10. PolyDNA Viruses: Wasp Bioweapons

This was originally written as a final paper for my entomology course. You may or may not notice some parallels between the contents here and some of my other works, namely the focus on fascinating evolutionary transitions. For those of you who don't like the idea of tiny larvae eating other insects from the inside out, perhaps look at one of my pieces about elephants.

Parasitism is a widespread life-strategy across all forms of life, and is found in a grand diversity of taxa. Darwin, in a letter to Asa Gray, stated, “I cannot persuade myself that a beneficent and omnipotent God would have designedly created the Ichneumonidae with the express intention of their feeding within the living bodies of caterpillars [...]” (Darwin, 1860), indicative of the ubiquity of parasitoid in the annals of natural history.  The term “parasitoid” has historically been used to describe insects whose larvae live and feed parasitically upon or within a host until adulthood, often to the exclusion of any other animals that utilize such a lifestyle (Eggleton and Gaston, 1990). Of the insect parasitoids, consisting of approximately 10% of all insect species (Eggletown and Belshaw, 992), approximately three-quarters of these are Hymenoptera (Belshaw et al., 2003). Of these wasps of the superfamily Ichneumonoidea are the most familiar to the layman, with the incredibly diverse and ubiquitous Ichneumonids being far more conspicuous than the less large and species rich Braconids. Both families parasitize hosts across the full range of possible available arthropod hosts, as well as life stages of those hosts; some members are plant parasitoids, although this lifestyle is more common in Cynipidae, the gall wasps (Ronquist and Liljeblad, 2001).

The free-living adults of parasitoids generally differ little morphologically from their nonparasitoid relatives. Mature females locate hosts, whereupon she lays her eggs either on or adjacent to it. Hymenopteran parasitoids have highly specialized ovipositors for both egg manipulation and the stinging of the host. The sting can permanent paralyze the host (typically in the idiobiont lifestyle), or the host may recover and continue feeding (koinobiosis). Cutting ridges at the end of the ovipositor allow wasps to chisel through plant tissue and even wood to access hosts concealed within leafy materials, galls, or beneath bark. Adult parasitoids may feed from flowers, sap fluxes, and other energy sources, and many also feed on potential hosts.

In some cases, the adult female does not lay her eggs on the hsot but on the host’s food plant. There are also some parasitoids that lay their eggs away from the host, whose active free-living first instar larvae responsible for host location. The hosts of parasitoids are almost exclusively insects, although some other arthropod groups are also parasitized. Juvenile stages are most frequently hosts, although a few groups use adult insects. The parasitoids can be identified as egg, larval, pupal, or adult parasitoids depending on the life stage used. Many lay eggs in one stage which endure and feed until a later stage. In hemimetabolous insects there is less distinction made by the parasitoids as regards life-stages.

Life-styles can divided into a number of dichotomies, beginning with the location of the parasitoids while they feed; Endoparasitoids or ectoparasitoids. This dichotomy holds fairly strong, although some species begin as one before transitioning to the other after a few instars. Another dichotomy exists in whether they are present singly or in numbers in/on a host, with numbers ranging multiple orders of magnitude in the gregarious sort. Many complicated elaborations of course exist, allowing for multiple bouts of parasitoidy in a single host, hyperparasitism of the parasitoids themselves by other parasites.

Another significant lifestyle dichotomy is whether the host is allowed to continue to feed and grow after parasitoids become active on them (koinobiosis), or where the host fails to continue developing and are rapidly depleted by the parasitoids (idiobiosis). Idiobonts are found to grow quickly and then have elongated adult stages, which mirrors the shortened lifespan of the stagnated hosts, while koinobonts tend to have prolonged larval stages as they feed on the still growing larvae, and comparatively shorter adult lifespans (Mayhew, 2016). It is typical that idiobonts are egg, pupal, or adult parasitoids, or feed on permanently paralyzed larval prey. Koinobonts, conversely, usually are targeted to egg-larva, larval-pupal, or active larval hosts. Koinobionts success is dependent on their selectively feeding on nonessential organs of their hosts to allow it to continue to feed, providing more resources for the growing parasitoids.

In spite of all this, these dichotomies are often highly variable, and so are more useful for general life-history descriptions than meaningful taxonomic organization.

