Biology subjects

Boots, M.

Publications and source records attributed to Boots, M..

At least 19 recordsLinked to original sources

bioRxiv2026

Complex epidemiological dynamics driven by the combination of host spatial structure and seasonal forcing

Spatial population structure and seasonality are both central to the spread of many infectious diseases of plants, animals and humans. While seasonal forcing in transmission often plays an important role in epidemiological models of a wide range of infectious disease, and we now have some theoretical understanding of the dynamical impacts of spatial structure, the combined effects of these two ubiquitous processes has not been examined in detail. Here, we develop a novel model to explore the combined influence of spatial structure and temporal variability on disease dynamics. Spatial structure is represented using a lattice-based approach with near-neighbour interactions, while temporal variability is included through regular, seasonal, variation of the transmission rate. We use bifurcation analysis of a pair approximation of the full spatial model to identify the parameter regimes associated with qualitatively distinct dynamical behaviours. The model exhibits a remarkably wide range of complex dynamics, including limit cycles, quasi-periodic cycles, multi-year cycles, chaotic dynamics and bistability between these different states. In particular, complex dynamics occur when reproduction is predominantly local, with the dynamics depending critically on the amplitude of the seasonal transmission rate. We show how high transmission rates, high birth rates and in particular low recovery rates are requirements for complex dynamics. We predict that SI-type disease interactions in plant pathogen systems will show complex dynamics even with relatively global transmission dynamics.

ecology↗

bioRxiv2025

The impacts of almond pollination on honeybee viral dynamics

Seasonal aggregation of hosts can rapidly reshape microbial and viral communities, with consequences for disease dynamics and spillover risk. Each year, millions of honey bee (Apis mellifera) colonies experience a mass human-mediated intercontinental migration to Californias Central Valley to pollinate most of the worlds almond supply. Clearly, this mass mixing event with hives from across the country has the risk of spreading highly virulent pathogens, including viruses. It is essential to weigh the benefits of the almond bloom against the risks of disease in honeybees, which may also affect native pollinators. We conducted an observational longitudinal RNA-seq study of colonies from a commercial beekeeping operation before, during, and after almond pollination, compared with non-migrating control colonies. We found that viral diversity increased in honeybee colonies during and directly after the bloom; however, it returned to pre-bloom levels a month later. The virome community composition also became more uniform between hives after the bloom. Hives in closer proximity had more similar viromes. This spatial variation suggests that inter-colony drift is a potential transmission route. Together, these findings suggest that the bloom increases viral transmission, with no single virus dominating the communities. Instead, a group of viruses (black queen cell virus, Lake Sinai Virus, deformed wing virus) were responsible for community shifts. Although crop bloom increased viral diversity and community homogenization, this effect was short-lived, with viromes reverting to pre-bloom levels once hives left the orchards. These findings indicate that pollination events can transiently restructure viral communities in managed bees.

microbiology↗

bioRxiv2024

The potential impacts of vector host species fidelity on zoonotic arbovirus transmission

The interaction between vector host preference and host availability on vector blood feeding behaviour has important implications for the transmission of vector-borne pathogens. In particular in multi-host disease systems the fidelity of the vector biting behaviour has the potential to have important implications to disease outcomes, particularly when there are amplifying and dead-end hosts. Using a mathematical model we showed that vector fidelity to the host species they take a first blood meal from leads to non-homogeneous mixing between hosts and vectors. Taking Japanese encephalitis virus (JEV) as a case study, we investigated how vector preference for amplifying vs dead-end hosts and fidelity can influence JEV transmission. We show that in regions where pigs (amplifying hosts) are scarce compared to cattle (dead-end hosts preferred by common JEV vectors), JEV can still be maintained through vector fidelity. Our findings demonstrate the importance of considering fidelity as a potential driver of transmission, particularly in scenarios such as Bangladesh and India where the composition of the host community might initially suggest that transmission is not possible.

ecology↗

bioRxiv2024

Multispecies interactions and the community context of the evolution of virulence

In nature, host-parasite/pathogen relationships are embedded in a network of ecological interactions that have the potential to shape the evolutionary trajectories of shared pathogens. Understanding this community context of infectious disease evolution is important for wildlife, agricultural, and human systems alike - illustrated, for example, by the increasing risk of zoonotic disease emergence. We introduce an eco-evolutionary model that examines ecological feedbacks across a range of host-host interactions. Specifically, we analyze a model of the evolution of virulence of a pathogen infecting hosts who themselves exhibit competitive, mutualistic, or exploitative relationships. We find that pathogen specialism is necessary for inter-host interactions to impact parasite evolution. An important general result is that increasing competition between hosts leads to higher shared pathogen virulence, while increasing mutualism leads to lower virulence. Across a range of scenarios, the nature of pathogen specialization is critical to the outcome - for instance, if hosts only differ in initial susceptibility to infection, there is no impact of host-host interactions on virulence evolution. In contrast, specialization in terms of onward transmission, host tolerance, or intra-host pathogen growth rate critically impact the evolution of virulence. For example, stronger specialism in transmission selects for lower virulence, while stronger specialism in tolerance and growth rate selects for higher virulence. Our work provides testable hypotheses for multi-host disease systems, predicts how changing interaction networks may impact the evolution of virulence, and broadly demonstrates the importance of looking beyond pairwise relationships to understand evolution in realistic natural contexts.

