Globalized infectious diseases are causing species declines worldwide, but their source often remains elusive. We used whole-genome sequencing to solve the spatiotemporal origins of the most devastating panzootic to date, caused by the fungus Batrachochytrium dendrobatidis, a proximate driver of global amphibian declines. We traced the source of B. dendrobatidis to the Korean peninsula, where one lineage, BdASIA-1, exhibits the genetic hallmarks of an ancestral population that seeded the panzootic. We date the emergence of this pathogen to the early 20th century, coinciding with the global expansion of commercial trade in amphibians, and we show that intercontinental transmission is ongoing. Our findings point to East Asia as a geographic hotspot for B. dendrobatidis biodiversity and the original source of these lineages that now parasitize amphibians worldwide.
B iodiversity and the many ecosystem functions and services it underpins are undergoing significant and often rapid changes worldwide 1. A range of global initiatives and policy frameworks, including the Convention on Biological Diversity (CBD) and Sustainable Development Goals (SDGs), have aimed to reduce this change and to halt the loss of biodiversity, with limited progress to date 2. Appropriately gauging the impact of such policies or the progress toward international biodiversity goals has a key requirement: the availability of information on the status and trends of biodiversity in a form that is easily understood, timely, scientifically rigorous, standardized, relevant, global and representative of species populations across taxa and regions over time. Such information is particularly crucial in assessments, such as those carried out by the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) 3 , and is needed to construct 'indicators' , which are aggregate measures that often address specific conservation targets 4,5. Underpinning such metrics are core, essential measurements known as EBVs, which capture key constituent components of biodiversity change 6,7 , akin and complementary to the 'essential climate variables' supporting climate change assessment and policy 8. Facilitated by the Group on Earth Observations Biodiversity Observation Network (GEO BON, http://geobon.org) and related efforts, the biodiversity science and observation community is now engaging in an effort to conceptualize and formulate these essential biodiversity components to enable more focused, integrated, and effective biodiversity monitoring in support of assessment and policy within a unified framework. This study represents the formal outcome of a process undertaken from 2015 through 2018 by the founding members of the GEO BON Species Populations Working Group 9 , which includes the authors of this Perspective, charged with providing the formal definitions, conceptualizations and recommendations addressing species distribution and abundance EBVs. Changes in species distribution and abundance affect all biodiversity facets 10 , including the loss of potentially significant traits and functions 1,11 and associated ecosystem consequences 12,13. Patterns of spatial distribution and changes to these patterns inform us about the commonness, rarity and potential extinction risk for species 14-16 , determine the national and regional stewardship of species and are key to ensuring effective monitoring 17 , protection 18,19 and population
Much biodiversity data is collected worldwide, but it remains challenging to assemble the scattered knowledge for assessing biodiversity status and trends. The concept of Essential Biodiversity Variables (EBVs) was introduced to structure biodiversity monitoring globally, and to harmonize and standardize biodiversity data from disparate sources to capture a minimum set of critical variables required to study, report and manage biodiversity change. Here, we assess the challenges of a 'Big Data' approach to building global EBV data products across taxa and spatiotemporal scales, focusing on species distribution and abundance. The majority of currently available data on species distributions derives from incidentally reported observations or from surveys where presence-only or presence-absence data are sampled repeatedly with standardized protocols. Most abundance data come from opportunistic population counts or from population time series using standardized protocols (e.g. repeated surveys of the same population from single or multiple sites). Enormous complexity exists in integrating these heterogeneous, multi-source data sets across space, time, taxa and different sampling methods. Integration of such data into global EBV data products requires correcting biases introduced by imperfect detection and varying sampling effort, dealing with different spatial resolution and extents, harmonizing measurement units from different data sources or sampling methods, applying statistical tools and models for spatial inter-or extrapolation, and quantifying sources of uncertainty and errors in data and models. To support the development of EBVs by the Group on Earth Observations Biodiversity Observation Network (GEO BON), we identify 11 key workflow steps that will operationalize the process of building EBV data products within and across research infrastructures worldwide. These workflow steps take multiple sequential activities into account, including identification and aggregation of various raw data sources, data quality control, taxonomic name matching and statistical modelling of integrated data. We illustrate these steps with concrete examples from existing citizen science and professional monitoring projects, including eBird, the Tropical Ecology Assessment and Monitoring network, the Living Planet Index and the Baltic Sea zooplankton monitoring. The identified workflow steps are applicable to both terrestrial and aquatic systems and a broad range of spatial, temporal and taxonomic scales. They depend on clear, findable and accessible metadata, and we provide an overview of current data and metadata standards. Several challenges remain to be solved for building global EBV data products: (i) developing tools and models for combining heterogeneous, multi-source data sets and filling data gaps in geographic, temporal and taxonomic coverage, (ii) integrating emerging methods and technologies for data collection such as citizen science, sensor networks, DNA-based techniques and satellite remote sensing, (iii) solv...
Without robust and unbiased systems for monitoring, changes in natural systems will remain enigmatic for policy makers, leaving them without a clear idea of the consequences of any environmental policies they might adopt. Generally, biodiversity-monitoring activities are not integrated or evaluated across any large geographic region. The EuMon project conducted the first large-scale evaluation of monitoring practices in Europe through an on-line questionnaire and is reporting on the results of this survey. In September 2007 the EuMon project had documented 395 monitoring schemes for species, which represents a total annual cost of about 4 million euro, involving more than 46,000 persons devoting over 148,000 person-days/year to biodiversity-monitoring activities. Here we focused on the analysis of variations of monitoring practices across a set of taxonomic groups (birds, amphibians and reptiles, mammals, butterflies, plants, and other insects) and across 5 European countries (France, Germany, Hungary, Lithuania, and Poland). Our results suggest that the overall sampling effort of a scheme is linked with the proportion of volunteers involved in that scheme. Because precision is a function of the number of monitored sites and the number of sites is maximized by volunteer involvement, our results do not support the common belief that volunteer-based schemes are too noisy to be informative. Just the opposite, we believe volunteer-based schemes provide relatively reliable data, with state-of-the-art survey designs or data-analysis methods, and consequently can yield unbiased results. Quality of data collected by volunteers is more likely determined by survey design, analytical methodology, and communication skills within the schemes rather than by volunteer involvement per se.
