ABSTRACT
Engineered gene drives create potential for both widespread benefits and irreversible harms to ecosystems. CRISPR-based systems of allelic conversion have rapidly accelerated gene drive research across diverse taxa, putting field trials and their necessary risk assessments on the horizon. Dynamic process-based models provide flexible quantitative platforms to predict gene drive outcomes in the context of system-specific ecological and evolutionary features. Here, we synthesize gene drive dynamic modeling studies to highlight research trends, knowledge gaps, and emergent principles, organized around their genetic, demographic, spatial, environmental, and implementation features. We identify the phenomena that most significantly influence model predictions, discuss limitations of biological complexity and uncertainty, and provide insights to promote responsible development and model-assisted risk assessment of gene drives.
Subject(s)
Gene Drive Technology , Ecosystem , Biological Evolution , Risk AssessmentABSTRACT
BACKGROUND: Parasites are recognized for their ability to modify host physiology and behaviours in ways that increase parasite fitness. Protozoan parasites of the genus Plasmodium are a group of widespread vector-borne parasites of vertebrates, causing disease to a wide range of hosts, but most notably to human and avian hosts. METHODS: The hypothesis that infection with the avian malaria, Plasmodium relictum (GRW4 lineage) impacts flight activity in one of their natural vectors, Culex quinquefasciatus, was tested using both parasites and mosquitoes colonized from local populations in East-Central Texas, USA. Groups of Cx. quinquefasciatus were allowed to feed directly on canaries with active P. relictum infections and control canaries with no P. relictum exposure history. Additionally, how P. relictum sporozoite invasion of mosquito salivary glands impacts mosquito flight activity behaviour was tested using a Locomotor Activity Monitor for both control and infected females. Generalized linear mixed models were used to evaluate the influence of infection status on the response variables of flight activity (continuous) and probability of flight occurring (binomial). RESULTS: Infection status was a significant predictor of flight activity and flight probability and interactions between infection status and experimental period of infection as well as infection status and dusk were statistically significant predictors of flight activity. Plasmodium relictum infected mosquitoes had a mean flight activity of 3.10 and control mosquitoes had an overall mean flight activity of 3.13. DISCUSSION: Based on these results, avian malaria parasites increase the flight activity of these mosquitoes at hours known for peak host-seeking behaviour but decrease overall diel activity. CONCLUSION: Although the ramifications of this behavioural change for P. relictum transmission are unclear, these results provide additional empirical evidence suggesting that avian malaria can influence mosquito behaviour and modulate transmission potential.
Subject(s)
Culex , Culicidae , Malaria, Avian , Malaria , Plasmodium , Animals , Culex/physiology , Culicidae/parasitology , Female , Humans , Malaria, Avian/parasitology , Mosquito VectorsABSTRACT
Arthropod vectors are frequently exposed to a diverse assemblage of parasites, but the consequence of these infections on their biology and behavior are poorly understood. We experimentally evaluated whether the ingestion of a common protozoan parasite of avian hosts (Haemoproteus spp.; Haemosporida: Haemoproteidae) impacted the survivorship of Culex quinquefasciatus (Say) (Diptera: Culicidae). Blood was collected from wild northern cardinals (Cardinalis cardinalis) in College Station, Texas, and screened for the presence of Haemoproteus spp. parasites using microscopic and molecular methods. Experimental groups of Cx. quinquefasciatus mosquitoes were offered Haemoproteus-positive cardinal blood through an artificial feeding apparatus, while control groups received Haemoproteus-negative cardinal blood or domestic canary (Serinus canaria domestica) blood. Culex quinquefasciatus mosquitoes exposed to Haemoproteus infected cardinal blood survived significantly fewer days than mosquitoes that ingested Haemoproteus-negative cardinal blood. The survival of mosquitoes fed on positive cardinal blood had a median survival time of 18 days post-exposure and the survival of mosquitoes fed on negative cardinal blood exceeded 50% across the 30 day observation period. Additionally, mosquitoes that fed on canary controls survived significantly fewer days than cardinal negative controls, with canary control mosquitoes having a median survival time of 17 days. This study further supports prior observations that Haemoproteus parasites can be pathogenic to bird-biting mosquitoes, and suggests that Haemoproteus parasites may indirectly suppress the transmission of co-circulating vector-borne pathogens by modulating vector survivorship. Our results also suggest that even in the absence of parasite infection, bloodmeals from different bird species can influence mosquito survivorship.
