Parasitic manipulation or by-product of infection: an experimental approach using trematode-infected snails.

Alice Namias,Lynda F Delph,Curtis M Lively

doi:10.1017/s0022149x21000699

Abstract

Natural selection should favour parasite genotypes that manipulate hosts in ways that enhance parasite fitness. However, it is also possible that the effects of infection are not adaptive. Here we experimentally examined the phenotypic effects of infection in a snail-trematode system. These trematodes (Atriophallophorus winterbourni) produce larval cysts within the snail's shell (Potamopyrgus antipodarum); hence the internal shell volume determines the total number of parasite cysts produced. Infected snails in the field tend to be larger than uninfected snails, suggesting the hypothesis that parasites manipulate host growth so as to increase the space available for trematode reproduction. To test the hypothesis, we exposed juvenile snails to trematode eggs. Snails were then left to grow for about one year in 800-l outdoor mesocosms. We found that uninfected males were smaller than uninfected females (sexual dimorphism). We also found that infection did not affect the shell dimensions of males. However, infected females were smaller than uninfected females. Hence, infection stunts the growth of females, and (contrary to the hypothesis) it results in a smaller internal volume for larval cysts. Finally, infected females resembled males in size and shape, suggesting the possibility that parasitic castration prevents the normal development of females. These results thus indicate that the parasite is not manipulating the growth of infected hosts so as to increase the number of larval cysts, although alternative adaptive explanations are possible.

Highlights

Natural selection should favour parasites that manipulate their host in ways that increase parasite fitness, and there are many examples of adaptive parasitic manipulation across a wide range of parasite taxa (Moore, 1984; Berdoy et al, 2000; Barber et al, 2004; Yanoviak et al, 2008; Wesołowska & Wesołowski, 2014; Westwood et al, 2019; Lovett et al, 2020)
We experimentally evaluated the effect of infection by a different digenetic trematode (Atriophallophorus winterbourni) on the growth and shell morphology of P. antipodarum
Parasites should be under selection to manipulate host phenotypes in ways that increase parasite fitness, but it can be difficult to separate adaptive parasitic manipulation from the side effects caused by infection (Poulin, 1995, 2010; Thomas et al, 2005)

Summary

Introduction

Natural selection should favour parasites that manipulate their host in ways that increase parasite fitness, and there are many examples of adaptive parasitic manipulation across a wide range of parasite taxa (Moore, 1984; Berdoy et al, 2000; Barber et al, 2004; Yanoviak et al, 2008; Wesołowska & Wesołowski, 2014; Westwood et al, 2019; Lovett et al, 2020). Lagrue et al (2007) found that field-collected snails (Potamopyrgus antipodarum) infected by a trematode (Coitocaecum parvum) were smaller (by volume) than uninfected snails; but they found that the internal shell volume available for parasite reproduction represented a larger proportion of the total internal shell volume. Based on these results, they suggested that the parasite might manipulate infected snails to increase the relative ‘parasitized’ shell volume of their hosts, even though infection reduces overall shell size (perhaps due to the energetic costs of infection). We experimentally evaluated the effect of infection by a different digenetic trematode (Atriophallophorus winterbourni) on the growth and shell morphology of P. antipodarum

Methods

Results

Conclusion