Dr Jekyll and Mrs Hyde: Risky hybrid sex by amphibian-parasitizing chytrids in the Brazilian Atlantic Forests

Batrachochytrium dendrobatidis, the causative agent of the disease chytridiomycosis in amphibians, is now known to comprise of at least five phenotypically and phylogenetically deeply diverged lineages (Bataille et al. 2013; Farrer et al. 2011). In Robert Louis Stevenson's creation ‘The Strange Case of Dr Jekyll and Mr Hyde’, the good side of one man's character, the benign Dr Jekyll, becomes entirely physically separated and conflicts with the evil side of his character, the violent Mr Hyde. Analogous to this tale, the five described lineages each present very different faces of the chytrid species, Bd.

One lineage, BdGPL, has expanded recently to achieve its current worldwide distribution and this lineage underpins all known chytrid-driven amphibian mass mortalities to date. Three lineages, BdCH from Switzerland, BdCape from Southern Africa and BdBrazil from the Brazilian Atlantic Forest, exhibit a much lower virulence than BdGPL and are restricted in their distributions. A fifth lineage of unknown virulence level, BdKorea, appears to be endemic to Asia (Bataille et al. 2013). It has been hypothesized that the hypervirulent BdGPL arose through recombination of previously isolated (allopatric) lineages and has subsequently been spread around the world by anthropogenic means. Evidence for recombination in Bd was first described in 2007 (Morgan et al. 2007), but the fungus has never been observed to reproduce sexually and it was not until Schloegel et al.'s paper in 2012 that any potential hybrids of known lineages were described.

In Stevenson's story, Jekyll and Hyde alternately inhabit one body, never existing simultaneously. Bd lineages, however, are able to meet and interact as they are transported and expand in distribution around the world. What is unknown is what happens when these meetings occur. Do the Jekyll and Hyde lineages coexist or compete? If they do compete, which side wins? Could we have Dr Jekylls and Mrs Hydes, where lineages hybridize via sexual processes and give rise to mixed genotypes? How dangerous will these hybrids be?

Significant progress in the field of Bd research has been made by comparative genomic analysis of the lineages, revealing expansions in genes associated with virulence compared with nonpathogenic chytrids as well as significant evolutionary divergence between lineages of Bd. It has also been shown that different lineages of Bd are associated with the variation in phenotype and levels of virulence (Fisher 2008; Farrer et al. 2011). However, there are two major areas of research that need to be tackled when it comes to unravelling the evolutionary history and future trajectory of Bd: first, the marrying of extensive mapping work around the world with the genomics data, and the placing of this information in the public domain. This information is crucial to enable potential contact zones between different lineages to be identified, highlighting areas which should be watched especially closely for emergence of new lineages. This is because new lineages may also exhibit novel traits that present a risk to biodiversity, such as hypervirulence. Second, investigations into what happens when two lineages do meet in nature are needed. As Jenkinson et al. show, there is now convincing evidence that different Bd lineages are capable of hybridizing with each other. The frequency with which different Bd genotypes hybridize in contact zones; the long-term viability of offspring genotypes; and whether lineages compete, coexist or influence host survival differentially when in contact, are all extremely poorly understood. In demonstrating a clear hybrid zone, Jenkinson et al. have made a base from which to address these important questions in the context of the Brazilian Atlantic Forest (Fig. 1).

In a wider context, the evolution of virulence in mycoses is becoming a truly urgent issue to tackle. With emerging fungal pathogens on the rise in animals and plants, global wildlife health, food security and ecosystem stability are threatened (Fisher et al. 2012). To control these mycoses, we need to understand the factors leading to (and to be able to accurately reconstruct) their geographical expansion and emergence. This is an area which to date has been poorly addressed and this study is a step forward in investigating this much wider issue. Research into how to mitigate these diseases is hampered by disproportionately low levels of funding. Fungi, as illustrated by the hybridization described here, have extremely plastic genomes and an extraordinary ability to adapt to changing environments or hosts, making them formidable targets for disease control. Understanding how fungal pathogens interact with each other, with their hosts, and the environment will be crucial for sustaining biodiversity, human health and food security in the future.

This study points towards the next frontiers in chytrid and emerging mycoses research more generally. The next tasks for the research community are as follows: (i) understand the evolutionary nuances of lineage within species; (ii) trying to predict whether, when and how lineages will interact with each other; and (iii) whether these interactions will ultimately impact host survival and onwards pathogen spread. Emerging fungal infections are a global, omnipresent threat not only to wildlife but also to crops and human health. To manage these threats, it will be necessary to delve deep into their evolutionary history and to understand what the factors were that drove them to become threats in the first place. It will be necessary to go beyond simple documentation of what is present now into the much more complex questions of where these pathogens came from, and how to predict where the next generations of Jekyll and Hyde hybrids will emerge in the future.

P.G. and M.C.F. both wrote this paper. Their research focusses on Bd evolutionary dynamics. Both authors are funded by the UK Natural Environmental Research Council.