Although satellite-based variables have for long been expected to be key components to a unified and global biodiversity monitoring strategy, a definitive and agreed list of these variables still remains elusive. The growth of interest in biodiversity variables observable from space has been partly underpinned by the development of the essential biodiversity variable (EBV) framework by the Group on Earth Observations -Biodiversity Observation Network, which itself was guided by the process of identifying essential climate variables. This contribution aims to advance the development of a global biodiversity monitoring strategy by updating the previously published definition of EBV, providing a definition of satellite remote sensing (SRS) EBVs and introducing a set of principles that are believed to be necessary if ecologists and space agencies are to agree on a list of EBVs that can be routinely monitored from space. Progress toward the identification of SRS-EBVs will require a clear understanding of what makes a biodiversity variable essential, as well as agreement on who the users of the SRS-EBVs are. Technological and algorithmic developments are rapidly expanding the set of opportunities for SRS in monitoring biodiversity, and so the list of SRS-EBVs is likely to evolve over time. This means that a clear and common platform for data providers, ecologists, environmental managers, policy makers and remote sensing experts to interact and share ideas needs to be identified to support long-term coordinated actions.
Dispersal is central in ecology and evolution because it influences population regulation, adaptation, and speciation. In many species, dispersal is different between genders, leading to sex-biased dispersal. Several theoretical hypotheses have been proposed to explain the evolution of this bias: the resource competition hypothesis proposed by Greenwood, the local mate competition hypothesis, and the inbreeding avoidance hypothesis. Those hypotheses argued that the mating system should be the major factor explaining the direction of such bias. Sociality and the presence of handicap in genders (exaggerated sexual characters or parental care) have recently been proposed to be linked with the direction of this bias. We tested these expected coevolutions using a database of 257 species. Based on phylogenetic approaches, our findings marginally corroborated Greenwood’s hypothesis by showing relationships between the direction of sex-biased dispersal, mating systems, and territoriality. More importantly, our results highlighted that the evolution of this bias was more linked to parental care and sexual dimorphism. These traits were also found to be associated with mating systems, suggesting that sexual asymmetry in morphology and parental care might be the main determinant of the evolution of sex-biased dispersal across species and not mating systems per se, as proposed in Greenwood’s hypothesis.
Amphibian chytridiomycosis is a disease caused by the fungus Batrachochytrium dendrobatidis (Bd). Whether Bd is a new emerging pathogen (the novel pathogen hypothesis; NPH) or whether environmental changes are exacerbating the host-pathogen dynamic (the endemic pathogen hypothesis; EPH) is debated. To disentangle these hypotheses we map the distribution of Bd and chytridiomycosis across the Iberian Peninsula centred on the first European outbreak site. We find that the infection-free state is the norm across both sample sites and individuals. To analyse this dataset, we use Bayesian zero-inflated binomial models to test whether environmental variables can account for heterogeneity in both the presence and prevalence of Bd, and heterogeneity in the occurrence of the disease, chytridiomycosis. We also search for signatures of Bd-spread within Iberia using genotyping. We show (1) no evidence for any relationship between the presence of Bd and environmental variables, (2) a weak relationship between environmental variables and the conditional prevalence of infection, (3) stage-dependent heterogeneity in the infection risk, (4) a strong association between altitude and chytridiomycosis, (5) multiple Iberian genotypes and (6) recent introduction and spread of a single genotype of Bd in the Pyrenees. We conclude that the NPH is consistent with the emergence of Bd in Iberia. However, epizootic forcing of infection is tied to location and shaped by both biotic and abiotic variables. Therefore, the population-level consequences of disease introduction are explained by EPH-like processes. This study demonstrates the power of combining surveillance and molecular data to ascertain the drivers of new emerging infections diseases.
In general, amphibians are known to exhibit a higher degree of population subdivision than any other major animal taxa, but large-scale population genetic surveys of widely distributed species are still scarce, especially in the Eurasian continent. Using microsatellite markers and mitochondrial DNA sequences, we investigated the large-scale population genetic structure of the common frog (Rana temporaria)--one of the most widespread amphibians of the Palearctic region. Analyses of cytochrome b sequences revealed evidence for two distinct lineages inhabiting western and eastern parts of Europe. The separation of these lineages c. 700,000 years ago may have been induced by the onset of the Middle Pleistocene continental glaciations. Analyses of the variability of microsatellite loci within each of the clades revealed evidence for evolution of a high degree of population subdivision (FST approximately 0.23) even in northern Fennoscandia, colonized less than 10,000 years ago. The high level of substructuring is puzzling in the face of an apparently high dispersal capacity, as evidenced by the rather rapid recolonization of northern Europe. This suggests that processes other than restricted dispersal capacity need to be explored as explanations for the high degree of population subdivision in amphibians. The colonization of northern Europe has been accompanied by loss of genetic variability as evidenced by decreasing levels of intrapopulational genetic variability in microsatellite loci from south to north across Europe.
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