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.
Highlights
Determination of morphologically and behaviorally distinct worker and reproductive castes occurs during larval development in ants [1], honey bees and stingless bees [2,3], vespine wasps [4,5], and many swarm-founding paper wasps [6], all of which represent ‘‘advanced eusocial’’ [7] insects
We previously found a hexameric storage protein to be differentially expressed in putative worker-destined vs. gyne-destined larvae of P. metricus [37,41], it is meaningful that one candidate
By targeted testing of 38 genes and non-restricted screening of protein levels, we found that mRNA expression of 16 of 38 quantified genes and quantities of 9 peptides/proteins were significantly up-regulated in worker-reared vs. foundress-reared fifth instar larvae of Polistes metricus
Summary
Determination of morphologically and behaviorally distinct worker and reproductive castes occurs during larval development in ants [1], honey bees and stingless bees [2,3], vespine wasps [4,5], and many (but not all) swarm-founding paper wasps [6], all of which represent ‘‘advanced eusocial’’ [7] insects. In contrast to advanced eusocial insects, worker and reproductive castes in ‘‘primitively eusocial’’ [7] insects are not morphologically distinct [3]. A question that bears directly on conditions presumed to have characterized the threshold of insect social evolution [10] is to ask whether the differentiation of workers and gynes (presumptive foundresses and, presumptive future queens) in anatomically monomorphic ‘‘primitively eusocial’’ Hymenoptera has an ontogenetic component, as in advanced eusocial forms. Hunt and Amdam [21] recognized that any adult female Polistes can become either a worker or queen and that worker/queen castes are determined among adults, but they proposed a specific hypothesis for a process whereby larval developmental divergence yields females reared early in the colony cycle that are biased to become workers and females reared later in the colony cycle that are biased to become gynes
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