Limits...
Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research.

James TY, Toledo LF, Rödder D, da Silva Leite D, Belasen AM, Betancourt-Román CM, Jenkinson TS, Soto-Azat C, Lambertini C, Longo AV, Ruggeri J, Collins JP, Burrowes PA, Lips KR, Zamudio KR, Longcore JE - Ecol Evol (2015)

Bottom Line: We explore factors associated with variance in severity of epizootics focusing on the disease triangle of host susceptibility, pathogen virulence, and environment.Instead of focusing on pathogen "hot spots," we need to identify pathogen "cold spots" so that we can better understand what limits the pathogen's distribution.Finally, we introduce the concept of "the Ghost of Epizootics Past" to discuss expected patterns in postepizootic host communities.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology University of Michigan Ann Arbor Michigan 48109.

ABSTRACT
The amphibian fungal disease chytridiomycosis, which affects species across all continents, recently emerged as one of the greatest threats to biodiversity. Yet, many aspects of the basic biology and epidemiology of the pathogen, Batrachochytrium dendrobatidis (Bd), are still unknown, such as when and from where did Bd emerge and what is its true ecological niche? Here, we review the ecology and evolution of Bd in the Americas and highlight controversies that make this disease so enigmatic. We explore factors associated with variance in severity of epizootics focusing on the disease triangle of host susceptibility, pathogen virulence, and environment. Reevaluating the causes of the panzootic is timely given the wealth of data on Bd prevalence across hosts and communities and the recent discoveries suggesting co-evolutionary potential of hosts and Bd. We generate a new species distribution model for Bd in the Americas based on over 30,000 records and suggest a novel future research agenda. Instead of focusing on pathogen "hot spots," we need to identify pathogen "cold spots" so that we can better understand what limits the pathogen's distribution. Finally, we introduce the concept of "the Ghost of Epizootics Past" to discuss expected patterns in postepizootic host communities.

No MeSH data available.


Related in: MedlinePlus

Distribution of Batrachochytrium dendrobatidis genotypes determined from multilocus sequence typing of cultured isolates. Bd clades are identified by color, and the captive status of the host amphibians is indicated by shape. The area of each shape represents the sample size of genotypes from each locality. Notable samples include the following: a captive an isolate of Bd‐GPL‐2 from Xenopus laevis imported to U.C. Berkeley, California (1), an isolate of a novel Bd‐Brazil strain from Lithobates catesbeianus in a Michigan market (2), captive isolates of GPL‐2 from the National Zoo, Washington, D.C. (3), and the Bronx Zoo and markets in New York City (4), and a region of high genetic heterogeneity in the Atlantic Forest of southeastern Brazil (5). Isolates are considered GPL‐1 if they are heterozygous or homozygous for diagnostic alleles at loci BdC24, R6046, or both. Data are compiled from published sources (Morgan et al. 2007; James et al. 2009; Schloegel et al. 2012; Velo‐Anton et al. 2012) and unpublished data.
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ece31672-fig-0004: Distribution of Batrachochytrium dendrobatidis genotypes determined from multilocus sequence typing of cultured isolates. Bd clades are identified by color, and the captive status of the host amphibians is indicated by shape. The area of each shape represents the sample size of genotypes from each locality. Notable samples include the following: a captive an isolate of Bd‐GPL‐2 from Xenopus laevis imported to U.C. Berkeley, California (1), an isolate of a novel Bd‐Brazil strain from Lithobates catesbeianus in a Michigan market (2), captive isolates of GPL‐2 from the National Zoo, Washington, D.C. (3), and the Bronx Zoo and markets in New York City (4), and a region of high genetic heterogeneity in the Atlantic Forest of southeastern Brazil (5). Isolates are considered GPL‐1 if they are heterozygous or homozygous for diagnostic alleles at loci BdC24, R6046, or both. Data are compiled from published sources (Morgan et al. 2007; James et al. 2009; Schloegel et al. 2012; Velo‐Anton et al. 2012) and unpublished data.

Mentions: The basis for these phenotypic distinctions among lineages may be a product of genomic differences among them. A prominent feature of the GPL lineages is the presence of particular LOH events that must have occurred before the global dispersal of the GPL because they occur in every strain (Rosenblum et al. 2013); other LOH events occurred after GPL began to diversify and led to the formation of two clades within GPL, GPL‐1 and GPL‐2 (Schloegel et al. 2012). Based on the LOH model, we infer that GPL‐1 is the more ancestral variant because it differs from GPL‐2 by the absence of particular LOH events. GPL‐2 is the most common lineage in the tropics (Fig. 4) and is the genotype isolated from massive die‐offs in Central America and Australia (Berger et al. 1998). In contrast, GPL‐1 is most common in North America and is the lineage associated with epizootics of Rana muscosa in the Sierra Nevada (Schloegel et al. 2012). GPL‐1 also predominates in Europe, but has not been found in Australia or Africa. If we are correct in our inference that GPL‐1 is the ancestral panzootic lineage, this indicates that GPL first emerged in the northern temperate zone and later dispersed into the tropics. Interestingly, only rarely is the dominant tropical form (GPL‐2) found in temperate regions, and vice versa for GPL‐1. Importantly, the spatial distribution of GPL‐2 points in North America suggests a role for anthropogenic movement of frogs or pathogen (Fig. 4), because most of the GPL‐2 points represent isolates from animals in captivity, including one from Dendrobates azureus at the National Zoo in Washington, D.C. (the type strain JEL197), and another isolate from a Xenopus laevis strain imported to U.C. Berkeley from Africa in the 1980s (Morgan et al. 2007).


Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research.

James TY, Toledo LF, Rödder D, da Silva Leite D, Belasen AM, Betancourt-Román CM, Jenkinson TS, Soto-Azat C, Lambertini C, Longo AV, Ruggeri J, Collins JP, Burrowes PA, Lips KR, Zamudio KR, Longcore JE - Ecol Evol (2015)

Distribution of Batrachochytrium dendrobatidis genotypes determined from multilocus sequence typing of cultured isolates. Bd clades are identified by color, and the captive status of the host amphibians is indicated by shape. The area of each shape represents the sample size of genotypes from each locality. Notable samples include the following: a captive an isolate of Bd‐GPL‐2 from Xenopus laevis imported to U.C. Berkeley, California (1), an isolate of a novel Bd‐Brazil strain from Lithobates catesbeianus in a Michigan market (2), captive isolates of GPL‐2 from the National Zoo, Washington, D.C. (3), and the Bronx Zoo and markets in New York City (4), and a region of high genetic heterogeneity in the Atlantic Forest of southeastern Brazil (5). Isolates are considered GPL‐1 if they are heterozygous or homozygous for diagnostic alleles at loci BdC24, R6046, or both. Data are compiled from published sources (Morgan et al. 2007; James et al. 2009; Schloegel et al. 2012; Velo‐Anton et al. 2012) and unpublished data.
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ece31672-fig-0004: Distribution of Batrachochytrium dendrobatidis genotypes determined from multilocus sequence typing of cultured isolates. Bd clades are identified by color, and the captive status of the host amphibians is indicated by shape. The area of each shape represents the sample size of genotypes from each locality. Notable samples include the following: a captive an isolate of Bd‐GPL‐2 from Xenopus laevis imported to U.C. Berkeley, California (1), an isolate of a novel Bd‐Brazil strain from Lithobates catesbeianus in a Michigan market (2), captive isolates of GPL‐2 from the National Zoo, Washington, D.C. (3), and the Bronx Zoo and markets in New York City (4), and a region of high genetic heterogeneity in the Atlantic Forest of southeastern Brazil (5). Isolates are considered GPL‐1 if they are heterozygous or homozygous for diagnostic alleles at loci BdC24, R6046, or both. Data are compiled from published sources (Morgan et al. 2007; James et al. 2009; Schloegel et al. 2012; Velo‐Anton et al. 2012) and unpublished data.
Mentions: The basis for these phenotypic distinctions among lineages may be a product of genomic differences among them. A prominent feature of the GPL lineages is the presence of particular LOH events that must have occurred before the global dispersal of the GPL because they occur in every strain (Rosenblum et al. 2013); other LOH events occurred after GPL began to diversify and led to the formation of two clades within GPL, GPL‐1 and GPL‐2 (Schloegel et al. 2012). Based on the LOH model, we infer that GPL‐1 is the more ancestral variant because it differs from GPL‐2 by the absence of particular LOH events. GPL‐2 is the most common lineage in the tropics (Fig. 4) and is the genotype isolated from massive die‐offs in Central America and Australia (Berger et al. 1998). In contrast, GPL‐1 is most common in North America and is the lineage associated with epizootics of Rana muscosa in the Sierra Nevada (Schloegel et al. 2012). GPL‐1 also predominates in Europe, but has not been found in Australia or Africa. If we are correct in our inference that GPL‐1 is the ancestral panzootic lineage, this indicates that GPL first emerged in the northern temperate zone and later dispersed into the tropics. Interestingly, only rarely is the dominant tropical form (GPL‐2) found in temperate regions, and vice versa for GPL‐1. Importantly, the spatial distribution of GPL‐2 points in North America suggests a role for anthropogenic movement of frogs or pathogen (Fig. 4), because most of the GPL‐2 points represent isolates from animals in captivity, including one from Dendrobates azureus at the National Zoo in Washington, D.C. (the type strain JEL197), and another isolate from a Xenopus laevis strain imported to U.C. Berkeley from Africa in the 1980s (Morgan et al. 2007).

Bottom Line: We explore factors associated with variance in severity of epizootics focusing on the disease triangle of host susceptibility, pathogen virulence, and environment.Instead of focusing on pathogen "hot spots," we need to identify pathogen "cold spots" so that we can better understand what limits the pathogen's distribution.Finally, we introduce the concept of "the Ghost of Epizootics Past" to discuss expected patterns in postepizootic host communities.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology University of Michigan Ann Arbor Michigan 48109.

ABSTRACT
The amphibian fungal disease chytridiomycosis, which affects species across all continents, recently emerged as one of the greatest threats to biodiversity. Yet, many aspects of the basic biology and epidemiology of the pathogen, Batrachochytrium dendrobatidis (Bd), are still unknown, such as when and from where did Bd emerge and what is its true ecological niche? Here, we review the ecology and evolution of Bd in the Americas and highlight controversies that make this disease so enigmatic. We explore factors associated with variance in severity of epizootics focusing on the disease triangle of host susceptibility, pathogen virulence, and environment. Reevaluating the causes of the panzootic is timely given the wealth of data on Bd prevalence across hosts and communities and the recent discoveries suggesting co-evolutionary potential of hosts and Bd. We generate a new species distribution model for Bd in the Americas based on over 30,000 records and suggest a novel future research agenda. Instead of focusing on pathogen "hot spots," we need to identify pathogen "cold spots" so that we can better understand what limits the pathogen's distribution. Finally, we introduce the concept of "the Ghost of Epizootics Past" to discuss expected patterns in postepizootic host communities.

No MeSH data available.


Related in: MedlinePlus