Evolution of the Polydnavirus: How Wasps Began Using Viruses to Engineer Their Hosts

In Polydnaviruses, Nature’s GMOs, I explained how polydnaviruses disabled host immune defenses through genetic modification. A post after that, I discussed how polydnaviruses use modified insect proteins to interfere with these systems.
So if you’re a biologically-minded person, there’s one question you should be asking yourself. It’s a rather important question because it’s answer could shed light on what makes these wasps species-specific, and this is essential for any biocontrol project.
So…how did they evolve?

These systems have arisen at least three times independently with different viruses. The Ichneumonid wasps use polydnaviruses which are derived from Ascoviruses, which are DNA viruses which infect invertebrates. The genus Nasonia uses poxviruses in a manner which is probably the same as the Ichnoviruses and Bracoviruses. We’ll discuss the Ichnovirus and Bracovirus system as examples of model systems.
Most eukaryotic genomes are essentially old battlegrounds between critters and their viruses. Viruses can go through a process called endogenization, which is when a virus integrates into the genome of a eukaryotic cell. Viral DNA will occasionally integrate into an organism’s genome and then get deactivated either by mutation or by a defense mechanism known as methylation. This DNA then gets passed on to the organism’s progeny. These viruses then become known as endogenized viruses. Many of these viruses happen to be retroviruses, but it’s possible for DNA viruses and even RNA viruses can become endogenized if the conditions are right.
In all eukaryotic genomes, there are also bits and pieces of parasitic DNA called transposons. These are little bits of parasitic DNA which copy themselves and re-integrate into the organism’s genome. These guys are also great at copying genes and moving them to places they ought not to be. Occasionally they plop down next to a gene and the enzyme which copies them copies that gene and moves the gene to a new location in the genome.
Polydnaviruses are thought to have taken one of two routes in evolution. The first possibility is that a virus which already was a benefit to the wasp integrated into the genome and began to be passed onto the progeny. The second possibility is that bits and pieces of viral DNA began to produce proteins and became useful to the wasp.

The first possibility is very evident in the Ichnovirus group of polydnaviruses. One primitive Ichneumonid wasp, Diadromus pulchellus has a virus that is very different from the polydnaviruses it’s brethren posses. It’s virus, Diadromus pulchellus Ascovirus (DpAv), unlike all other Ichnovirus, actually reproduces and amplifies in the cells of the caterpillar. The disease is fatal to the caterpillar, but could benefit the wasp by disallowing competing species from ovipositing into the same host because the host dies before they are able to complete development. Many Ascoviruses have similar effects to Ichnoviruses and differ in that they amplify within the Lepidopteran host.
Some Ascoviruses are transmitted mechanically from wasp to host. This means they do not actually infect the wasp, but are transmitted when the wasp lays eggs in another host in a similar manner how HIV would be transmitted between IV drug users. Even though they aren’t transmitted in the same manner as DpAv, they occasionally do infect other parasitoid wasps. This gives a great hypothetical mechanism by which these viruses could have evolved.

The Ichnoviruses transmitted by Ichneumonid wasps have a very high sequence similarity to Ascoviruses. Braconid wasps, however, present another problem. While the similarity of Ichnoviruses to Ascoviruses essentially closes the book on many questions pertaining to their evolution, Braconid wasps present a greater challenge.
Braconid wasps also transmit polydnaviruses, but their viruses are derived from a completely different set of viruses. Bracoviruses are genetically most similar to viruses known as Nudiviruses, which themselves are similar to Baculoviruses. Despite their similarity to Baculoviruses, Nudiviruses are quite different in ways I will need to discuss in another post. The greatest mystery for researchers such as myself lies within the host range of the Nudiviruses. No known Nudiviruses afflict Hymenoptera, although I should also be quick to point out that little is known about the host ranges of Nudiviruses in general. Many are sexually transmitted (insects get STDs, too), so many researchers think these viruses originated as STDs accidentally injected into the host during oviposition. It’s a great hypothesis, but with so little known about Nudiviruses, Bracovirus phylogeny remains a wide open mystery.
Pictures:
Webb, B., Fisher, T., & Nusawardani, T. (2009). The Natural Genetic Engineering of Polydnaviruses Annals of the New York Academy of Sciences, 1178 (1), 146-156 DOI: 10.1111/j.1749-6632.2009.05023.x
Wu, G., Jun, S., Sims, G., & Kim, S. (2009). Whole-proteome phylogeny of large dsDNA virus families by an alignment-free method Proceedings of the National Academy of Sciences, 106 (31), 12826-12831 DOI: 10.1073/pnas.0905115106
General Information:
Bigot, Y., Samain, S., Augé-Gouillou, C., & Federici, B. (2008). Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis BMC Evolutionary Biology, 8 (1) DOI: 10.1186/1471-2148-8-253
Tillman, P., Styer, E., & Hamm, J. (2004). Transmission of Ascovirus from (Lepidoptera: Noctuidae) by Three Parasitoids and Effects of Virus on Survival of Parasitoid (Hymenoptera: Braconidae) Environmental Entomology, 33 (3), 633-643 DOI: 10.1603/0046-225X-33.3.633
Bigot Y, Rabouille A, Doury G, Sizaret PY, Delbost F, Hamelin MH, & Periquet G (1997). Biological and molecular features of the relationships between Diadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host, Acrolepiopsis assectella. The Journal of general virology, 78 ( Pt 5), 1149-63 PMID: 9152436
Renault S, Petit A, Bénédet F, Bigot S, & Bigot Y (2002). Effects of the Diadromus pulchellus ascovirus, DpAV-4, on the hemocytic encapsulation response and capsule melanization of the leek-moth pupa, Acrolepiopsis assectella. Journal of insect physiology, 48 (3), 297-302 PMID: 12770103