Abstract

Coevolution between ant colonies and their rare specialized parasites are intriguing, because lethal infections of workers may correspond to tolerable chronic diseases of colonies, but the parasite adaptations that allow stable coexistence with ants are virtually unknown. We explore the trade-offs experienced by Ophiocordyceps parasites manipulating ants into dying in nearby graveyards. We used field data from Brazil and Thailand to parameterize and fit a model for the growth rate of graveyards. We show that parasite pressure is much lower than the abundance of ant cadavers suggests and that hyperparasites often castrate Ophiocordyceps. However, once fruiting bodies become sexually mature they appear robust. Such parasite life-history traits are consistent with iteroparity– a reproductive strategy rarely considered in fungi. We discuss how tropical habitats with high biodiversity of hyperparasites and high spore mortality has likely been crucial for the evolution and maintenance of iteroparity in parasites with low dispersal potential.

Highlights

  • Specialized parasites that interact with a single or narrow spectrum of hosts tend to have fascinating life-histories, because virulence and defence traits are likely to have been shaped by coevolutionary arms races [1,2]

  • We identified ants infected with O. camponoti-rufipedis by searching the underside of leaves along a ca. 460 m stretch of forest path and found five graveyards [27] with a high density of dead C. rufipes, each of them situated around a single host ant colony

  • We found that 30/31 O. unilateralis s.l monitored for 18 months became infected by hyperparasitic fungi

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Summary

Introduction

Specialized parasites that interact with a single or narrow spectrum of hosts tend to have fascinating life-histories, because virulence and defence traits are likely to have been shaped by coevolutionary arms races [1,2]. This is true for parasites that have evolved ways to manipulate host behaviour, so that dying hosts express extended phenotypes that serve parasite reproductive success [3,4]. Several lineages have evolved species that attack ants [6] leading to behavioural extended phenotypes, i.e. host manipulation, to make infected ants leave their nests to die and disperse spores in ways that serve parasite fitness [7]. Even though individual ants may die from infection, theory predicts that disease-induced mortality of mature ant colonies should be low, albeit evidence is only available for some species [17]

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