Cryptic diversity of a widespread global pathogen reveals expanded threats to amphibian conservation

Byrne, Allison Q.; Vredenburg, Vance T.; Martel, An; Pasmans, Frank; Bell, Rayna C.; Blackburn, David C.; Bletz, Molly C.; Bosch, Jaime; Briggs, Cheryl J.; Brown, Rafe M.; Catenazzi, Alessandro; López, Mariel Familiar; Figueroa-Valenzuela, Raul; Ghose, Sonia L.; Jaeger, Jef R.; Jani, Andrea J.; Jirků, Miloslav; Knapp, Roland A.; Muñoz, A.; Portik, Daniel M.; Richards‐Zawacki, Corinne L.; Rockney, Heidi; Rovito, Sean M.; Stark, Tariq; Sulaeman, Hasan; Tao, Nguyen Thien; Voyles, Jamie; Waddle, Anthony W.; Yuan, Zhongwei; Rosenblum, Erica Bree

doi:10.1073/pnas.1908289116

Cited by 100 publications

(156 citation statements)

References 37 publications

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“…The other, putatively less virulent lineages of Bd include: a Brazilian lineage endemic to the Atlantic Forest region of southern Brazil, BdBrazil (also known as BdBrazil/Asia2) [92,94]; an African lineage endemic to the Cape region of South Africa, BdCape [93]; and an endemic Asian lineage BdAsia1, believed to be closest to the source of origin for Bd diversity [92]. Recently, the existence of an additional endemic lineage, BdAsia3, widespread throughout southeast Asia was reported from amphibian swabs [95].…”

Section: The Amphibian Chytrid Batrachochytrium Dendrobatidismentioning

confidence: 99%

“…The other two known Bd hybrids are described from the Eastern Cape Province of South Africa where BdGPL and BdCape overlap. Putative hybrid isolates were also identified from genotyping DNA from amphibian skin swabs, but these could also be explained by coinfection [95]. Unlike the narrow geographic range of the Brazilian hybrid zone, the two South African hybrid isolates were collected approximately 200 km apart from one another [92].…”

Section: Hybrids In Batrachochytrium Dendrobatidismentioning

confidence: 99%

“…Unlike the narrow geographic range of the Brazilian hybrid zone, the two South African hybrid isolates were collected approximately 200 km apart from one another [92]. Additional regions where secondary contact could occur along with hybridization are Europe, western Africa, and Central America [92,95,98]. These regions are of interest with respect to hybridization because they harbor BdGPL and BdCape lineages which are already known to hybridize.…”

Section: Hybrids In Batrachochytrium Dendrobatidismentioning

confidence: 99%

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Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

Samarasinghe

You

Jenkinson

et al. 2020

Genes

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Hybridization is increasingly recognized as an important force impacting adaptation and evolution in many lineages of fungi. During hybridization, divergent genomes and alleles are brought together into the same cell, potentiating adaptation by increasing genomic plasticity. Here, we review hybridization in fungi by focusing on two fungal pathogens of animals. Hybridization is common between the basidiomycete yeast species Cryptococcus neoformans × Cryptococcus deneoformans, and hybrid genotypes are frequently found in both environmental and clinical settings. The two species show 10–15% nucleotide divergence at the genome level, and their hybrids are highly heterozygous. Though largely sterile and unable to mate, these hybrids can propagate asexually and generate diverse genotypes by nondisjunction, aberrant meiosis, mitotic recombination, and gene conversion. Under stress conditions, the rate of such genetic changes can increase, leading to rapid adaptation. Conversely, in hybrids formed between lineages of the chytridiomycete frog pathogen Batrachochytrium dendrobatidis (Bd), the parental genotypes are considerably less diverged (0.2% divergent). Bd hybrids are formed from crosses between lineages that rarely undergo sex. A common theme in both species is that hybrids show genome plasticity via aneuploidy or loss of heterozygosity and leverage these mechanisms as a rapid way to generate genotypic/phenotypic diversity. Some hybrids show greater fitness and survival in both virulence and virulence-associated phenotypes than parental lineages under certain conditions. These studies showcase how experimentation in model species such as Cryptococcus can be a powerful tool in elucidating the genotypic and phenotypic consequences of hybridization.