Subject(s)
Culex/physiology , Culex/parasitology , Haemosporida/physiology , Mosquito Vectors/physiology , Mosquito Vectors/parasitology , Passeriformes/parasitology , Animals , Bird Diseases/parasitology , Bird Diseases/transmission , Canaries/blood , Canaries/parasitology , DNA, Protozoan/blood , Passeriformes/blood , Polymerase Chain Reaction/veterinary , Probability , Proportional Hazards Models , Protozoan Infections, Animal/parasitology , Protozoan Infections, Animal/transmission , TexasABSTRACT
Great-tailed grackles (Quiscalus mexicanus) have dramatically expanded into North America over the past century. However, little is known about the blood that parasites they support. Here, for the first time, we document an assemblage of trypanosome, haemosporida, and filarial nematodes co-circulating in invasive great-tailed grackles. Between February and July, 2015, 61 individuals were captured in an urban environment of College Station, Texas. Field microscopy and molecular diagnostics indicate that 52% (24/46) were visually infected with filarioid nematodes, 24% (11/46) with avian trypanosomes, and 73% (n = 44/60) with haemosporida parasites, such as Haemoproteus (Parahaemoproteus) and Plasmodium cathemerium. Overall, 87% of great-tailed grackles were infected with blood parasites. Although 50% of individuals hosted parasites from multiple phylum, no patterns of parasite assembly were observed. Results indicate that great-tailed grackles can support a relatively high level of blood parasitism. However, the consequences for avian health remain to be determined.
ABSTRACT
Robust methods of predicting how gene drive systems will interact with ecosystems is essential for safe deployment of gene drive technology. We describe how quantitative tools can reduce risk uncertainty, streamline empirical research, guide risk management, and promote cross-sector collaboration throughout the process of gene drive technology development and implementation.
Subject(s)
Ecosystem , Gene Drive Technology , Models, Genetic , Gene Drive Technology/standards , Gene Drive Technology/trends , Risk ManagementABSTRACT
Environmental sources of infection can play a primary role in shaping epidemiological dynamics; however, the relative impact of environmental transmission on host-pathogen systems is rarely estimated. We developed and fit a spatially explicit model of African swine fever virus (ASFV) in wild boar to estimate what proportion of carcass-based transmission is contributing to the low-level persistence of ASFV in Eastern European wild boar. Our model was developed based on ecological insight and data from field studies of ASFV and wild boar in Eastern Poland. We predicted that carcass-based transmission would play a substantial role in persistence, especially in low-density host populations where contact rates are low. By fitting the model to outbreak data using approximate Bayesian computation, we inferred that between 53% and 66% of transmission events were carcass-based that is, transmitted through contact of a live host with a contaminated carcass. Model fitting and sensitivity analyses showed that the frequency of carcass-based transmission increased with decreasing host density, suggesting that management policies should emphasize the removal of carcasses and consider how reductions in host densities may drive carcass-based transmission. Sensitivity analyses also demonstrated that carcass-based transmission is necessary for the autonomous persistence of ASFV under realistic parameters. Autonomous persistence through direct transmission alone required high host densities; otherwise re-introduction of virus periodically was required for persistence when direct transmission probabilities were moderately high. We quantify the relative role of different persistence mechanisms for a low-prevalence disease using readily collected ecological data and viral surveillance data. Understanding how the frequency of different transmission mechanisms vary across host densities can help identify optimal management strategies across changing ecological conditions.
ABSTRACT
African swine fever virus (ASFV) continues to threaten global animal health and agricultural biosecurity. Mitigating the establishment of ASFV in the United States (U.S.) is contingent on (1) the identification of arthropod vectors and vertebrate hosts that are capable of viral maintenance and transmission in the U.S. and (2) knowledge of vector-host associations that may permit transmission. We aggregated data on vector competence, host competence and tick-host associations by systematic review of published articles and collection records to identify species that may support the invasion of ASFV in the U.S. Three species of competent soft ticks occur in the U.S., Ornithodoros coriaceus, Ornithodoros turicata, and Ornithodoros puertoricensis, however, vector competence for the majority of soft ticks in the U.S. remains unknown. Three species of competent vertebrate hosts currently occur in the U.S.: domestic pigs (Sus scrofa domesticus), feral hogs (Sus scrofa), and common warthogs (Phacochoerus africanus). Hierarchical hazard categories based on vector competence, tick-host contact rates, and vector abundance were used to semiquantitatively rank U.S. soft tick species by their relative risk for contributing to ASFV transmission to identify which soft tick species are a priority for future studies. High-risk vector and host species identified in this study can be used to focus ASFV risk assessments in the U.S., guide targeted surveillance and control strategies, and proactively prepare for an ASFV incursion event. Results indicate O. coriaceus, O. turicata, and O. puertoricensis demonstrate the highest relative risk for contributing to ASFV transmission in the U.S., however, many gaps in knowledge exist preventing the full evaluation of at least 30 soft tick species in the U.S. Further study is required to identify soft tick vectors that interact with feral swine populations, elucidate vector competence, and further understand the biology of soft tick species.
