Review of Venoms of Non-Polydnavirus Carrying Ichneumonoid Wasps

Abstract

Parasitoids are predominantly insects that develop as larvae on or inside their host, also usually another insect, ultimately killing it after various periods of parasitism when both parasitoid larva and host are alive. The very large wasp superfamily Ichneumonoidea is composed of parasitoids of other insects and comprises a minimum of 100,000 species. The superfamily is dominated by two similarly sized families, Braconidae and Ichneumonidae, which are collectively divided into approximately 80 subfamilies. Of these, six have been shown to release DNA-containing virus-like particles, encoded within the wasp genome, classified in the virus family Polydnaviridae. Polydnaviruses infect and have profound effects on host physiology in conjunction with various venom and ovarial secretions, and have attracted an immense amount of research interest. Physiological interactions between the remaining ichneumonoids and their hosts result from adult venom gland secretions and in some cases, ovarian or larval secretions. Here we review the literature on the relatively few studies on the effects and chemistry of these ichneumonoid venoms and make suggestions for interesting future research areas. In particular, we highlight relatively or potentially easily culturable systems with features largely lacking in currently studied systems and whose study may lead to new insights into the roles of venom chemistry in host-parasitoid relationships as well as their evolution.

Keywords: Aphidius; Asobara; Braconidae; Habrobracon; Ichneumonidae; Pimpla.

Figure 1

Summary of biological features of selected ichneumonoid subfamilies and probable ease of maintaining in culture. For ease of viewing the following rare subfamilies have been omitted: the braconids—Acampsohelconinae, Amicrocentrinae, Apozyginae, Maxfischeriinae, Microtypinae, Telengaiinae and Xiphozelinae; the ichneumonids—Acaenitinae, Agriotypinae, Clasinae, Cylloceriinae, Diacritinae, Eucerotinae, Hybrizontinae, Masoninae, Microleptinae, Nesomesochorinae, Oxytorinae, Pedunculinae, Sisyrostolinae and Tatogastrinae. (Phylogeny hand-drawn based upon a consensus from [4,6,7,8,9]).

Figure 2

Dissected venom glands and reservoirs or their chitinous intima. (A), dissected venom glands and reservoir of Diadromus collaris (Ichneumonidae: Ichneumoninae) from [56] (Reproduced under the terms of Creative Commons Attribution Licence CC-BY 4.0 via Scientific Reports), scale bar: 0.2 mm; (B), dissected venom glands and reservoir of Pimpla turionellae from [57] (Reproduced under the terms of Creative Commons Attribution Licence CC-BY 4.0 via Toxins), scale bar: 0.5 mm; (C–E), chlorozol black dyed reservoir, gland and primary duct chitinous intima: (C), gen. sp. (Doryctinae), scale bar: 0.25 mm; (D), Bracon sp. (Braconinae), scale bar: 0.2 mm; (E), Iphiaulax, unidentified species (Braconinae), scale bar: 0.25 mm.

Figure 3

Venom apparatus of two Psyttalia species: (a) P. lounsburyi female venom apparatus composed of a multi-lobed gland (G), a reservoir (R) and a long ovipositor (O); (b) Dissected P. lounsburyi venom gland showing the thick tissue envelope of the gland and the basal lateral branching of the reservoir; (c) P. concolor venom apparatus evidencing the small round gland at the base of the apparatus (Rg); (d) the same, overlaid with a fluorescence micrograph showing the green auto-fluorescence of the internal spirals of the reservoir and the small round gland. Bars = 100 μm. (Source: from [55] reproduced under the terms of Creative Commons Attribution Licence CC-BY 4.0 via Scientific Reports).

Figure 4

Diachasmimorpha longicaudata venom glands with abundant entomopox virus (DlEVP) in their lumens, and escape of virions into surrounding medium from puncture of lower filament in upper right venom apparatus. (Source: courtesy of Kelsey Anne Coffman, Univerity of Georgia, Athens, GA, USA).

Figure 5

SDS-PAGE separation of A. tabida venom extracts and asparaginase (AGA) immunostaining. Electrophoretic profiles of venom extracts and immunostaining of AGA under non-reducing conditions (nr) and reducing conditions (r). Gels were silver-stained or analyzed by western blot using the anti-hAGA and anti-P30. The two subunits are indicated α and β, and the heterodimer by αβ. (A. tabida AGA) antibodies. (Source: from [142] under the terms of Creative Commons Attribution Licence CC-BY 4.0 via PLoS ONE).

