The review article1 I wrote about last month has sensitized me to some of the issues with research on invertebrate immunity. Unfortunately for me, that made an otherwise-fascinating article on parasite resistance in ants a rather painful read.
The article is Social Prophylaxis: Group Interaction Promotes Collective Immunity in Ant Colonies. Line V. Ugelvig and Sylvia Cremer. Current Biology 17:1967-1971 (20 November 2007) (hat tip to Not Exactly Rocket Science, which drew my attention to it before publication). The fundamental observation in this paper is that
Social contact with individual workers, which were experimentally exposed to a fungal parasite, provided a clear survival benefit to nontreated, naive group members upon later challenge with the same parasite.
This is indeed very interesting — of course, you’d expect that contact with an infected peer would raise your risk of infection, rather than benefiting you, so it had been hard to explain why social insects do sometimes perform “meticulous care by the performance of hygienic behaviors” on infected individuals. Ugelvig and Cremer found that in fact exposure to the infected ant conferred resistance to the detrimental effect of the pathogen (the fungus Metarhizium anisopliae; see the figure to the right) on later exposure. They propose that
either parasites might be transferred between individuals eliciting an immune response potentially followed by immune priming in the naive group members or that the exposed individual might directly transfer immunity by passing on immune compounds to its nestmates.
Of course, it’s the use of the term “immunity”, and especially “immune priming”, that makes me uncomfortable. “Immunity” and “immune priming” have specific meanings; in particular, “priming” very strongly implies immune memory and an adaptive immune system, which has not been previously demonstrated2 in insects. Yet Line and Cremer did nothing to test immunity per se; they looked at ant survival after exposure, and assumed that the differences are due to immunity. This is exactly the practice that Hauton and Smith specifically criticized:
The failure to make assessment of immunological parameters is a consistent weakness in most papers purporting to demonstrate priming, memory or adaptivity in the invertebrate innate immune system. In some cases, only single-end points are taken and the role of the immune system is inferred but not actually tested.
3 ) Is there anything wrong with using the term “immune priming” loosely? It certainly raises the interest factor for the paper. As Hauton and Smith say:I realize that actually testing the role of the immune system in the ant system would be an enormous task, and that at least part of the importance of the paper has nothing to do with the terminology used. In fact, for the most part the word “immunity” could have been entirely metaphorical throughout the paper (except that they do cite a previous paper that attempted to identify a non-metaphorical immunity in insects.
Hypotheses erected from these observations appear revelatory because the terminology adopted draws analogy to processes that have been characterized in the adaptive immune responses of jawed vertebrates.
Is there any harm in speculating that this is immunity? Perhaps not, but given that there’s no case made for actual immunity here, I think the paper really is somewhat misleading; it will certainly reinforce the concept that insects have some form of adaptive memory. I don’t know whether insects do or not, frankly, but I do think the question is important enough that it should be tested — not taken as given, or treated as a metaphor. And I think Ugelvig and Cremer’s paper is interesting enough to stand on its own, even without the loaded terminology.
- Hauton, C., and Smith, V. J. (2007). Adaptive immunity in invertebrates: A straw house without a mechanistic foundation. Bioessays 29, 1138-1146. [↩]
- B.M. Sadd and P. Schmid-Hempel, Insect immunity shows specificity upon secondary pathogen exposure, Curr. Biol. 16 (2006), pp. 1206-1210. [↩]