Nicholas M. Fountain-Jones

Moving beyond the guild concept: developing a practical functional trait framework for terrestrial beetles

1. New logical and analytical frameworks for studying functional traits have led to major advances in plant and freshwater ecology at local and global scales. The ecological and taxonomic diversity of terrestrial adult beetles (Coleoptera) means that functional trait approaches should have considerable power to illuminate the function not only of these animals but also of the ecosystems in which they occur.

Living near the edge: Being close to mature forest increases the rate of succession in beetle communities

In increasingly fragmented landscapes, it is important to understand how mature forest affects adjacent secondary forest (forest influence). Forest influence on ecological succession of beetle communities is largely unknown. We investigated succession and forest influence using 235 m long transects across boundaries between mature and secondary forest at 15 sites, sampling a chronosequence of three forest age classes (5-10, 23- 29, and 42-46 years since clear-cutting) in tall eucalypt forest in Tasmania, Australia. Our results showed that ground-dwelling beetle communities showed strong successional changes, and in the oldest secondary forests, species considered indicators of mature forest had recolonized to abundance levels similar to those observed within adjacent mature forest stands. However, species composition also showed forest influence gradients in all age classes. Forest influence was estimated to extend 13 m and 20 m in the youngest and intermediate-aged secondary forests, respectively. However, the estimated effect extended to at least 176 m in the oldest secondary forest. Our environmental modeling suggests that leaf litter, microclimate, and soil variables were all important in explaining the spatial variation in beetle assemblages, and the relative importance of factors varied between secondary forest age classes. Mature-forest beetle communities can recolonize successfully from the edge, and our results provide a basis for land managers to build mature habitat connectivity into forest mosaics typical of production forests. Our results also indicate the importance of forest influence in determining potential conservation value of older secondary forest for beetles.

Urban Landscapes can change virus gene flow and evolution in a fragmentation-sensitive carnivore

Urban expansion has widespread impacts on wildlife species globally, including the transmission and emergence of infectious diseases. However, there is almost no information about how urban landscapes shape transmission dynamics in wildlife. Using an innovative phylodynamic approach combining host and pathogen molecular data with landscape characteristics and host traits, we untangle the complex factors that drive transmission networks of feline immunodeficiency virus (FIV) in bobcats (Lynx rufus). We found that the urban landscape played a significant role in shaping FIV transmission. Even though bobcats were often trapped within the urban matrix, FIV transmission events were more likely to occur in areas with more natural habitat elements. Urban fragmentation also resulted in lower rates of pathogen evolution, possibly owing to a narrower range of host genotypes in the fragmented area. Combined, our findings show that urban landscapes can have impacts on a pathogen and its evolution in a carnivore living in one of the most fragmented and urban systems in North America. The analytical approach used here can be broadly applied to other host–pathogen systems, including humans.

Mitochondrial genome sequencing reveals potential origins of the scabies mite Sarcoptes scabiei infesting two iconic Australian marsupials

BackgroundDebilitating skin infestations caused by the mite, Sarcoptes scabiei, have a profound impact on human and animal health globally. In Australia, this impact is evident across different segments of Australian society, with a growing recognition that it can contribute to rapid declines of native Australian marsupials. Cross-host transmission has been suggested to play a significant role in the epidemiology and origin of mite infestations in different species but a chronic lack of genetic resources has made further inferences difficult. To investigate the origins and molecular epidemiology of S. scabiei in Australian wildlife, we sequenced the mitochondrial genomes of S. scabiei from diseased wombats (Vombatus ursinus) and koalas (Phascolarctos cinereus) spanning New South Wales, Victoria and Tasmania, and compared them with the recently sequenced mitochondrial genome sequences of S. scabiei from humans.ResultsWe found unique S. scabiei haplotypes among individual wombat and koala hosts with high sequence similarity (99.1% - 100%). Phylogenetic analysis of near full-length mitochondrial genomes revealed three clades of S. scabiei (one human and two marsupial), with no apparent geographic or host species pattern, suggestive of multiple introductions. The availability of additional mitochondrial gene sequences also enabled a re-evaluation of a range of putative molecular markers of S. scabiei, revealing that cox1 is the most informative gene for molecular epidemiological investigations. Utilising this gene target, we provide additional evidence to support cross-host transmission between different animal hosts.ConclusionsOur results suggest a history of parasite invasion through colonisation of Australia from hosts across the globe and the potential for cross-host transmission being a common feature of the epidemiology of this neglected pathogen. If this is the case, comparable patterns may exist elsewhere in the ‘New World’. This work provides a basis for expanded molecular studies into mange epidemiology in humans and animals in Australia and other geographic regions.

