Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation

Abstract

Manipulation by parasites is a catchy concept that has been applied to a large range of phenotypic alterations brought about by parasites in their hosts. It has, for instance, been suggested that the carotenoid-based colour of acanthocephalan cystacanths is adaptive through increasing the conspicuousness of infected intermediate hosts and, hence, their vulnerability to appropriate final hosts such as fish predators. We revisited the evidence in favour of adaptive coloration of acanthocephalan parasites in relation to increased trophic transmission using the crustacean amphipod Gammarus pulex and two species of acanthocephalans, Pomphorhynchus laevis and Polymorphus minutus. Both species show carotenoid-based colorations, but rely, respectively, on freshwater fish and aquatic bird species as final hosts. In addition, the two parasites differ in the type of behavioural alteration brought to their common intermediate host.Pomphorhynchus laevis reverses negative phototaxis in G. pulex, whereas P. minutus reverses positive geotaxis. In aquaria, trout showed selective predation for P. laevis-infected gammarids, whereas P. minutusinfected ones did not differ from uninfected controls in their vulnerability to predation. We tested for an effect of parasite coloration on increased trophic transmission by painting a yellow-orange spot on the cuticle of uninfected gammarids and by masking the yellow-orange spot of infected individuals with inconspicuous brown paint. To enhance realism, match of colour between painted mimics and true parasite was carefully checked using a spectrometer. We found no evidence for a role of parasite coloration in the increased vulnerability of gammarids to predation by trout. Painted mimics did not differ from control uninfected gammarids in their vulnerability to predation by trout. In addition, covering the place through which the parasite was visible did not reduce the vulnerability of infected gammarids to predation by trout. We discuss alternative evolutionary explanations for the origin and maintenance of carotenoidbased colorations in acanthocephalan parasites.

Multidimensionality in host manipulation mimicked by serotonin injection

“…Second, the benefits, in terms of increased trophic transmission, of multidimensionality versus unidimensionality in host manipulation remain to be established. In our study model system, the increased vulnerability to predation of G. pulex infected with P. laevis has been demonstrated, both in microcosm experiments [7,9,52], and under field conditions [8], but the traits involved in such increase have not been identified yet. Two recent studies have shown that a single altered phenotypic dimension in P. laevis infected hosts cannot explain this increased vulnerability to predation [20,52].…”

“…In our study model system, the increased vulnerability to predation of G. pulex infected with P. laevis has been demonstrated, both in microcosm experiments [7,9,52], and under field conditions [8], but the traits involved in such increase have not been identified yet. Two recent studies have shown that a single altered phenotypic dimension in P. laevis infected hosts cannot explain this increased vulnerability to predation [20,52]. Since a transient increase in serotonin appears to mimic infection syndrome in a number of dimensions (this study), we would expect its injection in G. pulex to increase its vulnerability to predation.…”

Acanthocephalan size and sex affect the modification of intermediate host colouration

“…Although altered host colouration appears related to parasite transmission, a direct link has not been established. This caveat deserves mention because a recent study found no relationship between intermediate host appearance and predation risk in a different acanthocephalan (Kaldonski et al 2009). Here we test (1) if there is a relationship between parasite size and host colouration and (2) whether this pattern differs between male and female parasites.…”

Multidimensionality in parasite-induced phenotypic alterations: ultimateversusproximate aspects

“…In contrast, multiplication would perform better if one poorly manipulated dimension is sufficient to decrease the overall effect on trophic transmission. Analysing the results of experiments combining predation trials with phenotypic engineering of both infected and uninfected hosts (Bakker et al, 1997;Kaldonski et al, 2009;Perrot-Minnot et al, 2012) using multiple regression techniques might provide interesting insights in this respect.…”

“…This can be achieved through combining refined experimental design with phenotypic engineering (Kaldonski et al, 2009;PerrotMinnot et al, 2012). Furthermore, such experiments will allow one to estimate whether the effects of altered traits on enhanced transmission are additive or interactive.…”