Tapeworm manipulation of copepod behaviour: parasite genotype has a larger effect than host genotype

Abstract

Compared with uninfected individuals, infected animals can exhibit altered phenotypes. The changes often appear beneficial to parasites, leading to the notion that modified host phenotypes are extended parasite phenotypes, shaped by parasite genes. However, the phenotype of a parasitized individual may reflect parasitic manipulation, host responses to infection or both, and disentangling the contribution of parasite genes versus host genes to these altered phenotypes is challenging. Using a tapeworm (Schistocephalus solidus) infecting its copepod first intermediate host, I performed a full-factorial, cross-infection experiment with five host and five parasite genotypes. I found that a behavioural trait modified by infection, copepod activity, was affected by both host and parasite genotype. There was no clear evidence for host genotype by parasite genotype interactions. Several observations indicated that host behaviour was chiefly determined by parasite genes: (i) all infected copepods, regardless of host or parasite genotype, exhibited behavioural changes, (ii) parasitism reduced the differences among copepod genotypes, and (iii) within infected copepods, parasite genotype had twice as large an effect on behaviour as host genotype. I conclude that the altered behaviour of infected copepods primarily represents an extended parasite phenotype, and I discuss how genetic variation in parasitic host manipulation could be maintained.

Keywords: cestode; complex life cycle; genotype–genotype interactions; heritability; host manipulation; trophic transmission.

Figure 1.

(a) Mean activity (speed in pixels s⁻¹ over 1 min recording intervals) for five inbred copepod lines when they were uninfected or infected. (b) Mean activity of infected copepods split by either host or parasite genotype. (c) Mean activity of infected copepods split by both host and parasite genotype; host genotypes depicted by colours. In all panels, solid error bars depict the 95% CI as estimated by a mixed model. Dotted error bars show the interquartile range. (Online version in colour.)

Figure 2.

Time-dependent genotype effects. Copepod activity over the experiment is plotted for each copepod line (panels) infected with each parasite family (coloured, dashed lines). (Online version in colour.)