skip to main content

Title: Amphibian‐killing chytrid in B razil comprises both locally endemic and globally expanding populations

Chytridiomycosis, caused by the fungusBatrachochytrium dendrobatidis(Bd), is the emerging infectious disease implicated in recent population declines and extinctions of amphibian species worldwide.Bdstrains from regions of disease‐associated amphibian decline to date have all belonged to a single, hypervirulent clonal genotype (BdGPL). However, earlier studies in the Atlantic Forest of southeastern Brazil detected a novel, putatively enzootic lineage (Bd‐Brazil), and indicated hybridization betweenBdGPLandBd‐Brazil. Here, we characterize the spatial distribution and population history of these sympatric lineages in the Brazilian Atlantic Forest. To investigate the genetic structure ofBdin this region, we collected and genotypedBdstrains along a 2400‐km transect of the Atlantic Forest.Bd‐Brazil genotypes were restricted to a narrow geographic range in the southern Atlantic Forest, whileBdGPLstrains were widespread and largely geographically unstructured.Bdpopulation genetics in this region support the hypothesis that the recently discovered Brazilian lineage is enzootic in the Atlantic Forest of Brazil and thatBdGPLis a more recently expanded invasive. We collected additional hybrid isolates that demonstrate the recurrence of hybridization between panzootic and enzootic lineages, thereby confirming the existence of a hybrid zone in the Serra da Graciosa mountain range of Paraná State. Our field observations suggest thatBdGPLmay be more infective towards native Brazilian amphibians, and potentially more effective at dispersing across a fragmented landscape. We also provide further evidence of pathogen translocations mediated by the Brazilian ranaculture industry with implications for regulations and policies on global amphibian trade.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Molecular Ecology
Page Range / eLocation ID:
p. 2978-2996
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Species delimitation remains a challenge worldwide, but especially in biodiversity hotspots such as the Amazon. Here, we use an integrative taxonomic approach that combines data from morphology, phylogenomics, and leaf spectroscopy to clarify the species limits within theProtium heptaphyllumspecies complex, which includes subsp.cordatum, subsp.heptaphyllum, and subsp.ulei. Molecular phylogeny indicates that populations of subsp.cordatumdo not belong to theP. heptaphyllumclade, while morphology and near‐infrared spectroscopy data provide additional support for the recognition of a separate taxon.Protium cordatum(Burseraceae) is reinstated at species rank and described in detail. As circumscribed here,P. cordatumis endemic to white‐sand savannas located in the Faro and Tucuruí Districts, Pará State, Brazil, whereasP. heptaphyllumis a dominant and widespread plant lineage found in Amazonia, the Cerrado, and the Brazilian Atlantic Forest. We present an identification key toP. cordatumand closely related lineages and a detailed taxonomic description ofP. cordatum, including habitat and distribution, a list and images of diagnostic features. This study demonstrates the importance of using multiple tools to characterize and distinguish plant species in highly diverse tropical regions.

    more » « less
  2. Abstract

    We present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within thePogonomyrmex barbatusandP. rugosusspecies group. The genetic and geographic relationships within this clade are complex: Four of the identified lineages show genetic caste determination (GCD) and are divided into two pairs. Each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because theirGCDrequires interlineage matings for the production of F1 hybrid workers, and intralineage matings are required to produce queens. ThisGCDsystem maintains genetic isolation among these interdependent lineages, while simultaneously requiring co‐expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these fourGCDlineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrialDNAsequences sampled across most of the morphospecies’ ranges in the U.S.A. and Mexico, we conducted a detailed phylogeographic study. Remarkably, our results indicate that one of theGCDlineage pairs has experienced a dramatic range expansion, despite the genetic load and fitness costs of theGCDsystem. Our analyses also reveal a complex pattern of vicariance and dispersal inPogonomyrmexharvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid‐adapted taxa in North America.

