistes larvae of genes and proteins also differentially expressed during queen vs. worker caste development in honey bees may indicate that regulatory mechanisms of caste outcomes share similarities between primitively eusocial and advanced eusocial Hymenoptera.

Show MeSH
Related in: MedlinePlus