Abstract

Hybridization of parasites can generate new genotypes with high virulence. The fungal amphibian parasite Batrachochytrium dendrobatidis (Bd) hybridizes in Brazil’s Atlantic Forest, a biodiversity hotspot where amphibian declines have been linked to Bd, but the virulence of hybrid genotypes in native hosts has never been tested. We compared the virulence (measured as host mortality and infection burden) of hybrid Bd genotypes to the parental lineages, the putatively hypovirulent lineage Bd-Brazil and the hypervirulent Global Pandemic Lineage (Bd-GPL), in a panel of native Brazilian hosts. In Brachycephalus ephippium, the hybrid exceeded the virulence (host mortality) of both parents, suggesting that novelty arising from hybridization of Bd is a conservation concern. In Ischnocnema parva, host mortality in the hybrid treatment was intermediate between the parent treatments, suggesting that this species is more vulnerable to the aggressive phenotypes associated with Bd-GPL. Dendropsophus minutus showed low overall mortality, but infection burdens were higher in frogs treated with hybrid and Bd-GPL genotypes than with Bd-Brazil genotypes. Our experiment suggests that Bd hybrids have the potential to increase disease risk in native hosts. Continued surveillance is needed to track potential spread of hybrid genotypes and detect future genomic shifts in this dynamic disease system.

Highlights

  • The host-parasite dynamic is a classic example of an evolutionary arms race; hosts face pressure to evolve defenses against parasites, while parasites face pressure to overcome host defenses[1,2]

  • Mortality was first observed in frogs exposed to Batrachochytrium dendrobatidis (Bd)-GPL on day 26 and 6/9 frogs (67%) died by the end of the experiment (Fig. 1a)

  • Mortality was first observed in frogs exposed to Bd-GPL on day 18 and 6/6 frogs (100%) died by day 27 (Fig. 1b)

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Summary

Introduction

The host-parasite dynamic is a classic example of an evolutionary arms race; hosts face pressure to evolve defenses against parasites, while parasites face pressure to overcome host defenses[1,2]. Epizootic outbreaks of chytridiomycosis are predominantly associated with spread of the most recently derived lineage of Bd, termed the Global Panzootic Lineage (Bd-GPL) These outbreaks occurred in the Andes[29], Brazil[30], Central America[31], the Caribbean[32], California[33], Spain[34], Cameroon[35], New Zealand[36], and eastern Australia[37], mostly in the 1970s–2000s. In contrast to Bd-GPL, Bd lineages of Brazilian[38], Chinese[39], Japanese[40], Korean[41], Swiss, and South African[32] origin diverged early in the evolutionary history of Bd and have not been directly linked to host population declines. Amphibian declines and extirpations in the Atlantic Forest have been linked to Bd30, but it is unknown whether outbreaks resulted from the introduction of Bd-GPL, an increase in virulence of Bd-Brazil, the emergence of GPL-Brazil hybrids, or some combination of these factors[30]. Testing the relative virulence of these genotypes is a research priority, especially considering that the section of the Atlantic Forest in which amphibian declines and extirpations were most strongly linked to Bd overlaps with the hybrid zone[30]

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