 

Lifestyle

Koinobiosis and endoparasitism are commonly associated lifestyle traits in opposition to idiobiosis and ectoparasitism, part of the so-called dichotomous hypothesis (Godfray, 1988), and while this is a general trend, as mentioned prior there are numerous exceptions with all combinations found throughout Ichneumonoidea. In the Ichneumonoidea, Braconids are most commonly idiobionts, with the ichneumonids having a broader distribution of the two main side of the dichotomy, with a notably richer diversity of koinobiont endoparasites. Godfray (1988) proposed a number of evolutionary histories for the various forms of parasitoid in both families, and the general consensus seems to support that parasitoids evolved from phytophagous species, who would incidentally consume present insect material, and slowly transitioned to selectively finding and parasitizing these food items (Rasnitsyn, 1980). From here, there are countless proposed evolutionary trajectories to explain the various parasitoid strategies, and within both orders endoparasitism and koinobiosis seem to have occurred multiple times convergently (quicke and Belshaw 1998, more detail below). Braconids have been well-established as a monophyletic group consisting primarily of idiobionts, and much work has been done to explore their phylogeny using both morphological and molecular data (Quicke and Belshaw,1999; Sharanowski et al., 2011) in order to better understand the evolution of their life histories. In Ichneumonids, however, there remains much to be done to properly explore their interrelations, their life histories vary far more, and the monophyly of the group is still unclear.

PolyDNAviruses

The means by which parasitoid wasps overcome the natural defenses of their hosts are numerous, and include a range of weapons including symbiotic polyDNA viruses specific to each family (Braco- and Ichnovirus) (Cook and Stoltz, 1983), venom, teratocytes (special extraembryonic cells), and secretions of the larvae themselves. The polyDNA proviruses exist as endogenous viral elements in the wasp genome, and are delivered virally from egg coatings into the host’s cells, whereupon they are expressed and aid in suppressing host immune systems (Stoltz, 1990; Fleming and Summers, 1991). This viral domestication originates from baculovirus and related nudiviruses, both found as pathogens exclusively in insect systems, and the initial infection of Bracovirus’s ancestral nudivirus predates 100 Mya (Whitfield, 1997; Bezier et al., 2009), while Ichnovirus and other associated Ichnumonid viruses are less established (Herniou et al., 2013). Some wasp genes in turn have entered the viral genome, and unburden the metabolic cost of producing venom components onto the hosts (Webb and Summers, 1990). Bracovirus has been studied rather extensively (Whitfield, 2002; Burke and Strand, 2014; Herniou et al., 2013), and it’s diversification corresponds directly with Braconid evolution (Cook and Stoltz, 1983). What has occurred is a distinct symbiosis between wasp and virus, wherein the expression of the virus aids in the success of the parasitoids, while the parasitoids themselves carry forward the viral genetic line.

 

Livestyle Evolution

In terms of their parasitoid lifestyle, the most conspicuously distinct element that varies between the two families is adult body length and host body length, with Ichneumonids typically being large wasps with large hosts, and Braconids small with small (Traynor 2004). Below the family level, a number of different traits vary greatly, with traits including Ecto/endoparasitoidy, Koino/Idiobiosis, pupation locations (internal v external), and a number of other varying elements of life history (summarized in Mayhew, 2016). What is seen is that at broader taxonomic levels there are fewer distinct differences between the groups, and various elaborations and specializations occur more significantly in more narrow branches of the phylogeny (Mayhew, 2016).

Morphological traits often converge with lifestyle in Ichneumonoids (Quicke and Belshaw, 199), and this incongruence makes appreciating the evolutionary transitions involved in parasitoidy difficult to distinguish. Even a cursory examination of the host specialization of various ichneumonids within a single genus reveals a huge amount of diversity, and frequent specialization nodes with limited clustering of host specificity (Tschopp et al., 2013, see figures 1 and 2, below). Within the genu Ichneumon, which parasitizes Lepidopterans, there is ample scattering of the families of the hosts, and this, within the generic level, is indicative of the degree of variation in wasp/host interrelations. While all of these species are idiobionts on larvae, the adaptation to host pupation sites (above v below ground) seem to have arisen multiple times, and so the ecology of the hosts influences a number of characters of the corresponding parasite, creating multiple convergent events as species shift their hosts.
It has been shown that parasitism has evolved but once in Hymenoptera, with the various elaborations therein such as endoparasitism, and from thence, ectoparasitism, having occuring convergently multiple times (Whitfield, 1998; Quicke and Belshaw, 1999, Downton and Austin, 2001) in both Ichneumonids and Braconids (Quicke, 2009). This in conjunction with the baculo/nudivirus derived PolyDNAviruses which are ubiquitous in Ichneumonoids makes the mapping of the evolution of specific parasite stratagems challenging. While individual elements can be analyzed, building a cohesive picture is fraught with difficulties that remain to be addressed adequately.

