Department of Microbiology, Abasaheb Garware College, Karve Road, Pune 411 004, India

Life Research Foundation 10, Pranav, 1000/6-c Navi Peth, Pune 411 030, India

Abstract

Background

For parasites with a predator-prey life cycle, the completion of the life cycle often depends on consumption of parasitized prey by the predator. In the case of such parasite species the predator and the parasite have common interests and therefore a mutualistic relationship is possible. Some evidence of a predator-parasite mutualism was reported from spotted deer or chital (

Results

A tolerant predator strategy and a low or moderately virulent parasite strategy which together constitute mutualism are stable only at a high frequency of recycling of parasite and a substantial prey – capture benefit to the predator. Unlike the preliminary expectation, parasite will not evolve towards reduced virulence, but reach an optimum moderate level of virulence.

Conclusion

The available data on the behavioral ecology of dhole and chital suggest that they are likely to meet the stability criteria and therefore a predator-parasite mutualism can be stable in this system. The model also points out the gaps in the current data and could help directing further empirical work.

Background

Preferential killing of sick and disabled prey individuals by the predator has been the focus of many ecologists working with different predator – prey systems. In a variety of prey predator systems, diseased or weaker animals are shown to be consumed in greater proportion by predators

There can be a potential problem in such a mutualistic relationship. Low virulence of the parasite towards the predator host and parasite tolerance by the predator host are essential factors for the maintenance of a mutualistic relationship. However, it is possible that a virulent parasite can grow faster and invade a mild parasite population. On the other hand a parasite resistant predator can avoid the cost of parasitism but share the benefit of prey capture and therefore invade a tolerant population. Either of the events can destabilize the mutualistic relationship. It is essential therefore to examine the evolutionary stability of the mutualism. In a completely randomized distribution, a mild parasite population can be easily invaded by a virulent one and a tolerant predator can be invaded by a resistant one. Population viscosity, group selection and kin selection can alter the evolution of virulence

We examine here the effect of parasite recycling on the evolution of a predator-parasite mutualism, using a theoretical model.

The model

We consider two alternative strategies, namely mild and virulent, for the parasite (Table

Pay – off matrix for predator and parasite strategies.

parasite

predator

Mild

Virulent

Tolerant

Resistant

parasite

Mild

1-y

fr(1-y)+(1-fr)(1-x)

m

p* m

Virulent

fr(1-x)+(1-fr)(1-y)

(1-x)

v

p* v

predator

Tolerant

-y

-x

z

(1-fr) p *z + fr *z

Resistant

- p * y

- p* x

(1-fr)*z + fr (p* z)

p* z

The table differs from pay-off matrix tables for classical game theory models. The table accounts for two alternative strategies each for two different types of players namely parasite and predator. The pay-off of the parasite is not only decided by other parasites but also by the predator strategy and vice-versa. Therefore the complete pay-off of a mild parasite invading a virulent population in a tolerant host population is m * [fr(1-y)+(1-fr)(1-x)]. Others to be calculated similarly.

If the parasite population consists of the mild type, they enjoy a fitness of 'm' from the tolerant host and 'p*m' from a resistant one. Since they exert a cost y on the host, there is erosion of the host resource. The host resource available to them is therefore (1-y). Similarly for a population of virulent parasites the mean fitness gain is v and the host resource available (1-x). A virulent host invading a mild population will gain a fitness of 'v' such that v > m. In the absence of recycling the host resource available to it would be (1-y). However with a frequency of recycling 'fr', the host resource would be,

fr (1-x) + (1-fr)(1-y)

Similarly, that for a mild parasite invading a virulent population would be,

fr (1-y) + (1-fr)(1-x)

If the predator population is tolerant the parasite will be harbored in large numbers and disseminated to the prey population. Since the parasitized prey is more susceptible to predation the predator gets a benefit 'z' of easy catching. A resistant population, on the other hand has a small probability 'p' of harboring the parasite. Therefore the benefit the predator gets would be 'p*z'. If a resistant predator invades a tolerant population, with the recycling factor 'fr', the benefit of prey capture would be,

fr * p *z + z(1-fr).