Linking social and spatial networks to viral community phylogenetics reveals subtype-specific transmission dynamics in African lions

Heterogeneity within pathogen species can have important consequences for how pathogens transmit across landscapes; however, discerning different transmission routes is challenging. Here, we apply both phylodynamic and phylogenetic community ecology techniques to examine the consequences of pathogen heterogeneity on transmission by assessing subtype-specific transmission pathways in a social carnivore. We use comprehensive social and spatial network data to examine transmission pathways for three subtypes of feline immunodeficiency virus (FIVPle ) in African lions (Panthera leo) at multiple scales in the Serengeti National Park, Tanzania. We used FIVPle molecular data to examine the role of social organization and lion density in shaping transmission pathways and tested to what extent vertical (i.e., father- and/or mother-offspring relationships) or horizontal (between unrelated individuals) transmission underpinned these patterns for each subtype. Using the same data, we constructed subtype-specific FIVPle co-occurrence networks and assessed what combination of social networks, spatial networks or co-infection best structured the FIVPle network. While social organization (i.e., pride) was an important component of FIVPle transmission pathways at all scales, we find that FIVPle subtypes exhibited different transmission pathways at within- and between-pride scales. A combination of social and spatial networks, coupled with consideration of subtype co-infection, was likely to be important for FIVPle transmission for the two major subtypes, but the relative contribution of each factor was strongly subtype-specific. Our study provides evidence that pathogen heterogeneity is important in understanding pathogen transmission, which could have consequences for how endemic pathogens are managed. Furthermore, we demonstrate that community phylogenetic ecology coupled with phylodynamic techniques can reveal insights into the differential evolutionary pressures acting on virus subtypes, which can manifest into landscape-level effects.

Spatiotemporal evolutionary epidemiology of H5N1 highly pathogenic avian influenza in West Africa and Nigeria, 2006–2015

H5N1 highly pathogenic avian influenza virus (HPAIV) was first observed in Nigeria in early 2006 and has now spread to more than 17 African countries having severe economic and public health implications. Here, we explore the spatiotemporal patterns of viral dispersal both among West African countries and within Nigeria using sequence data from hemagglutinin (HA) gene region of the virus. Analyses were performed within a statistical Bayesian framework using phylodynamic models on data sets comprising of all publically available HA sequence data collected from seven West African countries and Egypt between 2006 and 2015. Our regional-level analyses indicated that H5N1 in West Africa originated in Nigeria in three geopolitical regions, specifically north central and north-east, where backyard poultry and wild birds are in frequent contact, as well as south-west, a major commercial poultry area, then dispersed to West African countries. We inferred significant virus dispersal routes between Niger and Nigeria on one side and Burkina Faso, Ivory Coast, Ghana and Egypt on the other. Furthermore, south-west Nigeria identified as a primary source for virus dispersal within Nigeria as well as to Niger in 2006 and 2008. Niger was an important epicentre for the virus spread into other West African countries in 2015. Egyptian introductions from West Africa were sporadic and resulted most likely from poultry trade with Nigeria rather than contact with infected wild birds. Our inferred viral dispersal routes reflected the large-scale unrestricted movements of infected poultry in the region. Our study illustrates the ability of phylodynamic models to trace important HPAIV dispersal routes at a regional and national level. Our results have clear implications for the control and prevention of this pathogen across scales and will help improve molecular surveillance of transboundary HPAIVs.

Towards an eco-phylogenetic framework for infectious disease ecology

Identifying patterns and drivers of infectious disease dynamics across multiple scales is a fundamental challenge for modern science. There is growing awareness that it is necessary to incorporate multi‐host and/or multi‐parasite interactions to understand and predict current and future disease threats better, and new tools are needed to help address this task. Eco‐phylogenetics (phylogenetic community ecology) provides one avenue for exploring multi‐host multi‐parasite systems, yet the incorporation of eco‐phylogenetic concepts and methods into studies of host pathogen dynamics has lagged behind. Eco‐phylogenetics is a transformative approach that uses evolutionary history to infer present‐day dynamics. Here, we present an eco‐phylogenetic framework to reveal insights into parasite communities and infectious disease dynamics across spatial and temporal scales. We illustrate how eco‐phylogenetic methods can help untangle the mechanisms of host–parasite dynamics from individual (e.g. co‐infection) to landscape scales (e.g. parasite/host community structure). An improved ecological understanding of multi‐host and multi‐pathogen dynamics across scales will increase our ability to predict disease threats.