Subject(s)
African Swine Fever/transmission , Arachnid Vectors/virology , Ornithodoros/virology , Swine Diseases/radiotherapy , African Swine Fever Virus , Animals , Argasidae/virology , Sus scrofa , Swine , Swine Diseases/transmission , Swine Diseases/virology , United StatesABSTRACT
Flanders virus (FLAV; family Rhabdoviridae) is a mosquito-borne hapavirus with no known pathology that is frequently isolated during arbovirus surveillance programs. Here, we document the presence of FLAV in Culex tarsalis mosquitoes and a Canada goose (Branta canadensis) collected in western North America, outside of the currently recognized range of FLAV. Until now, FLAV-like viruses detected in the western United States were assumed to be Hart Park virus (HPV, family Rhabdoviridae), a closely related congener. A re-examination of archived viral isolates revealed that FLAV was circulating in California as early as 1963. FLAV also was isolated in Nebraska, Colorado, South Dakota, North Dakota, and Saskatchewan, Canada. Phylogenetic analysis of the U1 pseudogene for 117 taxa and eight nuclear genes for 15 taxa demonstrated no distinct clustering between western FLAV isolates. Assuming the range of FLAV has been expanding west, these results indicate that FLAV likely spread west following multiple invasion events. However, it remains to be determined if the detection of FLAV in western North America is due to expansion or is a result of enhanced arbovirus surveillance or diagnostic techniques. Currently, the impact of FLAV infection remains unknown.
Subject(s)
Bird Diseases/virology , Culex/virology , Geese/virology , Mosquito Vectors/virology , Rhabdoviridae Infections/veterinary , Rhabdoviridae/isolation & purification , Animals , Bird Diseases/transmission , North America , Phylogeny , Rhabdoviridae/classification , Rhabdoviridae/genetics , Rhabdoviridae Infections/transmission , Rhabdoviridae Infections/virology , SeasonsABSTRACT
Culex quinquefasciatus is the principal vector of West Nile virus (WNV) in the South Central United States, yet limited data on host utilization are available. We evaluated host utilization over a 3-month period in 2013 in a residential landscape in College Station, Texas. PCR sequencing of the mitochondrial cytochrome oxidase 1 gene permitted molecular identification of vertebrate bloodmeals to the species level. Forage ratio analysis identified bird species that were overutilized and underutilized by comparing community feeding index values to expected relative abundance values of bird species, derived from eBird data. Community feeding index values were also used in conjunction with reservoir competence data from the literature to generate reservoir capacity index values, a means of identifying relative importance of vertebrate reservoir hosts. Of 498 blood-engorged Cx. quinquefasciatus, 313 (62.9%) were identified to vertebrate species. The majority (95.5%) of bloodmeals originated from avian species with the remainder from mammals, but not humans. Northern mockingbird (Mimus polyglottos) was the principal host for mosquito feeding in June and July, but northern cardinal (Cardinalis cardinalis) became primary host in August. Forage ratio analysis revealed the overutilization of house finch (Haemorhous mexicanus), American robin (Turdus migratorius), northern mockingbird, northern cardinal, white-winged dove (Zenaida asiatica), and mourning dove (Zenaida macroura). Great-tailed grackle (Quiscalus mexicanus), blue jay (Cyanocitta cristata), and Carolina wren (Thryothorus ludovicianus) were under-utilized relative to availability. Reservoir capacity calculations suggested that northern mockingbird and northern cardinal were the principal amplifiers in the study area. These data identify the primary avian species contributing to the enzootic amplification of WNV in East-Central Texas and reveal that the heavy feeding on moderately competent hosts and no feeding on humans likely limit epidemics in this region.
Subject(s)
Birds/blood , Culex/physiology , Feeding Behavior , Mammals/blood , Animals , Species Specificity , TexasABSTRACT
Rift Valley fever virus (RVFV) is a mosquito-borne virus in the family Bunyaviridiae that has spread throughout continental Africa to Madagascar and the Arabian Peninsula. The establishment of RVFV in North America would have serious consequences for human and animal health in addition to a significant economic impact on the livestock industry. Published and unpublished data on RVFV vector competence, vertebrate host competence, and mosquito feeding patterns from the United States were combined to quantitatively implicate mosquito vectors and vertebrate hosts that may be important to RVFV transmission in the United States. A viremia-vector competence relationship based on published mosquito transmission studies was used to calculate a vertebrate host competence index which was then combined with mosquito blood feeding patterns to approximate the vector and vertebrate amplification fraction, defined as the relative contribution of the mosquito or vertebrate host to pathogen transmission. Results implicate several Aedes spp. mosquitoes and vertebrates in the order Artiodactyla as important hosts for RVFV transmission in the U.S. Moreover, this study identifies critical gaps in knowledge which would be necessary to complete a comprehensive analysis identifying the different contributions of mosquitoes and vertebrates to potential RVFV transmission in the U.S. Future research should focus on (1) the dose-dependent relationship between viremic exposure and the subsequent infectiousness of key mosquito species, (2) evaluation of vertebrate host competence for RVFV among North American mammal species, with particular emphasis on the order Artiodactyla, and (3) identification of areas with a high risk for RVFV introduction so data on local vector and host populations can help generate geographically appropriate amplification fraction estimates.