Richard J. Hall

Explaining the explosion: modelling hybrid invasions

The emergence of hybrids between native and introduced species is an increasingly widespread problem which can alter entire ecosystems. We present a general model for the hybridization of two plant species to investigate the conditions under which hybrid invasions can occur, and the ecological and genetic consequences of such hybridizations. We find that parental compatibility and fecundity are important determinants of whether (and at what rate) hybrid genotypes emerge. Enhanced hybrid fitness traits affect both the populations genetic structure and total rate of increase, with rapid selection for the fittest genotype. Conversely, if different genotypes maximize different life-history characteristics, the ensuing population can be genetically very variable. The model provides a novel approach to evaluate the contributions of population dynamic and genetic processes in the study of hybrid invasions.

MinION nanopore sequencing of an influenza genome

Influenza epidemics and pandemics have significant impacts on economies, morbidity and mortality worldwide. The ability to rapidly and accurately sequence influenza viruses is instrumental in the prevention and mitigation of influenza. All eight influenza genes from an influenza A virus were amplified by PCR simultaneously and then subjected to sequencing on a MinION nanopore sequencer. A complete influenza virus genome was obtained that shared greater than 99% identity with sequence data obtained from Illumina MiSeq and traditional Sanger-sequencing. The laboratory infrastructure and computing resources used to perform this experiment on the MinION nanopore sequencer would be available in most molecular laboratories around the world. Using this system, the concept of portability, and thus sequencing influenza viruses in the clinic or field is now tenable.

Too much of a good thing: resource provisioning alters infectious disease dynamics in wildlife.

Provisioning of abundant food resources in human-altered landscapes can have profound effects on wildlife ecology, with important implications for pathogen transmission. While empirical studies have quantified the effects of provisioning on host behaviour and immunology, the net interactive effect of these components on host–pathogen dynamics is unknown. We use simple compartmental models to investigate how provisioning-induced changes to host demography, contact behaviour and immune defence influence pathogen invasion and persistence. We show that pathogen invasion success and equilibrium prevalence depend critically on how provisioning affects host immune defence and that moderate levels of provisioning can lead to drastically different outcomes of pathogen extinction or maximizing prevalence. These results highlight the need for further empirical studies to fully understand how provisioning affects pathogen transmission in urbanized environments.

Greater migratory propensity in hosts lowers pathogen transmission and impacts.

Animal migrations are spectacular and migratory species have been shown to transmit pathogens that pose risks to human health. Although migration is commonly assumed to enhance pathogen dispersal, empirical work indicates that migration can often have the opposite effect of lowering disease risk. Key to assessing disease threats to migratory species is the ability to predict how migratory behaviour influences pathogen invasion success and impacts on migratory hosts, thus motivating a mechanistic understanding of migratory host-pathogen interactions. Here, we develop a quantitative framework to examine pathogen transmission in animals that undergo two-way directed migrations between wintering and breeding grounds annually. Using the case of a pathogen transmitted during the hosts breeding season, we show that a more extreme migratory strategy (defined by the time spent away from the breeding site and the total distance migrated) lowers the probability of pathogen invasion. Moreover, if migration substantially lowers the survival probability of infected animals, then populations that spend comparatively less time at the breeding site or that migrate longer distances are less vulnerable to pathogen-induced population declines. These findings provide theoretical support for two non-exclusive mechanisms proposed to explain how seasonal migration can lower infection risk: (i) escape from habitats where parasite transmission stages have accumulated and (ii) selective removal of infected hosts during strenuous journeys. Our work further suggests that barriers to long-distance movement could increase pathogen prevalence for vulnerable species, an effect already seen in some animal species undergoing anthropogenically induced migratory shifts.

Metagenomic Analysis of Viruses in Feces from Unsolved Outbreaks of Gastroenteritis in Humans

ABSTRACT The etiology of an outbreak of gastroenteritis in humans cannot always be determined, and ∼25% of outbreaks remain unsolved in New Zealand. It is hypothesized that novel viruses may account for a proportion of unsolved cases, and new unbiased high-throughput sequencing methods hold promise for their detection. Analysis of the fecal metagenome can reveal the presence of viruses, bacteria, and parasites which may have evaded routine diagnostic testing. Thirty-one fecal samples from 26 gastroenteritis outbreaks of unknown etiology occurring in New Zealand between 2011 and 2012 were selected for de novo metagenomic analysis. A total data set of 193 million sequence reads of 150 bp in length was produced on an Illumina MiSeq. The metagenomic data set was searched for virus and parasite sequences, with no evidence of novel pathogens found. Eight viruses and one parasite were detected, each already known to be associated with gastroenteritis, including adenovirus, rotavirus, sapovirus, and Dientamoeba fragilis. In addition, we also describe the first detection of human parechovirus 3 (HPeV3) in Australasia. Metagenomics may thus provide a useful audit tool when applied retrospectively to determine where routine diagnostic processes may have failed to detect a pathogen.

