Fungi in the phylum Chytridiomycota are incredibly ancient, biologically diverse, geographically widespread, and generally overlooked. Chytrids tend to be tiny, inconspicuous organisms that do not produce harmful compounds or cause diseases of plants or animals. Consequently, there has been little impetus to study their biology, diversity, or geographic distribution. Unfortunately, what finally gave chytrids some notoriety is the recent emergence of a single species, Batrachochytrium dendrobatidis (Chytridiomycota; Chytridiales), as a ubiquitous and deadly amphibian pathogen.
Amphibians are disappearing worldwide at an alarming rate, and several factors contribute to the decline and extinction of many species, including habitat loss, environmental contaminants, and UV-B irradiation. One of the most alarming and devastating causes of declines is Batrachochytrium dendrobatidis (or Bd), which causes a skin infection of metamorphosed amphibians called chytridiomycosis (1). The precise cellular processes that lead to morbidity and mortality in amphibians remain unclear (2). Bd is the first chytrid fungus known to parasitize vertebrate animals, affecting over 100 species worldwide (3), and Bd has only been recognized as the cause of amphibian declines within the last ten years (4). This has prompted questions about Bd’s geographic origin, and when, how and why it has spread across the globe. The answer proves characteristic of our current era of globalization: humans appear to be responsible for spreading Bd across the globe.
Xenopus laevis is an African frog species known as the amphibian “model organism,” primarily due to its suitability for studying immunology and developmental biology in a laboratory setting. Xenopus laevis is endemic to southern Africa, where the oldest record of Bd was found in the skin of museum specimens dating back to 1938 (5). However, Bd has never been reported to cause X. laevis mortality in nature, and laboratory inoculations with Bd only cause mild infections (6). In the 1930s, a human pregnancy test was developed using female X. laevis individuals, which are induced to ovulate when injected with urine from pregnant women (7). This finding resulted in the massive export of thousands of X. laevis frogs per year from Africa to labs all over the world, where they were used to produce the first home pregnancy test. Bd is an aquatic fungus that produces motile zoospores, so we think Bd may have originally spread from these laboratory X. laevis individuals to wild frogs through the water they were housed in. Also, some laboratory X. laevis frogs escaped and established feral populationsÃ¢â‚¬â€first discovered in the 1960s in the United Kingdom and the United States, and in 1985 in Chile—and these feral frogs may have directly spread the fungus to native frog species (8).
Although frogs are no longer used to produce pregnancy tests, X. laevis has persisted worldwide in research labs, feral populations, and the pet trade, providing countless opportunities for spreading Bd to native species. Thus, the leading hypothesis explaining the chytridiomycosis epidemic is that, because non-African amphibians did not co-exist with Bd over long periods of time, they presumably have not evolved any resistance mechanisms to fight chytridiomycosis, while X. laevis from Africa has been exposed over a long enough period of time to evolve defenses against Bd. Consistent with the hypothesis that Bd was recently spread across the world, phylogenetic studies of nuclear genes (9) and microsatellite markers (A. Savage, unpublished data) find very little genetic polymorphism across Bd strains isolated from every continent, suggesting all strains come from a single species that has only recently existed worldwide and therefore hasn’t had time to diverge.
Several findings contradict the “out of Africa” hypothesis for the origin and spread of Bd. For example, the initial cases of chytridiomycosis occurred at the same time on different continents (5), but X. laevis was introduced to each of these locations at different time points. This suggests a pervasive environmental factor, such as global warming, may have contributed to the initial pathogenicity of Bd, rather than the exact time point the fungus was introduced. The African origin of Bd is also questionable. Museum collections are not extensive or old enough to accurately plot the historical distribution of Bd in amphibians; the fact that the oldest known infection is from an African frog may simply be coincidental. Further, if Africa is truly the continent of Bd’s origin, then African strains should have more genetic diversity than strains recently introduced elsewhere, but there are no significant differences in DNA variability among African strains compared to strains from any other continent. These issues are currently unresolved, but the Bd genome sequence has just been released (10), and should provide considerable insight into the biological differences and genetic composition of Bd strains, worldwide.
For more information about Bd and amphibian declines, please see my previous blog entry.
- Berger L et al. (1998) PNAS USA 95:9031-6.
- Piotrowski JS et al. (2004) Mycologia 96: 9-15.
- The Global Amphibian Assessment, IUCN (2004).
- Barinaga M (1990) Science 247:1033-34
- Weldon C et al. (2004) Emer Infect Dis 10: 2100-5.
- Parker JM et al. (2002) Comp Med 52: 265-8.
- Shapiro HA, Zwarenstein H (1934) Nature 133: 762.
- Tinsley RC, McCoid MJ (1996) In: The biology of Xenopus. Oxford, UK: Clarendon Press, p. 81-94.
- Morehouse EA et al. (2003) Mol Ecol 12: 395-403.
- Batrachochytrium dendrobatidis database, Broad Institute (2006).
Photos courtesy of the author, Anna Savage