Trophic position determines functional and phylogenetic recovery after disturbance within a community

Summary 1.The roles that functional traits and/or evolutionary history of species from co-occuring trophic groups have in determining community recovery following disturbance are poorly understood. Functional traits help determine how species interact with their environment, thus functional traits are likely to change with time since logging. However, traits of species may also be phylogenetically constrained depending on their evolutionary history. Because beetles are trophically diverse, the effects of phylogenetic and functional aspects of community recovery can be compared between co-occuring trophic groups. 2.Using a chronosequence of forest ages following logging, we applied a novel combination of functional trait and phylogenetic approaches to assess the extent to which taxonomic, functional and phylogenetic composition recovered after logging, and if these dimensions of composition approached those characteristic of mature forests, for both predators and decomposers/primary consumers. We also examined to what extent functional traits of both trophic groups were phylogenetically conserved. 3.Predator functional compostion had recovered ~45 years after logging, and this recovery preceded taxonomic recovery. Neither taxonomic nor functional composition had recovered for the decomposer/primary consumer communites by this time. 4.In contrast to decomposers/primary consumers, predator community recovery had no distinct phylogenetic signature, yet predator functional traits were more phylogenetically conserved than decomposers/primary consumer functional traits. 5.Trait syndromes that characterise forest recovery stages are identified and provide a basis for future work on community re-assembly following disturbance. 6.We demonstrate differential recovery of co-occuring beetle trophic groups following disturbance. We show that functional and phylogenetic composition may be disconnected from taxonomic composition; highlighting the advantages of integrating understanding of these three potentially independent components of ecological diversity to enable deeper understanding of animal community composition. This article is protected by copyright. All rights reserved.

Chronic infections can shape epidemic exposure: Pathogen co-occurrence networks in the Serengeti lions

Pathogens are embedded in a complex network of microparasites that can collectively or individually alter disease dynamics and outcomes. Chronic pathogens, for example, can either facilitate or compete with subsequent pathogens thereby exacerbating morbidity and mortality. Pathogen interactions are ubiquitous in nature, but poorly understood, particularly in wild populations. We report here on ten years of serological and molecular data in African lions, leveraging comprehensive demographic and behavioral data to utilize pathogen networks to test if chronic infections shape infection by acute pathogens. We combine network and community ecology approaches to assess broad network structure and characterize associations between pathogens across spatial and temporal scales. We found significant non-random structure in the lion-pathogen co-occurrence network and identified potential facilitative and competitive interactions between acute and chronic pathogens. Our results provide a novel insight for untangling the complex associations underlying pathogen co-occurrence networks.

Pathogens in space: Advancing understanding of pathogen dynamics and disease ecology through landscape genetics

Landscape genetics has provided many insights into how heterogeneous landscape features drive processes influencing spatial genetic variation in free‐living organisms. This rapidly developing field has focused heavily on vertebrates, and expansion of this scope to the study of infectious diseases holds great potential for landscape geneticists and disease ecologists alike. The potential application of landscape genetics to infectious agents has garnered attention at formative stages in the development of landscape genetics, but systematic examination is lacking. We comprehensively review how landscape genetics is being used to better understand pathogen dynamics. We characterize the field and evaluate the types of questions addressed, approaches used and systems studied. We also review the now established landscape genetic methods and their realized and potential applications to disease ecology. Lastly, we identify emerging frontiers in the landscape genetic study of infectious agents, including recent phylogeographic approaches and frameworks for studying complex multihost and host‐vector systems. Our review emphasizes the expanding utility of landscape genetic methods available for elucidating key pathogen dynamics (particularly transmission and spread) and also how landscape genetic studies of pathogens can provide insight into host population dynamics. Through this review, we convey how increasing awareness of the complementarity of landscape genetics and disease ecology among practitioners of each field promises to drive important cross‐disciplinary advances.