Studying immunity at the whole organism level
Sir, Hauton and Smith (BioEssays 29:1138) make the strong assertion that a whole-organism phenomenological approach to investigating invertebrate immunity is flawed and sidesteps scientific rigour. Their major claim appears to be that we should not study immunity based on observations at the level of the whole organism, and should instead limit ourselves to measuring the levels, regulation and interactions of immune molecules. We do not want to argue against the desideratum of understanding the physiological, biochemical and molecular genetic basis of immune responses but, unfortunately, the case that Hauton and Smith make both misrepresents and misunderstands the evolutionary ecology work that is being carried out on immunity. Consequently, whilst they claim to have discovered a straw house, they have instead erected a straw man.
Immunity can be regarded as a state of having sufficient biological defenses to avoid infection or reduce the consequences of infection. It is by its nature an organism-level phenomenon. The intricate mechanisms that give rise to immunity are interesting and their elucidation can only help in understanding the phenomenon of immunity. For example, measurement of molecules can often be used as a proxy for immunity when it cannot be measured directly at the organismic level. But to argue that we cannot say that an organism has increased immunity unless we have studied the molecule responsible is illogical. We should remember that the phenomenon of immune memory (e.g. as exploited by Edward Jenner in the 18 th century) was known and accepted long before the molecular basis of adaptive immunity was understood. So why not study immunity in invertebrates in the same spirit? And if the phenomenon is really based on an as-yet-undiscovered mechanism, then what molecule would Hauton and Smith have us measure? The primacy of mechanistic study is also questionable at the practical level mentioned by Hauton and Smith: would aquaculturalists prefer a drug that actually had a demonstrable effect to reduce disease outbreaks, even if it is not known what molecules are involved, or one that raised the level of a known molecule with no known fitness effect?
Consistently, Hauton and Smith dismiss host fitness measures, such as fecundity or survival, as being irrelevant for the discussion of immune memory. However, precisely because immune memory must have effects on host fitness to either evolve or be eliminated by natural selection, such measures are appropriate. It is ironic that, in several places, Hauton and Smith invoke evolution by natural selection