Richard Dawkins famously suggested that animals are little more than ‘robot vehicles blindly programmed to preserve’ their selfish genes. However, the true pilots of animal vehicles may not be their own genes, but rather those of their parasites. Whereas some parasites consume the host they colonize from within, others change the behaviour of the host to ensure a meal for the host's predator. A foolish strategy? According to new research led by Thierry Rigaud from the Université de Bourgogne, France, the answer is yes and no, depending upon the particular stage in the life of the parasite.

Some parasites spend their lives exploiting a single host. Others, by contrast, do a bit of travelling, spending time in one or more intermediate hosts before finally settling into a definitive host where the parasite reaches maturity. For these parasites, reaching the final host requires that their intermediate hosts are eaten by their definitive host. And thus the parasite takes over the strings of its puppet host to make it suicidal.

Examples of parasitic manipulation of behaviour are widespread: parasites can reduce the fear of predators, e.g. rats that become fatally attracted to cats. Others change the appearance of their hosts to make them look tasty, e.g. by turning an ant's abdomen bright red to make it look like a berry, or by making the tentacles of snails pulsate with light to make them look like caterpillars. Perhaps because scientists have spent so much time marvelling at these bizarre changes that increase predation, they have failed to recognize the flip-side, that there are key moments of a parasite's development where they wouldn't want their host to be consumed. Can parasites also make their hosts less susceptible to predation?

To examine this possibility, Rigaud's team infected freshwater crustaceans called gammarids with an acanthocephalan parasite that reaches maturity in a trout. This parasite passes through two developmental stages in the gammarid. The first, called an acanthella, is not infective to trout, while the second, called a cystacanth, is. To analyze behavioural effects of parasitism, the researchers infected gammarids with parasite eggs and allowed them to develop into acanthella or cystacanths. They then measured the time gammarids spent hiding in a refuge. As expected, gammarids infected with acanthella were the models of caution. By contrast, gammarids infected with cystacanths were downright reckless.

But are these manipulations adaptive for the parasite? In a word, yes. Gammarids infected with acanthella are less likely to be eaten than uninfected animals, while those infected with cystacanths are more likely to be preyed upon. It thus appears that the parasites in this system play both sides of the game. As immature acanthella they keep their hosts safe. But when they become ready to see the world, cystacanths rapidly change tack and send their hosts into the eye of the storm.

What better example for Dawkins' idea that animals are little more than ‘lumbering robots’ than zombie gammarids being sustained and then summarily marched to their death by their parasites?

Dianne
L.
,
Perrot-Minnot
M.-J.
,
Bauer
A.
,
Gaillard
M.
,
Léger
E.
,
Rigaud
T.
(
2010
).
Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage
.
Evolution
doi: 10.1111/j.1558-5646.2011.01330.x