The benefit for a tolerant one invading a resistant population would be,

fr * z + (1-fr)* p*z.

We assume that 'v', the benefit for a virulent parasite by infecting single host is directly proportional to 'x' i.e the loss to the host from infection by virulent parasite.

V = α *x similarly, m = α *y

Results and discussion

A mild parasite will be able to invade a virulent population if the pay-off to the mild invader is greater than that for the virulent population. When the predator population is tolerant, this condition is satisfied when,

y * [fr (1-y)+(1-fr) (1-x)] > x (1-x)

The condition under which a virulent invader is unable to invade a mild population is

(1-y)* y > [fr *(1-x) + (1-fr)*(1-y)]*x

Since x > y, for satisfying both these conditions, fr should be large, y should be moderate and x should be large. Thus selection would favour a moderate virulence in the parasite towards the predator host. Unlike our expectation, low virulence is unlikely to be stable. However, a mutualistic relation can remain if the prey capture benefit is sufficiently large. It can be easily seen that the above conditions remain unaffected even if the predator population is resistant.

Considering predator strategies, a tolerant predator will be able to invade a resistant population in the presence of a mild predator if,

p *z - p*y < (1-fr) p *z + fr*z - y

i. e. p*fr * z - p* y < fr *z - y

This condition will be satisfied if fr *z > y since p < 1. A resistant predator will be unable to invade a tolerant population since the necessary condition is

z-y < (1-fr)*z + fr*(p*z) - (p * y)

fr*z - y < p*fr*z - p*y

This invasion is impossible if fr*z > y. If the parasite is virulent, the necessary condition would be fr*z > x. Since x is assumed to be large, a resistant predator would be stable if the prevalent parasite strategy is virulent.

Thus when fr and z are large and y is small mutualism would be stable. When this condition is not satisfied the predator will evolve resistance to the parasite and the parasite will evolve greater virulence.

Conclusion

A large recycling frequency (fr) appears to be the only critical factor in the evolution of parasite virulence. However, the parasite is unlikely to evolve towards low virulence. There will be a moderate virulence optimum. For a net benefit to the host the cost associated with this level of virulence should be less than the benefit in terms of ease of prey capture.

For the evolution and stability of the tolerant strategy in the predator a large fr as well as large z and small y are necessary. A predator-parasite mutualism therefore critically depends upon these factors, whereas it is independent of p and α.

In the case of Dhole-chital – ^{2 }

Although we are far from having an empirical estimate of y, fr and z, the known ecology of chital and dhole suggest that fr and z could be sufficiently large. This makes the system a likely candidate for the evolution of predator parasite mutualism. Any other predator-prey system that satisfies these conditions is also likely to co-evolve with some parasite species towards a predator-parasite mutualism. Parasites of diverse taxa have evolved predator-prey life cycles and any of them could be possible candidates for a mutualism. Predator-prey-parasite systems that satisfy the following three criteria are the most likely candidates for a stable mutualistic relationship:

i) parasitized prey individuals are killed with substantially greater frequency by the predator

ii) pathogenicity of the parasite towards the predator host is low or moderate

iii) there is a high rate of parasite recycling to the predator host.

We need to look at a number of systems that could satisfy these criteria. The chital-dhole-

Authors' contributions

Both authors have contributed approximately equally to the model development.

Acknowledgements

We are grateful to the Department of Science & Technology, Govt. of India for financially assisting this work. We thank the forest departments of Tamilnadu and Maharashtra State for their permission for field work. We thank Dr. R. Sukumar, CES, field station in Mudumalai for providing necessary facilities, and Arun Venkatraman and R. Arumugum for their active interaction during field work. Discussions with Dr. S. A. Paranjape, Dr. N. V. Joshi and Arun Venkatraman were useful. We are grateful to Prof. Arun Bhagwat for his help in language and presentation during revision of the manuscript. We also thank Sachin, Krushnamegh, Rahul, Shantanu and Dilip for field support.