Figure 1. Family preference of wasps within a single genus, showing high variation in hosts

Figure 1. Family preference of wasps within a single genus, showing high variation in hosts

Figure 2 Showing host pupation sites within the same species as figure 1, again showing high variation across the phylogeny

Figure 2 Showing host pupation sites within the same species as figure 1, again showing high variation across the phylogeny

What evidence there is suggest that the common evolutionary thread, as briefly summarized above, was a transition of plant-feeding adults facultatively making use of the food resource that was any present boring larvae, transitioning to other insect hosts that may be present in such burrows, and then moving outward to hosts exterior to the plant or fungal sources, obscured pupae, or a combination/reiteration of both. The development of koinobiosis from idiobiosis, ectoparasitism from endoparasitism, and the various life-stages of hosts specialized upon seem to unsurprisingly follow rather sequential patterns. However, the ample abundance of homoplasy in parasitoid behavior makes it difficult to find easily observable gross patterns over the broader framework of Ichneumonoid phylogeny.



 

Citations:

 

Askew, R. R. (1971). Parasitic insects.

Belshaw, R., Fitton, M., Herniou, E., Gimeno, C., & Quicke, D. L. (1998). A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Systematic Entomology, 23(2), 109-123.

Belshaw, R., Grafen, A., & Quicke, D. L. (2003). Inferring life history from ovipositor morphology in parasitoid wasps using phylogenetic regression and discriminant analysis. Zoological Journal of the Linnean Society, 139(2), 213-228.

Belshaw R & Quicke DLJ (2002) Robustness of ancestral state estimates: evolution of life history strategy in ichneumonoid parasitoids. Systematic Biology 51: 450–477

Bézier, A., Annaheim, M., Herbinière, J., Wetterwald, C., Gyapay, G., Bernard-Samain, S., ... & Pfister-Wilhem, R. (2009). Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science, 323(5916), 926-930.

Blackburn, T. M. (1991). A comparative examination of life-span and fecundity in parasitoid Hymenoptera. The Journal of Animal Ecology, 151-164.; Blackburn, T. M. (1991). Evidence for a fast-slow'continuum of life-history traits among parasitoid Hymenoptera. Functional Ecology, 65-74.)

Burke, G. R., & Strand, M. R. (2014). Systematic analysis of a wasp parasitism arsenal. Molecular ecology, 23(4), 890-901.

Cook, D., & Stoltz, D. B. (1983). Comparative serology of viruses isolated from ichneumonid parasitoids. Virology, 130(1), 215-220.

Darwin, C. (1860, May 22). [Letter to Asa Gray].

Djoumad, A., Stoltz, D., Béliveau, C., Boyle, B., Kuhn, L., & Cusson, M. (2013). Ultrastructural and genomic characterization of a second banchine polydnavirus confirms the existence of shared features within this ichnovirus lineage. Journal of General Virology, 94(8), 1888-1895.

Dowton M & Austin AD (2001) Simultaneous analysis of 16S, 28S, COI and morphology in the Hymenoptera: Apocrita – evolutionary transitions among parasitic wasps. Biological Journal of the Linnean Society 74: 87–111.

Eberhard, W. G. (1990). Function and phylogeny of spider webs. Annual Review of Ecology and Systematics, 341-372.; Wenzel, J. W. (1992). Behavioral homology and phylogeny. Annual Review of Ecology and Systematics, 23, 361-381.

Eggleton, P., & Gaston, K. J. (1990). " Parasitoid" Species and Assemblages: Convenient Definitions or Misleading Compromises?. Oikos, 417-421.

Frank, S. A. (1984). The behavior and morphology of the fig wasps, Pegoscapus assuetus and P. jimenszi: descriptions and suggested behavioral characters for phylogenetic studies. Psyche, 91(3-4), 289-308.

Fleming, J. G., & Summers, M. D. (1991). Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proceedings of the National Academy of Sciences, 88(21), 9770-9774.

Gauld, I. D.. (1988). Evolutionary patterns of host utilization by ichneumonoid parasitoids (Hymenoptera: Ichneumonidae and Braconidae). Biological Journal of the Linnean Society, 35(4), 351-377.

