Population Structure and Evolutionary Ecology of Batrachochytrium dendrobatidis in the Brazilian Atlantic Forest

Abstract

The pathogen Batrachochytrium dendrobatidis (Bd), also known as the amphibian-killing chytrid fungus, causes the emerging disease implicated in recent population declines and extinctions of frog species worldwide. By taking advantage of unique Bd genetic diversity in the Brazilian Atlantic Forest this dissertation seeks to better understand the pathogen population history of the region, and to learn what ecological processes shape current – and future – distributions of this ecologically consequential pathogen. Data from prior infection studies show that the global Bd pandemic is caused by a single clonal genotype that is hypervirulent to amphibian hosts. In 2012, however, novel, divergent strains were reported from the Atlantic Forest region of southern Brazil. To investigate the distribution and population structure of this novel lineage, pure isolates of pathogen strains were collected from Bd infected anurans along a 2400 Km transect of the historical range of the Atlantic rainforest over three field seasons, The population genetic structure suggested the presence of a long-term endemic Brazilian lineage, and a recently introduced, invasive lineage, with an active hybrid zone that has formed in the southern Atlantic Forest where the two lineages come into contact. The discovery of the Brazilian hybrid zone is significant because Bd was once thought to be a strictly asexual pathogen, and the only known cases of hybridization in this species are restricted to this narrow zone on the Atlantic coast of Brazil. Natural hybrids present a valuable opportunity to understand the genetic basis of lineage divergence, and the first steps toward speciation. To understand the genetic differentiation between the divergent parental lineages, Illumina whole-genome sequences were obtained for 51 Brazilian Atlantic Forest strains of Bd ¬– including three hybrids and representatives of both parental populations. Loci with unequally inherited alleles occurred in clustered blocks throughout the hybrid genomes. Gene ontology analyses showed that these divergent loci were enriched for genes responding to oxidative stress, suggesting a potential mechanism underlying the ecological diversification between Bd lineages. To investigate the competitive differences between Bd lineages, I assessed the competitive performance of Bd-Brazil against Bd-GPL in-vivo using a model amphibian host (Hymenochirus curtipes). Competition trials were performed using four different pairwise combinations of Bd-GPL and Bd-Brazil strains. The dominant strains at regular time points throughout the experiment were assessed by digital PCR using strain specific fluorescent probes. Competitive effects are observed between lineages, with Bd-GPL as the superior competitor, especially at the earlier stages of infection.