The Evolution of Trophic Transmission

doi:10.1016/S0169-4758(99)01397-6

Parasitology Today

Volume 15, Issue 3, 1 March 1999, Pages 111-115

Parasitology Today

https://doi.org/10.1016/S0169-4758(99)01397-6 Get rights and content

Abstract

Parasite increased trophic transmission (PITT) is one of the more fascinating tales of parasite evolution. The implications of this go beyond cocktail party anecdotes and science fiction plots as the phenomenon is pervasive and likely to be ecologically and evolutionarily important. Although the subject has already received substantial review, Kevin Lafferty here focuses on evolutionary aspects that have not been fully explored, specifically: (1) How strong should PITT be? (2) How might sexual selection and limb autotomy facilitate PITT? (3) How might infrapopulation regulation in final hosts be important in determining avoidance of infected prey? And (4) what happens when more than one species of parasite is in the same intermediate host?

Section snippets

How deep a PITT?

How dramatic should we expect PITT to be? If resources needed for PITT come at the expense of a parasite’s future reproductive success, parasites should invest an optimal intermediate amount of energy in PITT5, 10. An alternative hypothesis is that parasites will evolve to minimize energetic costs and that PITT will derive from mechanisms that are energetically efficient or are byproducts of infection or pathology.

Dobson¹¹ provided one of the first reviews about the strength of behavior

Intermediate hosts

If infection leads to increased predation, intermediate hosts should be under strong selective pressure to resist PITT1, 5, 14. Consequently, the magnitude of PITT might be the outcome of an evolutionary arms race between virulence and resistance. The literature is replete with examples of how parasites evade host defenses and how hosts respond to infection. Some parasites infect components of the vertebrate central nervous systems (CNS), perhaps because the CNS is poorly guarded by the host’s

Definitive hosts

In addition to modifying intermediate host behavior, the parasite must enlist the participation of the definitive host, who risks the consequence of becoming sick by eating infected prey. Thus, the evolution of PITT requires either that the parasite should be cryptic or that feeding on parasitized prey becomes less costly than avoiding such prey5, 14. Why do predators choose to feed on infected prey? It may simply be that predators are unable to distinguish between infected and uninfected prey.

Co-occurring parasites

In some cases, more than one trophically transmitted parasite may infect the same intermediate host. This might lead to a diversity of PITT strategies. For example, several trematodes use the California killifish as an intermediate host. Euhaplorchis californiensis alters killifish behavior while the others, such as Renicola buchanani, seem not to¹². All are probably able to use the same definitive host bird. In multiple infections, R. buchanani clearly benefits from increased transmission

PITT as an adaptive strategy

I have taken a different approach from other recent reviews of behavior modification by concentrating on PITT as an adaptive strategy and asking how it might evolve under different conditions. If PITT is a consequence of pathology, or if parasites are able to modify host neurobiology directly, PITT is likely to be strong. Alternatively, PITT should be more moderate if it requires an energy investment, or if intermediate hosts are able to mount a successful defense. Resistance of intermediate

Acknowledgements

I thank Greta Aeby, Todd Huspeni, Armand Kuris, Fr $e caa$ d $e caa$ ric Thomas and Mark Torchin for comments and for unpublished information.

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ReviewThe Evolution of Trophic Transmission

Abstract

Section snippets

How deep a PITT?

Intermediate hosts

Definitive hosts

Co-occurring parasites

PITT as an adaptive strategy

Acknowledgements

Anim. Behav.

Int. J. Parasitol.

Anim. Behav.

Anim. Behav

Trophic interactions: similarity of parasitic castrators to parasitoids

Q. Rev. Biol.

Ethological aspects of parasite transmission

Am. Nat.

Host life-history variation in response to parasitism

Parasitology

Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance?

Parasitology

The evolution of parasite manipulation of host behavior: a theoretical analysis

Parasitology

The population biology of parasite-induced changes in host behavior

Q. Rev. Biol.

Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts

Ecology

The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods

J. Parasitol.

Foraging on prey that are modified by parasites

Am. Nat.

Structure, development and behavior of new Strigeatoid metacercariae from subtropical fishes of South America

J. Fish. Res. Board Can.

Heritable true fitness and bright birds: a role for parasites?

Science

Review
The Evolution of Trophic Transmission