Network-based vaccination improves prospects for disease control in wild chimpanzees

Many endangered wildlife populations are vulnerable to infectious diseases for which vaccines exist; yet, pragmatic considerations often preclude large-scale vaccination efforts. These barriers could be reduced by focusing on individuals with the highest contact rates. However, the question then becomes whether targeted vaccination is sufficient to prevent large outbreaks. To evaluate the efficacy of targeted wildlife vaccinations, we simulate pathogen transmission and control on monthly association networks informed by behavioural data from a wild chimpanzee community (Kanyawara N = 37, Kibale National Park, Uganda). Despite considerable variation across monthly networks, our simulations indicate that targeting the most connected individuals can prevent large outbreaks with up to 35% fewer vaccines than random vaccination. Transmission heterogeneities might be attributed to biological differences among individuals (e.g. sex, age, dominance and family size). Thus, we also evaluate the effectiveness of a trait-based vaccination strategy, as trait data are often easier to collect than interaction data. Our simulations indicate that a trait-based strategy can prevent large outbreaks with up to 18% fewer vaccines than random vaccination, demonstrating that individual traits can serve as effective estimates of connectivity. Overall, these results suggest that fine-scale behavioural data can help optimize pathogen control efforts for endangered wildlife.

Metapopulation models for seasonally migratory animals

Metapopulation models are widely used to study species that occupy patchily distributed habitat, but are rarely applied to migratory species, because of the difficulty of identifying demographically independent subpopulations. Here, we extend metapopulation theory to describe the directed seasonal movement of migratory populations between two sets of habitat patches, breeding and non-breeding, with potentially different colonization and extinction rates between patch types. By extending the classic metapopulation model, we show that migratory metapopulations will persist if the product of the two colonization rates exceeds the product of extinction rates. Further, we develop a spatially realistic migratory metapopulation model and derive a landscape metric—the migratory metapopulation capacity—that determines persistence. This new extension to metapopulation theory introduces an important tool for the management and conservation of migratory species and may also be applicable to model the dynamics of two host–parasite systems.

Invasive ants carry novel viruses in their new range and form reservoirs for a honeybee pathogen.

When exotic animal species invade new environments they also bring an often unknown microbial diversity, including pathogens. We describe a novel and widely distributed virus in one of the most globally widespread, abundant and damaging invasive ants (Argentine ants, Linepithema humile). The Linepithema humile virus 1 is a dicistrovirus, a viral family including species known to cause widespread arthropod disease. It was detected in samples from Argentina, Australia and New Zealand. Argentine ants in New Zealand were also infected with a strain of Deformed wing virus common to local hymenopteran species, which is a major pathogen widely associated with honeybee mortality. Evidence for active replication of viral RNA was apparent for both viruses. Our results suggest co-introduction and exchange of pathogens within local hymenopteran communities. These viral species may contribute to the collapse of Argentine ant populations and offer new options for the control of a globally widespread invader.

Discovery of novel virus sequences in an isolated and threatened bat species, the New Zealand lesser short-tailed bat (Mystacina tuberculata).

Bats harbour a diverse array of viruses, including significant human pathogens. Extensive metagenomic studies of material from bats, in particular guano, have revealed a large number of novel or divergent viral taxa that were previously unknown. New Zealand has only two extant indigenous terrestrial mammals, which are both bats, Mystacina tuberculata (the lesser short-tailed bat) and Chalinolobus tuberculatus (the long-tailed bat). Until the human introduction of exotic mammals, these species had been isolated from all other terrestrial mammals for over 1 million years (potentially over 16 million years for M. tuberculata). Four bat guano samples were collected from M. tuberculata roosts on the isolated offshore island of Whenua hou (Codfish Island) in New Zealand. Metagenomic analysis revealed that this species still hosts a plethora of divergent viruses. Whilst the majority of viruses detected were likely to be of dietary origin, some putative vertebrate virus sequences were identified. Papillomavirus, polyomavirus, calicivirus and hepevirus were found in the metagenomic data and subsequently confirmed using independent PCR assays and sequencing. The new hepevirus and calicivirus sequences may represent new genera within these viral families. Our findings may provide an insight into the origins of viral families, given their detection in an isolated host species.

New Alphacoronavirus in Mystacina tuberculata Bats, New Zealand

Because of recent interest in bats as reservoirs of emerging diseases, we investigated the presence of viruses in Mystacina tuberculata bats in New Zealand. A novel alphacoronavirus sequence was detected in guano from roosts of M. tuberculata bats in pristine indigenous forest on a remote offshore island (Codfish Island).