By Michel Cusson, ESC President
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For my first blog post, you’d probably expect me to talk about some hot issue pertaining to the ESC. However, I chose otherwise (at least this time) and I’ll save Society-related topics for my “Up Front” column, which you can read in the online version of the Bulletin. Instead, I’d like to introduce you to what I consider the coolest product of insect evolution: the use of symbiotic viruses by parasitic wasps to manipulate the physiology of their caterpillar hosts.
Aleiodes indiscretus wasp parasitizing a gypsy moth caterpillar. Photo by Scott Bauer.
In an unusual twist of evolutionary history, some ichneumonid and braconid parasitoids have “captured” a conventional virus and “domesticated” it so that it can be used to their own advantage in the course of parasitism. The viruses in question, known as polydnaviruses (from poly-DNA-virus, but typically pronounced “polyd-na-virus”), replicate in wasp ovaries where they accumulate in the fluid bathing the eggs, before being injected into the caterpillar during parasitization (egg laying). While the carrier wasp is completely asymptomatic, the infected caterpillar displays AIDS-like symptoms, whereby its ability to mount an immune response against the wasp egg or larva is depressed by the virus. In addition, the virus will often block host metamorphosis, particularly when parasitization takes place late in caterpillar development; this will allow the wasp larva to complete its own development before the host undergoes the traumatic events associated with the larva-to-adult transformation.
But what makes these viruses pathogenic in the caterpillar while being apparently harmless in the wasp, and how could such unusual creatures have evolved? To begin understanding the answers to these questions one first needs to know that polydnavirus genomes are permanently integrated into the chromosomal DNA of the carrier wasps. This means that all individuals within a species known to carry one of these viruses contain the viral DNA within their own genome. Production of the viral particles, however, is confined to females and occurs only in ovaries. There, copies of the integrated form of the viral genome are synthesized and packaged into a proteinacious coat known as the “capsid”. These viral particles are released into the lumen of the oviduct, where they accumulate until injection into the caterpillar host.
What’s going on “behind the scenes”. Image by Michel Cusson and Marlene Laforge.
Once injected, the virus gains access to various host tissues where some of its genes are expressed, leading to the synthesis of viral proteins that do the dirty work, i.e., depress the host immune response and perturb host development. Few, if any, of these virulence genes are expressed in the wasp, which probably explains why the wasp is asymptomatic. While the virus does not replicate in the caterpillar, it is the expression of viral genes that makes it possible for the wasp egg and larva to survive within the host. And successful development of the immature wasp is what ensures transmission of the integrated form of the virus to the next wasp generation.
Whether polydnaviruses are “real” viruses has been a matter of debate for many years. For example, some have argued that, although they look like viruses, they are nothing more than a smart device that the wasps have evolved to transfer host-regulating factors to caterpillars during oviposition. However, it is becoming increasingly clear that polydnaviruses arose from ‘conventional’ viruses.
Recently, a group from France has shown that the proteins that make up the coat of braconid polydnavirus particles are highly similar to those of ‘nudiviruses’1, a group of conventional insect viruses that are capable of integrating their genomes into those of their hosts. So, it appears that the genome of a nudivirus became permanently integrated into the chromosomal DNA of an ancestral braconid, some 100 MYA. Since then, evolution has led to the replacement of the original nudiviral virulence genes by other genes that are usefull to the wasp during parasitism. The wasps may therefore be viewed as having ‘domesticated’ the nudivirus, turning it into a mutualistic virus – a phenomenon fairly unique in the world of viruses. Cool stuff, isn’t it?
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1Bezier, A., Annaheim, M., Herbiniere, J., Wetterwald, C., Gyapay, G., Bernard-Samain, S., Wincker, P., Roditi, I., Heller, M., Belghazi, M. & (2009). Polydnaviruses of Braconid Wasps Derive from an Ancestral Nudivirus, Science, 323 (5916) 930. DOI: 10.1126/science.1166788