Could you ever feel sorry for a parasite? Doubtful as it seems, a recent paper exploring the evolutionary conflict between the parasitoid wasp Leptopilina boulardi and the LbFV virus has left me not only supporting the parasite, but cheering at recent evidence that it seems to be putting up a good fight.
The lifecycle of L. boulardi seems particularly nasty: it lays a single egg in the larvae of Drosophila (fruit flies), which then hatches, consumes the larva from the inside, and eventually emerges from the now (thankfully) deceased host to repeat the cycle. However, this wasp can itself become prey to a parasite: the imaginatively named Leptopilina boulardi filamentous virus (LbFV). Ordinarily, an L. boulardi wasp would avoid larvae which have already been parasitized, to prevent her offspring having to compete with others. However, wasps infected with LbFV will not discriminate between parasitized and non-parasitized larvae, and may lay eggs in a larva already hosting an egg (termed “superparasitism”). This egg laying behaviour is a perfect example of an extended phenotype: “all effects of a gene upon the world” according to the idea’s originator Richard Dawkins (2008), but usually used in reference to those effects beyond the organism in whose genome the gene resides.
Superparasitism is great from the virus’s point of view: it gets an opportunity to infect the other eggs in the larva, as well as its usual route of infecting the offspring of the current host. However, it is disadvantageous to the wasp, as it reduces the amount of food available to its offspring through competition with the other eggs. Any wasp able to reduce or avoid superparasitism will therefore leave more offspring, and if this variation in superparasitism-avoidance is heritable, wasps will evolve resistance to superparasitism.
Researchers at the University of Lyon investigated this evolution in 30 wasp lines from five wild populations (with each population differing in its level of viral prevalence), aiming to answer three questions:
1. Is variation in superparasitism explained by the presence or absence of the virus?
2. Do viruses vary in the superparasitism phenotype they induce?
3. Does this variation correlate with variation in the viral titre (the amount of virus) in a wasp host?
They found that infection status of the wasp explains 77% of variation in superparasitism (measured as the number of eggs per parasitized larva): uninfected wasps had lower levels of superparasitism than infected wasps. Thus, question number 1 was answered: a large part of the variation in superparasitism can be explained by viral presence.
The authors’ second finding was that lines differed in their degree of superparasitism – two (Sf12 and Av3) laid 8-10 eggs per larva and were therefore highly susceptible to viral manipulation; and two were less susceptible (Av8 and Go16), laying roughly half as many eggs per larva as the highly susceptible lines. They also found a loose but significant correlation between the extent of superparasitism in one generation and the next. From these results they concluded that not only is there variation in susceptibility to viral manipulation (leading to variation in the level of superparasitism), but that this variation is heritable, and therefore likely to have a genetic basis.
And finally, they found no difference between the viral titre of wasps with high and low levels of superparasitism. The authors suggest that this may be due to a “tolerance mechanism”, giving a tantalizing hint as to the possible identity of this genetic difference in susceptibility. One allele (form) of the same antiviral gene could endow some lines with high tolerance and hence low levels of superparasitism, whereas another allele produces lower tolerance and more superparasitism. However, in the words of the authors, “we must be cautious about this conclusion, because only four lines were tested, which reduces the statistical power of the viral titre analysis.”
Puzzlingly, the authors found no geographical differentiation in the amount of viral resistance in wasp populations, even though the south’s higher viral prevalence leads to the expectation of higher resistance in the southern wasps. The authors give three possible explanations: recent invasion of the virus into the wasp host; a high migration rate of wasps between north and south; and a high cost of tolerance. While this last hypothesis is supported by their data (they found lower egg load in individuals of the Av12 line, which had higher tolerance), the authors admit that “this correlation needs to be tested over a wider range of parasitoid and virus genotypes.”
This paper also highlights the element of serendipity that seems to feature in some research: a “severe dysfunction” of their incubators caused the loss of many of their lines halfway through the investigation, meaning they had to reconstruct some lines. However, this eventually supported their original claim that variation in the wasp genome leads to variation in level of superparasitism: their reconstructed “less susceptible” line displayed equally low levels of superparasitism as the original, strengthening the case for heritable variation in the susceptibility of wasps to the virus.
So in the end I was cheering for the wasp, which seems to be fighting back against this insidious (if fascinating) virus. However, I was also cheering for the authors: they presented what could have been sensationalised data in a moderate and responsible manner, as well as pointing out the flaws in their method and the way that these could actually further inform their conclusions.
Dawkins, R. (2008) The Extended Phenotype. pp. 264. Oxford University Press
Martinez, J., Fleury, F. and Varaldi, J. (2011) Heritable variation in an extended phenotype: the case of a parasitoid manipulated by a virus. Journal of Evolutionary Biology, Early View