Cotesia congregata

In order to reproduce, the wasp, Cotesia congregata, lays her eggs in the tobacco sphinx caterpillar (Manduca sexta). The caterpillar thus serves as a protective storehouse for the larva of the wasp, and dies when the larva attain a sufficient stage of maturity to burst out of the bloodless body of their host where they continue their transformation, metamorphosing into pupas, and then flying adults.
More than half the Hymenoptera reproduce in this way. Of course the insect host does not let itself be taken advantage of easily. Its main defense mechanism consists in surrounding the egg of the parasite in a sort of capsule of cells which liberate toxic substances to destroy the invader. Ever since the adoption of a parasitic mode of life by the Hymenoptera in the Jurassic era, the host species has constantly evolved, because the genes which permit an escape from parasitism are advantageous for the wasp. As a response to this, new means of avoiding the immune defenses of the caterpillar have been selected in Hymenoptera.

Wasp larvae emergence from parasitized Manduca sexta (Photo from the website http://www.biochemistry.ucr.edu)

The two organisms have thus evolved in parallel such that the parasite always finds something to eat. It turns out that there is a virus which permits the wasp to manipulate the physiology of the caterpillar so that the wasp larva can develop.
Virus particles, which have the form of cylindrical rods in a protein matrix, are introduced at the same time as the parasite eggs, when they are laid in the body of the caterpillar. There, the genes of the virus are expressed, leading to modifications in the physiology of the host.
These induced modifications may differ depending on the biological system, but they are always advantageous for the parasite. They can be divided into categories: inactivation of host defense mechanisms, and perturbation of its development. Generally,the parasitized caterpillar does not go through metamorphosis and remains blocked in a prepupal stage, which allows the parasite to continue its own development.

To understand the role of these viruses, more precisely polydnaviruses, in the success of wasps as parasites, it is important to know not only the proteins which are expressed in the host, but also the manner in which their production is controlled by the wasp, as well as their precise characteristics.

This is the goal of the genetics group of the IRBI

(Institute for Research on the Biology of Insects). One of the goals, at the end of the project, will be to develop new methods of control of harmful insects based on a better understanding of the molecular bases for these mechanisms of circumventing the defenses of the host. The results published in Science (8 October 2004; 306:286-289) removed some of the obscurity surrounding the organization of the viral genome, its evolutionary origin and its characteristics.

The first surprise is that the complete sequence of the DNA (about 568 000 base pairs) of the virus particle introduced into the caterpillar reveals a complex genomic organization that resembles a genomic region of a eukaryote more than that of a virus. In contrast to other known viruses, the DNA of the polydnavirus is very gene-dense. It contains a total of 156 coding regions, of which 42% have no homology with known genes. Furthermore, this genome does not contain any groups of genes which can be linked to a known viral family, and no gene which is similar to a major virus gene.
Another unusual characteristic is the abundance of gene families: 66 genes are organized into 9 families. Another interesting fact: the proteins produced from 4 of these gene families contain domains previously described in toxins utilized by pathogenic bacteria (Pseudomonas, Yersinia, Salmonella,...) or parasitic worms, i.e. by bacteria and eukaryotes.

The current hypothesis is that these virulence genes may have come from the wasp genome during the evolution of lineages. These polydnaviruses may therefore not be descended from a large viral genome, but were constructed from the genome of the wasp using a system of production of circular DNA - because the genome present in particles produced in the ovary of the wasp is composed of 30 DNA circles.

On the other hand, the proteins of each of the capsids containing this genome would have a viral origin, probably acquired in the course of an infection. The genes implicated in the replication of this original virus were probably not transferred into the genome of the wasp.

“Nature,” estimates CNRS scientist Jean-Michel Drezen, "seems to have developed here a technique for gene transfer which is similar to the medical approaches currently being used to produce pseudoviruses used to transfer genes with a therapeutic goal, and to allow their expression."

Articles about this subject :

• Drezen JM, Provost B, Espagne E, Cattolico L, Dupuy C, Poirie M, Periquet G, Huguet E. Polydnavirus genome: integrated vs. free virus. J Insect Physiol. 2003 May;49(5):407-17
• Espagne E, Dupuy C, Huguet E, Cattolico L, Provost B, Martins N, Poirie M, Periquet G, Drezen JM. Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science. 2004 October;306:286-289