Important considerations for adaptive vs. non-adaptive
manipulation
Parasitic manipulation of host behavior is not always adaptive. Both
direct and indirect mechanisms can lead to increased parasite
transmission (Adamo 2002) and making the distinction between
‘advantageous by-products’ of infection and true adaptive manipulation
requires an understanding of which mechanisms are involved (Poulin 1995,
2010; Thomas et al. 2005). In effort to deal with this, Poulin (1995)
synthesized four criteria by which one can theoretically distinguish
between ‘true’ adaptive traits and advantageous ‘side-effects’. The
first criteria regard “complexity”, considering that complex traits
are unlikely to arise by chance or accident and require an organizing
principle like natural selection. Poulin (1995) acknowledges the
difficulty in assessing these criteria since even simple changes in
behavior can result from complex mechanisms. Nevertheless, the behavior
presented in this paper whereby the host spider is manipulated to
perform a task serving the post-mortem needs of the parasite, is
indicative of a complex mechanism refined by selection. The second
criteria is of “purposiveness of design”, referring to characters or
traits seemingly “too well fitted” to fulfil a certain function to
have arisen by chance. Such observations of apparent conformity between
purpose, design, and function, used to be presented as evidence of
divine creation, but are now seen as strong evidence of adaptation
through selection (Bekoff and Allen 1995). The locations of host spiders
killed by Gibellula spp. certainly appear to serve an obvious
purpose by ensuring that the host is in an elevated and protected
position for the dispersal of conidia. The third criterion is regarding
the “convergence”, or independent origins of an adaptive trait in the
phylogenetic lineage of a group of organisms and is seen as a “strong”
indicator that the trait is not an accidental side-effect (Allen and
Bekoff 1995). Poulin (1995) stipulates that traits do not have to be
identical but only analogous, performing the same function (i.e.
dispersal). As mentioned above, the closely related genusOphiocordyceps contains a huge assemblage of ant-pathogenic
species wherein hosts secure themselves to the substrata via
irreversible death-grip behavior immediately prior to death. This
behavior, we argue, is analogous to the deathbed behavior of infected
spiders. The final and most important of the four criteria according to
Poulin (1995) are the “fitness effects”, though he admits that
measuring fitness is logistically difficult and not on its own
conclusive since even undetectable fitness advantages can be adaptive.
As mentioned above, the specificity of these death locations ostensibly
serves no other purpose than to maximize fungal spore dispersal and
thus, parasite fitness.