When Parasites are Wonderful and Relationships are Weird

So nat’ralists observe, a flea
Hath smaller fleas that on him prey;
And these have smaller fleas to bite ’em.
And so proceeds Ad infinitum

From On Poetry: A Rhapsody by Jonathan Swift

I’ve said ‘weird and wonderful’ in this blog perhaps far too many times but over billions of years evolution has led to so many incredible things in nature that I never cease to be amazed. And here again I found myself the other week reading a story that just blew my mind! If I say upfront that the story is about parasitic wasps, most people will probably not get too excited about it. Neither parasites nor wasps are the first things that even I would associate with being wonderful. Weird maybe, but wonderful??? But do bear with me here for a moment and I hope I can convince you otherwise.

So lets start with parasitic wasps and what they are? As the term parasite indicates parasitic wasps exploit the resources of other animals to benefit themselves and in turn harm the organism they parasitise. The “poor” animal in question here is a caterpillar, which sits innocently on a leaf, eats its greens and hopes to one day become a beautiful butterfly (pardon the anthropomorphism here). The wasp parasitise the caterpillar by laying eggs inside it, which later develop into larvae. The larvae use caterpillar’s tissues as food resource, which ultimately leads to emergence of a new progeny of parasitoid wasps (killing the caterpillar as a result). It is actually not all so black and white here and the caterpillar is not even the biggest victim. The caterpillar itself is a parasite of the plant it eats. As a defence mechanism, when the chewing caterpillar damages the plant leaves, the leaves release volatile compounds that will attract the parasitic wasps so that the caterpillar would not be able to do more damage to the plant (fig.1). And actually the trail of parasitism doesn’t stop here, same plant volatile compounds can be detected by a hyperparasitoid wasp (a parasite of a parasite). Hyperparasitoid wasp will then lay its eggs in the larvae of a parasitoid wasp and devour these to emerge as new hyperparasitoids.

Figure 1. Attack of a caterpillar by a parasitoid wasp
Figure 1. Attack of a caterpillar by a parasitoid wasp

To this trail of parasites a small but no less significant organism needs to be added. The genome of a parasitoid wasp has a number of endogenous viral elements (EVEs) present in it. EVEs are DNA sequences, which are derived from viruses, that at some point during evolution have integrated into a genome of an infected host. EVEs usually lack some important parts of the original virus genome and therefore, are no longer able to make what would be considered a fully infectious virus. Perhaps the most successful EVEs belong to polydnaviruses (PDVs), which have integrated into the genomes of parasitoid wasps. There are two types of PDVs, bracoviruses and ichnoviruses, grouped by the family of parasitoid wasp they are associated with (Braconidae and Ichneumonoidea, respectively). The two types of PDVs have integrated into wasp genomes independently and are good example of convergent evolution (similarity of traits which is not due to a common ancestry). The PDVs in the wasp genome still express genes that make the machinery which is required for producing viral particles (including viral capsid and polymerase proteins) but lack many accessory genes. In addition, so called PDV proviral DNA regions, which are wasp virulence genes that are flanked by viral genome packaging sequence, are transcribed to make circular double stranded DNA (cdsDNA) (fig.2).

Fig.2 PDV genes are transcribed to make cdsDNA and viral capsids (a-c). Viruses coat and protect the eggs, which are injected into caterpillars (d). After some time new wasps emerge from the an infected caterpillar (e-f).
Figure 2. PDV genes are transcribed to make cdsDNA and viral capsids (a-c). Viruses coat and protect the eggs, which are injected into caterpillars (d). After some time new wasps emerge from the infected caterpillar (e-f).

Figure 3. EM images of viral particles (marked with 'n') found in various species of parasitoid wasps.
Figure 3. EM images of viral particles (marked with ‘n’) found in various species of parasitoid wasps.
All of these viral components are only expressed in the ovaries of the wasp (the site were eggs are made) and lead to production of virus-like particles made of viral capsid proteins with packaged cdsDNA inside. One can even see these virus-like particles being made in abundance in the electron microscopy images of the ovary tissues (fig.3).

PDVs are vertically transmitted between the wasps, meaning the wasp progeny receives the virus by inheriting its genes from the parental wasp and not by being newly infected with the virus. The relationship between the wasp and PDV is a mutualistic one, i.e. both sides benefit from it. The viral genetic elements get more or less free ride from one host to another without the need for a new infection each time. What’s in it for the wasp then? Well, without the virus-like particles the wasp may not be able to successfully infect the caterpillar. When the virus-like particles are made inside the wasp’s ovaries, depending on the PDV they originate from, several important things can happen. The wasp’s eggs get coated with these viruses and when they are injected into the caterpillar the “viral coat” protects the eggs from being recognised by the caterpillar’s immune system. Not only that but the cdsDNA that is packaged into the viral particles encodes wasp’s virulence factors that act as suppressors of caterpillar’s immune system. In addition, it has also been recently shown that PDVs which lack the ability to package cdsDNA can incorporate proteins, such as peroxidases and metaloproteases, which are also there to modulate the caterpillar’s immune defences. This particular group of PDVs, which is not able to package cdsDNA, is actually found in Venturia canescens wasp and is as yet perhaps the only example of endogenous mutualistic virus replacement, were an EVE that was able to package cdsDNA was replaced by one that packages proteins.

Seriously, isn’t this weird and wonderful?! And I haven’t even told you about the parasites of the hyperparasitoid wasps.
Hmmmm… I wonder if anyone has looked for PDVs in the hyperparasitoids?

Herniou, Elisabeth A., et al. “When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses.” Philosophical Transactions of the Royal Society of London B: Biological Sciences 368.1626 (2013): 20130051.

Bézier, Annie, et al. “Polydnaviruses of braconid wasps derive from an ancestral nudivirus.” Science 323.5916 (2009): 926-930.

Pichon, Apolline, et al. “Recurrent DNA virus domestication leading to different parasite virulence strategies.” Science Advances 1.10 (2015): e1501150.

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