Storage proteins in vespid wasps: characterization, developmental pattern, and occurrence in adults

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Abstract

Wasps of family Vespidae contain three types of major proteins that have the size, amino acid composition, subunit composition, immunological reactivity, and pattern of occurrence characteristic of storage proteins. The three types of storage protein, which have been identified in other Hymenoptera, are very high density lipoprotein, high glutamine/glutamic acid protein, and hexamerin. The predominant pattern of occurrence for these proteins is as known from most or all Holometabola: synthesis during the last larval instar and utilization as an amino acid source during metamorphosis. Hexamerin also occurred in a large young adult female Monobia quadridens but not a small one, which suggests that carry-over into adult females is a reaction norm response to quantity of larval provisions, because these wasps could not have fed as adults. In two paper wasp species of the genus Polistes, hexamerin was present in large adult females which emerged during the colony cycle phase when reproductive females are typically produced, but not in adult female offspring that emerged earlier in the colony cycle or in adult females that were workers. It cannot be confirmed by these data that the hexamerin in the adult paper wasps represented carry-over from metamorphosis rather than post-emergence feeding, but the pattern of occurrence suggests that presence of storage protein may play a role in caste differentiation in paper wasps. No storage protein was found in any adult Vespula maculifrons, a yellowjacket wasp, suggesting that caste differentiation in vespine wasps does not incorporate storage protein as a component.

Introduction

Berlese (1900) was the first to report presence of protein in the insect fat body. The intracellular protein granules (‘albuminoidi’) that he described drew considerable attention from insect histologists of the time. Pardi (1939) extensively reviews that classical literature and presents his own photomicrographs and drawings of the ‘globuli proteici di riserva’—storage protein globules. Storage proteins are now known to be large molecular weight proteins that occur in most or all holometabolous insects. Their most frequent function explains the pattern, observed by Berlese and detailed by Pardi, of occurrence in close association with metamorphosis: they provide amino acid storage at the end of larval growth prior to serving as a supply of amino acids for tissue building during metamorphosis (reviewed in Levenbook, 1985). An increasing number of cases have also been identified in which storage proteins are important in adult insects (e.g. Capurro et al., 1997, Wheeler et al., 2000).

Storage proteins play diverse roles in adult social Hymenoptera, which are often characterized by long lifetimes as well as by group living and division of reproductive effort. Koehler (1921) reported that protein is present in large quantities in the fat body of worker honeybees early in the temperate zone winter but that by spring most of that protein is gone. Martinez and Wheeler, 1991a, Martinez and Wheeler, 1991b, Martinez and Wheeler, 1993 showed that storage proteins accumulate in hemolymph and fat body of worker ants held in queenless groups. In new queens of claustrally founding ants, which do not forage for food, storage proteins are present (Martinez and Wheeler, 1994, Wheeler and Buck, 1994) and play a significant role in provisioning the queen’s first brood (Martinez and Wheeler, 1994, Wheeler and Buck, 1996). Three types of storage proteins have been identified in Hymenoptera (Wheeler and Buck, 1994): hexamerins, a protein high in glutamtine/glutamic acid (HiGLX), and a dimeric very high density lipoprotein (VHDL).

Here we investigate the occurrence, characterization and life history correlations of storage proteins in the hymenopteran family Vespidae. Focal taxa are a solitary wasp, Monobia quadridens (subfamily Eumeninae), two eusocial paperwasps, Polistes metricus and P. fuscatus (Polistinae), and two highly eusocial yellowjackets, Dolichovespula maculata and Vespula maculifrons (Vespinae). Specimens were collected at phases of their annual life cycles that could reveal if storage proteins might be present in newly emerged adults and, if so, if any pattern of presence might indicate involvement of storage proteins in female caste differentiation. Most eumenines are solitary and so they have no castes, although females of a species can vary in size. In most species of the highly eusocial Vespinae, female castes (queen and worker) differ conspicuously in size and morphology as a consequence of differences in larval ontogeny that have long been recognized (Marchal, 1897). Queens and workers also differ in size and/or shape in a number of genera of Neotropical swarm-founding Polistinae (e.g. Jeanne et al., 1995; Hunt et al., 1997; see especially Noll, 2000), whereas in Polistes, the sister genus to all other eusocial Polistinae (Carpenter, 1991), castes do not differ in external morphology, although queens are generally, but not always, larger than workers (e.g. Haggard and Gamboa, 1980, for P. metricus). A role for differences during larval ontogeny in at least predisposition of caste in Polistes has long been suspected (e.g. Roubaud, 1916), yet the actual role, if any, of larval ontogeny in Polistes caste differentiation is still unresolved (O’Donnell, 1998).

Section snippets

Wasps

All specimens were field-collected in 1999 near St. Louis, MO. Colonies of Polistes metricus, Polistes fuscatus, and Dolichovespula maculata had been naturally founded in early spring in boxes placed as wasp nest shelters in oldfield habitats at Shaw Nature Reserve, Gray Summit, Franklin County, MO. Entire colonies of P. metricus were collected early on the mornings of July 6 and July 30. The earlier date is during the time of the colony cycle in Missouri when worker P. metricus offspring are

Identification and characterization of proteins

Proteins were characterized on the basis of molecular mobilities on PAGE gels, binding to antibody in a western blot, and amino acid composition. A non-denaturing gel of extracts of Polistes metricus (Fig. 1) and denaturing gels of extracts of five species of Vespidae (Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8) showed presence of proteins with native and subunit molecular weights consistent with three classes of storage proteins: VHDL, HiGLX, and hexamerins. A similar array of storage proteins

Discussion

As in other Hymenoptera, vespid wasps have three classes of storage proteins: hexamerins, high glutamine/glutamic acid protein, and a very high density lipoprotein. Results of two-dimensional gel electrophoresis suggest the existence of at least three different members of the hexamerin family, as found in ants. These are the two hexamerin-type hexamerins and HiGLX protein, which seems to be restricted to Hymenoptera (Danty et al., 1998, Burmester, 1999). VHDL, which is found in Lepidoptera as

Acknowledgements

We thank James C. Trager for enabling our field work at Shaw Nature Reserve and Owen J. Sexton for enabling our field work at Tyson Research Center. John A. Eimes generously provided the Monobia specimens and helped collect the Vespula colony. Dan Hahn helped with the average amino acid calculations. Stefano Turillazzi alerted us to an historical reference. An anonymous reviewer made helpful comments. JHH was supported in part by a University of Missouri Research Board Award.

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