Global Epidemiology of Batrachochytrium dendrobatidis Emergence
Following the discovery that Bd was a key driver of declines in amphibian species in Australia and the Americas (Berger et al. 1998; Longcore et al. 1999), attention has been focused on determining where outbreaks of chytridiomycosis have occurred and whether there were any spatiotemporal patterns that indicate the original sources of infection as well as pathways of spread.
A key technological advance has been the development of a Bd-specific quantitative PCR reaction that has been widely used to screen amphibian populations for infection (Boyle et al. 2004). A global mapping project (http://www.bd-maps.net) (Olson et al. 2013) showed Bd occurred in 56 of 82 (68%) countries and, in 516 of 1240 (42%) species tested, determined using a dataset of more than 36,000 individuals (Bd-maps.net data snapshot August 2012). Across the world, broadscale distribution patterns are evident, with Bd widely detected in the Americas and detected only patchily in Australia, Africa, Asia, and Europe.Combining data on amphibian population health alongside molecular qPCR surveys has uncovered regional epidemiological trends. In eastern Australia, prospective and retrospective sampling of amphibian populations showed that populations were Bd-negative prior to 1978 followed by an expansion north and south from an inferred centre in Southern Queensland, reaching its northern limits in the mid-1990s. Western Australia was Bd-negative until mid-1985 where upon the arrival and spread of disease was documented (Berger et al. 2009). Mesoamerica has witnessed a very rapid wave-like front of expansion from a putative origin in Mexico in the 1970s (James et al. 2006), through Guatemala to Monteverde, Costa Rica, in the 1980s, and then southwards at estimated rates of up to 50 km y 1, until the infection jumped the Panama Canal. This epidemic front of chytridiomycosis along the North-South transect of Central America was predictable to the extent that researchers were able to anticipate the arrival of Bd in uninfected regions, such as El Cope in Panama in 2004, and to then document the subsequent collapse of the amphibian community (Lips et al.
2008). North America saw steep declines across populations of the Sierra mountain yellow-legged frogs (Rana muscosa and R. sierrae), most notably in the Sequoia-Kings Canyon National Park, where regional populations were sequentially extirpated as Bd invaded lakes in 2004 (Vredenburg et al. 2010). However, historical declines across other regions of the Sierras suggest that the infection had been present since at least the 1970s, and elsewhere in the United States, retrospective surveys of museum collections have demonstrated a widespread prevalence since as early as 1888 in Illinois (Talley et al. 2015).Although the pattern of declines in Ecuador, Venezuela, Bolivia and Peru are consistent with Chytridiomycosis, most of South America lacks convincing evidence for outbreaks of chytridiomycosis, and retrospective analyses of museum specimens have shown Bd to be enzootic in the Brazilian Atlantic Forests for over a century (Rodriguez et al. 2014). Surveillance in Europe showed that outbreaks occurred around the 1990s in Spain (Bosch et al. 2001; Walker et al. 2010); however, it is suspected that asymptomatic infections were widespread prior to the 1990s as outbreaks of the disease have only been witnessed at high altitudes (Walker et al.
2010). In Southeast Asia, Bd has a low prevalence, patchy distribution and outbreaks of chytridiomycosis, or cryptic population declines have not been recorded (Sweietal. 2011).
Given these patterns of declines, is it possible to determine whether there is a single original ‘source’ of the panzootic of chytridiomycosis or are we rather witnessing multiple regional and perhaps unlinked foci? Answers to this question have been sought by attempting to identify geographic regions where Bd has had a long and stable association with host species (which is possibly indicative of longterm co-evolutionary associations), as well as through phylogenomic analyses. Histological studies from Southern African museum collections (Weldon et al.
2004; Soto-Azat et al. 2010) identified Africa as a potential source of the panzootic, leading to the ‘Bd Out of Africa’ hypothesis being coined to suggest that Bd was spread around the world via the extensive trade in the African clawed frog Xenopus laevis from the 1930s onwards. However, the widespread occurrence of century-old infections from similar retrospective studies means that Brazil, the United States and Asia are now also included as possible origins (Goka et al. 2009; Rodriguez et al. 2014; Talley et al. 2015; Fong et al. 2015).A paradigm shift in our understanding of Bd’s epidemiology occurred with the onset of high-throughput whole-genome sequencing (WGS). The phylogenetic resolution afforded by being able to align and detect single-nucleotide polymorphisms (SNPs) across the ~24 Mb genome of Bd has uncovered over 500,000 polymorphic sites. An initial phylogenetic analysis of 20 global isolates showed that Bd is composed of at least 3 deeply diverged lineages (Farrer et al.
2011). Of these, one was found to have a global distribution and showed low levels of genetic polymorphism as well as a lack of genetic structure among continents. These data are consistent with a rapid global emergence that was dated to sometime in the twentieth century, and accordingly the lineage was named the ‘Bd Global Panzootic Lineage’ (Bd GPL). Alongside Bd GPL, two other regionally endemic lineages were identified: one was found in Switzerland (Bd CH), while the other was found widely occurring in South Africa (Bd CAPE). Subsequent genome sequencing of Bd isolates from other global regions identified a fourth endemic lineage that infects amphibians in the Brazilian Atlantic forest (Bd Brazil) (Rodriguez et al.
2014). Further genome sequencing from a broader spatial collection of isolates will undoubtedly uncover further endemic lineages, consolidating the finding that Bd is an amphibian pathogen with a broad global distribution and ancient associations with its amphibian hosts.
These phylogenomic analyses have shown that the worldwide emergence of Chytridiomycosis is mostly likely explained by the rapid transmission of Bd GPL across a global scale as this lineage has now been found to co-occur in all continents alongside endemic lineages. In support of this hypothesis is that all mass mortality and extinction events thus far attributed to chytridiomycosis are associated with the presence of Bd GPL. In vivo laboratory assessments of Bd's virulence have shown that the lineage is hypervirulent when compared against other lineages, a feature that confers “superbug” status on Bd GPL (Farrer et al. 2011). However, the origin of Bd GPL remains currently unknown, as are details on the historical timing of this lineage's emergence across different continents. Answers to these questions await the accumulation of genome sequences from a more representative set of spatial regions and a more nuanced understanding of the molecular clock rates that govern Bd's evolution (Rosenblum et al. 2013; Farrer et al. 2013).
What is clear, however, is that the global trade in amphibians is a potent force in spreading Bd into naive populations and species. This statement is especially true for the so-called ‘Typhoid Mary' species such as X. laevis and the North American bullfrog Lithobates catesbeianus; these species carry Bd infections but rarely become diseased (Fisher et al. 2009). They are also widely traded and are often highly invasive when introduced by accident or deliberately into new environments (Lips et al. 2008). Therefore, these two species constitute ideal vectors for introducing Bd into uninfected regions of the globe (Garner et al. 2006) and are likely a major source of new Bd infections when released into naive environments. Molecular epidemiology from whole-genome sequencing is now being used to identify the sources of regional outbreaks. The best understood example of this is the introduction of Bd onto the Balearic island of Mallorca where genome sequencing showed that Bd CAPE was found to be infecting two populations of Mallorcan midwife toads Alytes muletensis. Retrospective analyses identified a spillover event within a zoo captive assurance population of A. muletensis that had been subsequently released onto the island in order to supplement the wild populations. In this example, the co-housing of Southern African Xenopus species alongside A. muletensis led to cross-transmission and the vectoring of Bd CAPE onto the island (Walker et al. 2008; Doddington et al. 2013).
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