Differential influence ofPomphorhynchus laevis(Acanthocephala) on brain serotonergic activity in two congeneric host species

Abstract

The physiological mechanisms by which parasites with complex life cycles manipulate the behaviour of their intermediate hosts are still poorly understood. In Burgundy, eastern France, the acanthocephalan parasite Pomphorhynchus laevis inverses reaction to light in its amphipod host Gammarus pulex, but not in Gammarus roeseli, a recent invasive species. Here, we show that this difference in manipulation actually reflects a difference in the ability of the parasite to alter brain serotonergic (5-HT) activity of the two host species. Injection of 5-HT in uninfected individuals of both host species was sufficient to inverse reaction to light. However, a difference in brain 5-HT immunocytochemical staining levels between infected and uninfected individuals was observed only in G. pulex. Local adaptation of the parasite to the local host species might explain its inability to manipulate the behaviour and nervous system of the invasive species.

Multidimensionality in parasite-induced phenotypic alterations: ultimateversusproximate aspects

“…Indeed, it has been shown in various host-parasite systems (see Perrot-Minnot and Cézilly, 2012) that infection can affect various neuromodulators, such as, serotonin (5-HT). For instance, an increase in brain 5-HT immunoreactivity has been observed in amphipods infected with fish acanthocephalans (Tain et al, 2006;Tain et al, 2007), and injection with 5-HT mimics the reversed photophobia observed in amphipods naturally infected with fish acanthocephalans. Interestingly, infection with fish acanthocephalans induces partial castration in female amphipods, whereas 5-HT is known to affect ovarian development in crustaceans (Makkapan et al, 2011).…”

“…Symmetrically, the existence of cryptic species in hosts (see Westram et al, 2011), eventually living in sympatry, may also affect the assessment of multidimensionality in PIPAs, as the effect of a parasite is known to vary between closely related species of intermediate hosts (Bauer et al, 2000;Bauer et al, 2005;Tain et al, 2007;Cornet et al, 2010). Ideally, then, such a study should be conducted in a single host-parasite system; a single system is advantageous in that it allows the researcher to assess whether all infected hosts express the same combination of modified traits at the same intensity.…”

Parasite-induced alterations of sensorimotor pathways in gammarids: collateral damage of neuroinflammation?

“…The acanthocephalans affect various sensory pathways in their hosts: mechanical, photic, geotactic and olfactory, in different combinations (Table1). Particularly intriguing is the differential effect of P. laevis on the behavior of G. pulex, a native species, and G. roeseli, an invasive species in central France (Bauer et al, 2005;Tain et al, 2007). Whereas P. laevis induces a strong photophilic behavior in G. pulex, it does not affect the photic behavior of G. roeseli (Table1).…”

“…Whereas P. laevis induces a strong photophilic behavior in G. pulex, it does not affect the photic behavior of G. roeseli (Table1). Tain and colleagues suggest that local strains of P. laevis may have co-evolved with the dominant intermediate host G. pulex, allowing the behavioral manipulation to become established (Tain et al, 2007). Interestingly, P. minutus seems to have similar behavioral effects on G. pulex and G. roeseli, hinting that the great dispersal range of birds, definitive hosts of P. minutus, may result in less specificity in the relationship between P. minutus and its gammarid hosts (Bauer et al, 2005).…”

“…5-HT, 5-hydroxytryptamine (serotonin); PO, phenoloxidase. Tain et al, 2007. to 10µgl -1 ) over a period of weeks. Moreover, exposure to fluoxetine, but not to the anticonvulsant carbamazepine or the analgesic diclofenac, also significantly altered phototaxis and geotaxis activity in gammarids.…”