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Section: The Amphibian Chytrid Batrachochytrium Dendrobatidismentioning

confidence: 99%

Section: Hybrids In Batrachochytrium Dendrobatidismentioning

confidence: 99%

Section: Hybrids In Batrachochytrium Dendrobatidismentioning

confidence: 99%

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Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

Samarasinghe

You

Jenkinson

et al. 2020

Genes

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“…There is considerably more information on Bd distribution than Bd genotypes; however, where population declines occur and Bd has been genotyped, it has been shown that the pathogen is of the Bd‐GPL lineage. Few places are known to contain multiple lineages (Byrne et al., 2019; O’hanlon et al., 2018; Schloegel et al., 2012), and this may speak to the ability of Bd‐GP L to outcompete enzootic lineages. Recent findings have shown that when Bd‐GPL and the older Brazilian strain (now considered Bd ‐ASIA‐2/ Bd ‐BRAZIL; see O’hanlon et al., 2018) are co‐inoculated onto a single host, Bd‐GPL grows much faster, suggesting that it has the potential to outcompete endemic strains (Jenkinson et al., 2018).…”

Section: Introductionmentioning

confidence: 99%

Genetic analysis of post‐epizootic amphibian chytrid strains in Bolivia: Adding a piece to the puzzle

Burrowes

James

Jenkinson

et al. 2020

Transbound Emerg Dis

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The evolutionary history and dispersal pattern of Batrachochytrium dendrobatidis (Bd), an emergent fungal pathogen responsible for the decline and extinctions of many species of amphibians worldwide, is still not well understood. In South America, the tropical Andes are known as an important site for amphibian diversification, but also for being a place where hosts are at greater risk of chytridiomycosis. In an attempt to understand the history and the geographic pattern of Bd‐associated amphibian declines in Bolivia, we isolated Bd from hosts at two locations that differ in their chronology of Bd prevalence and host survival outcome, the cloud forests of the Amazonian slopes of the Andes and Lake Titicaca in the altiplano. We genotyped Bd from both locations and sequenced the genome from the cloud forest isolate and then compared them to reference sequences of other Bd strains across the world. We found that the Bolivian chytrid isolates were nearly genotypically identical and that they belong to the global panzootic lineage (Bd‐GPL). The Bolivian Bd strain grouped with other tropical New World strains but was closest to those from the Brazilian Atlantic Forest. Our results extend the presence of Bd‐GPL to the central Andes in South America and report this hypervirulent strain at Lago Titicaca, where Bd has been detected since 1863, without evidence of amphibian declines. These findings suggest a more complex evolutionary history for this pathogen in Bolivia and may point to the existence of an old lineage of Bd that has since been extirpated following the arrival of the panzootic Bd‐GPL or that the timing of Bd‐GPL emergence is earlier than generally acknowledged.

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“…Within Bd there are at least six phylogenetically distinct lineages -BdCAPE, BdGPL, BdASIA-1, BdASIA-2/BRAZIL, BdASIA-3 and BdCH. However, BdCAPE and BdGPL are primarily associated with mass mortality events and species declines or extinctions (Byrne et al, 2019;Farrer et al, 2011;Doddington et al, 2013;Jenkinson et al, 2016;O'Hanlon et al, 2018). While only BdGPL has undergone a rapid, recent and global range expansion, recent research indicates that the other five lineages, which had previously been considered largely spatially restricted, have achieved intercontinental distributions.…”

Section: Introductionmentioning

confidence: 99%

Discriminating Lineages ofBatrachochytrium dendrobatidisusing quantitative PCR

Ghosh

Verster

Sewell

et al. 2020

Preprint

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The ability to detect and monitor infectious disease in a phylogenetically informative manner is critical for their management. Phylogenetically informative diagnostic tests enable patterns of pathogen introduction or changes in the distribution of genotypes to be measured, enabling research into the ecology of the pathogen. Batrachochytrium dendrobatidis (Bd), a causative agent of chytridiomycosis in amphibian populations, emerged worldwide in the 21st century and is composed of six lineages which are display varying levels of virulence in their hosts. Research into the distribution, ecology and pathogenicity of these lineages has been hampered by an inability to type lineage efficiently. Here, we describe a lineage-specific TaqMan qPCR assay that differentiates the two lineages of Bd most commonly associated with chytridiomycosis: BdGPL and BdCAPE. We demonstrate how this assay can be used for the surveillance of wild populations of amphibians in Southern Africa using skin swabs, tissue samples and cultured isolates.

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Cryptic diversity of a widespread global pathogen reveals expanded threats to amphibian conservation

Cited by 100 publications

References 37 publications

Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

Genetic analysis of post‐epizootic amphibian chytrid strains in Bolivia: Adding a piece to the puzzle

Discriminating Lineages ofBatrachochytrium dendrobatidisusing quantitative PCR

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