Figure 6

Effects of Asobara japonica venom and treated venom on the survivorship of D. melanogaster larvae one day after injection. Enzymatic treatments were conducted for 2 h at 25 °C (trypsin) or 37 °C (the others). (Source: redrawn based on [149] under the terms of Creative Commons Attribution Licence CC-BY 4.0 via PLoS ONE). N.S.: not significant.

Figure 7

Effects of Asobara japonica venom and products of ultracentrifugation on survivorship of D. melanogaster larvae one day after injection. (Source: redrawn based on [149] under the terms of Creative Commons Attribution Licence CC-BY 4.0 via PLoS ONE). N.S.: not significant.

Figure 8

TEM section of pellet obtained by ultracentrifugation of Asobara japonica venom at 450,000 g. (Source: from [149] under the terms of Creative Commons Attribution Licence CC-BY 4.0 via PLoS ONE).

Figure 9

Time course of reduction and loss of miniature parasitism-specific proteins (PSPs) in the silk moth Philosamia cynthia following injection of H. hebetor venom (Source: data from [184]).

Figure 10

Examples of melanotic encapsulation response to plastic implant by G. mellonella larva naturally envenomated by H. hebetor. (A), initial implant, (B), control (untreated) larva 24 h post treatment. (C), envenomated larva, 24 hrs post treatment. (Source: reproduced by permission of Ivan Dubovskiy, Novosibirsk State Agrarian University, Russia).

Figure 11

Coomassie Brilliant Blue G250 stained, SDS-PAGE of H. nigricans venom extract with known molecular weight protein ladder on left, showing numbered protein bands that were analysed separately. Left hand lane (M) shows protein molecular weight markers, right hand lane shows venom (V) proteins. (Source from [51] under the terms of Creative Commons Attribution Licence CC-BY 4.0 via BMC Genomics).

Figure 12

Expression of selected genes in terms of abundance of transcripts measured by qRT-PCR in H. nigricans females with their venom glands removed, whole males, and isolated venom glands. Results are presented as mean fold changes on a logarithmic scale, based of three independent biological replicates. Values are standardised with respect to females that had had their venom glands removed and which were assigned a value of 1. Error bars indicate standard error and letters indicate significant difference adjusted for multiple tests using Tukey’s HSD (Source: data from Figure 4 in [51]).

Figure 13

Effects of injection of M. pulchricornis products into northern armyworm, Mythimna separata (Noctuidae) caterpillars parasitised (on the same day) by Cotesia kariyai. Different letters above columns indicate significantly different values at 5% level using Tukey–Kramer test. (Data from Table 2B in [205]).

Figure 14

Gene gains and losses of parasitism-associated gene families of Macrocentrus cingulum (Braconidae: Macrocentrinae) and a range of other hymenopterans. (A) Number of gene families with apparent expansion/contraction among M. cingulum and 12 other species. (B) Gene families with significant contraction or expansion. (C) Numbers of venom proteins in different parasitic wasps. (Source: from [54] reproduced under the terms of Creative Commons Attribution Licence CC-BY 4.0 via BMC Genomics).

Figure 15

1D SDS-PAGE separation of P. lounsburyi (Pl_AS and Pl_K strains from Kenya and South Africa, respectively) and P. concolor venom proteins under reducing conditions and silver staining. Stained protein bands (numbered) excised and submitted for protein identification by LC-MS-MS. (Source: from [55] reproduced under the terms of Creative Commons Attribution Licence CC-BY 4.0 via Scientific Reports).

Figure 16

Melanisation of Sephadex DEAE A-25 beads in Galleria mellonella pupae and larvae experimentally envenomated and parasitised by P. turionellae after 4 and 24 h. (Source: data from Tables 4 and 5 [246]).

Figure 17

Effect of P. turionellae venom and parasitisation on host, Galleria mellonella haemocyte health and viability (Source: data from [250]).

Figure 18

Transcript diversity and expression levels of identified known venom protein families (Source: from [57], reproduced under the terms of Creative Commons Attribution Licence CC-BY 4.0 via Toxins).