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Understanding the evolutionary history of microbial pathogens is critical for mitigating the impacts of emerging infectious diseases on economically and ecologically important host species. We used a genome resequencing approach to resolve the evolutionary history of an important microbial pathogen, the chytrid Batrachochytrium dendrobatidis (Bd), which has been implicated in amphibian declines worldwide. We sequenced the genomes of 29 isolates of Bd from around the world, with an emphasis on North, Central, and South America because of the devastating effect that Bd has had on amphibian populations in the New World. We found a substantial amount of evolutionary complexity in Bd with deep phylogenetic diversity that predates observed global amphibian declines. By investigating the entire genome, we found that even the most recently evolved Bd clade (termed the global panzootic lineage) contained more genetic variation than previously reported. We also found dramatic differences among isolates and among genomic regions in chromosomal copy number and patterns of heterozygosity, suggesting complex and heterogeneous genome dynamics. Finally, we report evidence for selection acting on the Bd genome, supporting the hypothesis that protease genes are important in evolutionary transitions in this group. Bd is considered an emerging pathogen because of its recent effects on amphibians, but our data indicate that it has a complex evolutionary history that predates recent disease outbreaks. Therefore, it is important to consider the contemporary effects of Bd in a broader evolutionary context and identify specific mechanisms that may have led to shifts in virulence in this system.

In species-rich assemblages of acoustically communicating animals, heterospecific sounds may constrain not only the evolution of signal traits but also the much less-studied signal-processing mechanisms that define the recognition space of a signal. To test the hypothesis that the recognition space is optimally designed, i.e., that it is narrower toward the species that represent the higher potential for acoustic interference, we studied an acoustic assemblage of 10 diurnally active frog species. We characterized their calls, estimated pairwise correlations in calling activity, and, to model the recognition spaces of five species, conducted playback experiments with 577 synthetic signals on 531 males. Acoustic cooccurrence was not related to multivariate distance in call parameters, suggesting a minor role for spectral or temporal segregation among species uttering similar calls. In most cases, the recognition space overlapped but was greater than the signal space, indicating that signal-processing traits do not act as strictly matched filters against sounds other than homospecif ic calls. Indeed, the range of the recognition space was strongly predicted by the acoustic distance to neighboring species in the signal space. Thus, our data provide compelling evidence of a role of heterospecific calls in evolutionarily shaping the frogs' recognition space within a complex acoustic assemblage without obvious concomitant effects on the signal.

The amphibian chytrid fungus, Batrachochytrium dendrobatidis , Bd , has been implicated in the decimation and extinction of many amphibian populations worldwide, especially at mid and high elevations. Recent studies have demonstrated the presence of the pathogen in the lowlands from Australia and Central America. We extend here its elevational range by demonstrating its presence at the sea level, in the lowland forests of Gorgona Island, off the Pacific coast of Colombia. We conducted two field surveys, separated by four years, and diagnosed Bd by performing polymerase chain reactions on swab samples from the skin of five amphibian species. All species, including the Critically Endangered Atelopus elegans , tested positive for the pathogen, with prevalences between 3.9 % in A. elegans (in 2010) and 52 % in Pristimantis achatinus . Clinical signs of chytridiomycosis were not detected in any species. To our knowledge, this is the first report of B. dendrobatidis in tropical lowlands at sea level, where temperatures may exceed optimal growth temperatures of this pathogen. This finding highlights the need to understand the mechanisms allowing the interaction between frogs and pathogen in lowland ecosystems.

Microbial symbionts are increasingly recognized as playing a critical role in organismal health across a wide range of hosts. Amphibians are unique hosts in that their skin helps to regulate the exchange of water, ions, and gases, and it plays an active role in defense against pathogens through the synthesis of anti-microbial peptides. The microbiome of amphibian skin includes a diverse community of bacteria known to defend against pathogens, including the global pandemic lineage of Batrachochytrium dendrobatidis associated with mass amphibian die-offs. The relative influence of host phylogeny and environment in determining the composition of the amphibian skin microbiome remains poorly understood. We collected skin swabs from montane amphibians in Mexico and Guatemala, focusing on two genera of plethodontid salamanders and one genus of frogs. We used high throughput sequencing to characterize the skin bacterial microbiome and tested the impact of phylogeny and habitat on bacterial diversity. Our results show that phylogenetic history strongly influences the diversity and community structure of the total bacterial microbiome at higher taxonomic levels (between orders), but on lower scales (within genera and species), the effect of habitat predominates. These results add to a growing consensus that habitat exerts a strong effect on microbiome structure and composition, particularly at shallow phylogenetic scales.

While the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) is driving catastrophic biodiversity loss worldwide, some amphibian communities persist seemingly unaffected despite occurring in climates conducive to pathogen establishment. These amphibian communities may remain epidemiologically naive. As mitigation of Bd is rarely successful after establishment, identifying remaining Bd-free refuges is imperative. Presently, the only known large-scale Bd-free refuge is the island of New Guinea (NG), safeguarding Australasias amphibian phylogenetic diversity otherwise devastated by Bd. Following extensive multi-year disease surveillance, we here uncover a second large-scale Bd-free refuge in the Sierra Nevada de Santa Marta (SNSM), a Neotropical biodiversity hotspot in northern Colombia. We detected no evidence of Bd in SNSM-wide screening, while we uncovered the presence of hypervirulent Bd-GPL in adjacent areas of the tropical Andes. Population genomic analyses in an SNSM-endemic anuran found no evidence for demographic bottlenecks indicative of cryptic epizootic decline. Niche modelling highlights the high risk for Bd establishment and Bd-induced declines in both the SNSM and NG, and the important role of lowland environmental barriers in restricting Bd invasion. Infection trials using three SNSM-endemic amphibians reveal varying disease susceptibility. Together, these data identify the SNSM as an epidemiologically naive refuge likely facing imminent Bd invasion, which could result in the loss of at least 25 endemic amphibian species. We highlight the urgent need for proactive conservation action and strict implementation of biosecurity to safeguard the unique and vast amphibian diversity of the world's last major Bd-free refuges.Competing Interest StatementThe authors have declared no competing interest.Funder Information DeclaredUniversität Trier, https://ror.org/02778hg05, ForschungsfondsResearch Foundation Flanders (FWO), 1104226NGerman Society of Herpetology DGHT, Wilhelm-Peters-FondsNational Geographic Society, NGS-66509C-20