Gauld, I. D., & Mound, L. A. (1982). Homoplasy and the delineation of holophyletic genera in some insect groups. Systematic Entomology, 7(1), 73-86.;

Greene, A. (1979). Behavioral characters as indicators of yellowjacket phylogeny (Hymenoptera: Vespidae). Annals of the Entomological Society of America, 72(5), 614-619.; Reconstructing web evolution and spider diversification in the molecular era)

Godfray, H. C. J. (1994). Parasitoids: behavioral and evolutionary ecology. Princeton University Press

Godfray, H. C. J. (2016). Four decades of parasitoid science. Entomologia Experimentalis et Applicata, 159(2), 135-146.

Herniou EA, Huguet E, Thézé J, Bézier A, Periquet G, Drezen JM (2013). "When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses". Philos Trans R Soc Lond B Biol Sci. 368 (1626): 20130051)

Jervis MA, Moe A & Heimpel GE (2012) The evolution of parasitoid fecundity: a paradigm under scrutiny. Ecology Letters15: 357–364.

Laurenne, N. M., Broad, G. R., & Quicke, D. L. (2006). Direct optimization and multiple alignment of 28S D2–D3 rDNA sequences: problems with indels on the way to a molecular phylogeny of the cryptine ichneumon wasps (Insecta: Hymenoptera). Cladistics, 22(5), 442-473.

Mayhew, P. J. (2016). Comparing parasitoid life histories. Entomologia experimentalis et applicata, 159(2), 147-162.

Quicke, D. L., Basibuyuk, H. H., & Rasnitsyn, A. P. (1999). Morphological, palaeontological and molecular aspects of ichneumonoid phylogeny (Hymenoptera, Insecta). Zoologica Scripta, 28(1‐2), 175-202.

Quicke, D. L., & Belshaw, R. (1999). Incongruence between morphological data sets: an example from the evolution of endoparasitism among parasitic wasps (Hymenoptera: Braconidae). Systematic Biology, 48(3), 436-454.

Quicke, D. L., Laurenne, N. M., Fitton, M. G., & Broad, G. R. (2009). A thousand and one wasps: a 28S rDNA and morphological phylogeny of the Ichneumonidae (Insecta: Hymenoptera) with an investigation into alignment parameter space and elision. Journal of Natural History, 43(23-24), 1305-1421.)

Rasnitsyn, A. P., (1980). The origin and evolution hymenopteran insects. Trudy Paleontologischekogo Institute, Akademiya Nauk SSSR 74: 1-91

Ronquist, F., & Liljeblad, J. (2001). Evolution of the gall wasp‐host plant association. Evolution, 55(12), 2503-2522.; Godfray 1994

Sharkey, M. J. (2007). Phylogeny and classification of Hymenoptera. Zootaxa, 1668(521), e548.

Sharanowski, B. J., Dowling, A. P., & Sharkey, M. J. (2011). Molecular phylogenetics of Braconidae(Hymenoptera: Ichneumonoidea), based on multiple nuclear genes, and implications for classification. Systematic Entomology, 36(3), 549-572.

Stoltz, D. B. (1990). Evidence for chromosomal transmission of polydnavirus DNA. Journal of General Virology, 71(5), 1051-1056.

Traynor RE (2004) Life History Evolution in the Parasitoid Hymenopera. PhD Dissertation, University of York, York, UK.

Tschopp, A., Riedel, M., Kropf, C., Nentwig, W., & Klopfstein, S. (2013). The evolution of host associations in the parasitic wasp genus Ichneumon (Hymenoptera: Ichneumonidae): convergent adaptations to host pupation sites. BMC evolutionary biology, 13(1), 1.

Webb, B. A., & Summers, M. D. (1990). Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. Proceedings of the National Academy of Sciences, 87(13), 4961-4965.

Whitfield, J. B. (1997). Molecular and morphological data suggest a single origin of the polydnaviruses among braconid wasps. Naturwissenschaften, 84(11), 502-507.

Whitfield JB (1998) Phylogeny and evolution of host-parasitoid interactions in Hymenoptera. Annual Review of Entomology 43: 129–151.

Whitfield, J. B. (2002). Estimating the age of the polydnavirus/braconid wasp symbiosis. Proceedings of the National Academy of Sciences, 99(11), 7508-7513.

09. The Long overdue Spider Story