    more » « less
  3. Abstract

    The arrival to theUnitedStates of theAfricanized honey bee, a hybrid betweenEuropean subspecies and theAfrican subspeciesApis mellifera scutellata, is a remarkable model for the study of biological invasions. This immigration has created an opportunity to study the dynamics of secondary contact of honey bee subspecies fromAfrican andEuropean lineages in a feral population inSouthTexas. An 11‐year survey of this population (1991–2001) showed that mitochondrial haplotype frequencies changed drastically over time from a resident population of eastern and western European maternal ancestry, to a population dominated by theAfrican haplotype. A subsequent study of the nuclear genome showed that theAfricanization process included bidirectional gene flow between European and Africanized honey bees, giving rise to a new panmictic mixture ofA. m. scutellata‐and European‐derived genes. In this study, we examined gene flow patterns in the same population 23 years after the first hybridization event occurred. We found 28 active colonies inhabiting 92 tree cavities surveyed in a 5.14 km2area, resulting in a colony density of 5.4 colonies/km2. Of these 28 colonies, 25 were ofA. m. scutellatamaternal ancestry, and three were of western European maternal ancestry. No colonies of eastern European maternal ancestry were detected, although they were present in the earlier samples. NuclearDNArevealed little change in the introgression ofA. m. scutellata‐derived genes into the population compared to previous surveys. Our results suggest this feral population remains an admixed swarm with continued low levels of European ancestry and a greater presence of African‐derived mitochondrial genetic composition.

    more » « less
  4. Abstract Aim

    The “sexy shrimp”Thor amboinensisis currently considered a single circumtropical species. However, the tropical oceans are partitioned by hard and soft barriers to dispersal, providing ample opportunity for allopatric speciation. Herein, we test the null hypothesis thatT. amboinensisis a single global species, reconstruct its global biogeographical history, and comment on population‐level patterns throughout the Tropical Western Atlantic.


    Coral reefs in all tropical oceans.


    Specimens ofThor amboinensiswere obtained through field collection and museum holdings. We used one mitochondrial (COI) and two nuclear (NaK, enolase) gene fragments for global species delimitation and phylogenetic analyses (n = 83 individuals, 30 sample localities), while phylogeographical reconstruction in theTWAwas based onCOIonly (n = 303 individuals, 10 sample localities).


    We found evidence for at least five cryptic lineages (9%–22%COIpairwise sequence divergence): four in the Indo‐West Pacific and one in the Tropical Western Atlantic. Phylogenetic reconstruction revealed that endemic lineages from Japan and the South Central Pacific are more closely related to the Tropical Western Atlantic lineage than to a co‐occurring lineage that is widespread throughout the Indo‐West Pacific. Concatenated and species tree phylogenetic analyses differ in the placement of an endemic Red Sea lineage and suggest alternate dispersal pathways into the Atlantic. Phylogeographical reconstruction throughout the Tropical Western Atlantic reveals little genetic structure over more than 3,000 km.

    Main conclusions

    Thor amboinensisis a species complex that has undergone a series of allopatric speciation events and whose members are in secondary contact in the Indo‐West Pacific. Nuclear‐ and mitochondrial‐ gene phylogenies show evidence of introgression between lineages inferred to have been separated more than 20 Ma. Phylogenetic discordance between multi‐locus analyses suggest thatT. amboinensisoriginated in the Tethys sea and dispersed into the Atlantic and Indo‐West Pacific through the Tethys seaway or, alternatively, originated in the Indo‐West Pacific and dispersed into the Atlantic around South Africa. Population‐level patterns in the Caribbean indicate extensive gene flow across the region.

    more » « less
  5. Abstract

    Phenotypes are the target of selection and affect the ability of organisms to persist in variable environments. Phenotypes can be influenced directly by genes and/or by phenotypic plasticity. The amphibian‐killing fungusBatrachochytrium dendrobatidis(Bd) has a global distribution, unusually broad host range, and high genetic diversity. Phenotypic plasticity may be an important process that allows this pathogen to infect hundreds of species in diverse environments. We quantified phenotypic variation of nine Bd genotypes from two Bd lineages (Global Pandemic Lineage [GPL] and Brazil) and a hybrid (GPL‐Brazil) grown at three temperatures (12, 18 and 24°C). We measured five functional traits including two morphological traits (zoospore and zoosporangium sizes) and three life history traits (carrying capacity, time to fastest growth and exponential growth rate) in a phylogenetic framework. Temperature caused highly plastic responses within each genotype, with all Bd genotypes showing phenotypic plasticity in at least three traits. Among genotypes, Bd generally showed the same direction of plastic response to temperature: larger zoosporangia, higher carrying capacity, longer time to fastest growth and slower exponential growth at lower temperatures. The exception was zoospore size, which was highly variable. Our findings indicate that Bd genotypes have evolved novel phenotypes through plastic responses to temperature over very short timescales. High phenotypic variability likely extends to other traits and may facilitate the large host range and rapid spread of Bd.

    more » « less