evolutionary biology↗

bioRxiv2023

The direction of local adaptation on pathogen exploitation rates reverses with environmental context

Host heterogeneity and spatial population structure each influence parasite evolution but may also interact because space structures contacts between host types. Here, we experimentally evolve granulosis virus in microcosms of its Plodia interpunctella (Indian meal moth) host that differ in both spatial structure and host genetic diversity. We control spatial structure by manipulating the viscosity of the food that the larvae live within and host genetic diversity by adding larvae from either a single or two inbred lines to opposite ends of the microcosm. We preserve spatial structure across passages and assay virus from different positions within the microcosm on both host genotypes. We find that the lower contact rates between host genotypes resulting from spatial structure can lead to the evolution of locally specialized virus, even when the host population is genetically diverse overall. We also find that spatial structure changes how viruses specialize: viruses evolved in well-mixed environments had lower exploitation of familiar hosts, while those in spatially structured environments exhibited higher exploitation of familiar hosts. These results demonstrate that spatial structure and host heterogeneity interact to shape pathogen specialization and that the evolutionary consequences of host diversity depends on the population structure.

evolutionary biology↗

bioRxiv2022

Extending eco-evolutionary theory with oligomorphic dynamics

Understanding the interplay between ecological processes and the evolutionary dynamics of quantitative traits in natural systems remains a major challenge. Two main theoretical frameworks are used to address this question, adaptive dynamics and quantitative genetics, both of which have strengths and limitations and are often used by distinct research communities to address different questions. In order to make progress, new theoretical developments are needed that integrate these approaches and strengthen the link to empirical data. Here, we discuss a novel theoretical framework that bridges the gap between quantitative genetics and adaptive dynamics approaches. "Oligomorphic dynamics" can be used to analyse eco-evolutionary dynamics across different time scales and extends quantitative genetics theory to account for multimodal trait distributions, the dynamical nature of genetic variance, the potential for disruptive selection due to ecological feed-backs, and the non-normal or skewed trait distributions encountered in nature. Oligomorphic dynamics explicitly takes into account the effect of environmental feedback, such as frequency- and density-dependent selection, on the dynamics of multi-modal trait distributions and we argue it has the potential to facilitate a much tighter integration between eco-evolutionary theory and empirical data.

evolutionary biology↗

bioRxiv2022

The evolution of host resistance to a virus is determined by resources, historical contingency, and time scale

Hosts can often evolve resistance to parasites (and other stressors), but such resistance is generally thought to be constrained by trade-offs with other traits. These trade-offs determine the hosts optimal resistance strategy and whether resistance cycles, diversifies, and/or is maintained in the absence of parasite. However, trade-offs are often inconsistently measured across experiments and can depend on environmental conditions. Here, we extend a selection experiment evolving resistance to viral infection under variable resource quality in the Plodia interpunctella model system to explore the evolutionary conditions leading to an incongruent earlier measurement of costless resistance. We find that environmental resource quality, historical contingency, and the time scale of selection all affect trade-offs in our long-term selection experiment. Specifically, populations selected for resistance with the dual stressor of low resource quality are slowed, but not prevented, from evolving resistance. Second, variation in starting populations or early sampled adaptations led to contingency towards context-dependent resistance. Finally, some costs to resistance observed at early time points were compensated over longer evolutionary time scales. Our work therefore informs perspectives for the predictability of adaptation and how variation in specific evolutionary conditions can alter the evolutionary trajectories of a population towards costly or costless resistance strategies.

evolutionary biology↗

bioRxiv2022

Multimodal disease transmission as a limiting factor for the spatial extent of a host plant

Theoretical models suggest that infectious diseases could play a substantial role in determining species ranges, but few studies have collected the empirical data required to test this hypothesis. Pathogens that sterilize their hosts or spread through frequency-dependent transmission could have especially strong effects on the limits of species distributions because sterilized hosts can serve as long-lived disease reservoirs and frequency-dependent transmission mechanisms are effective even at very low population densities. We collected spatial disease prevalence data and population abundance data for alpine carnations infected by the sterilizing pathogen M. violaceum, a disease that is spread through both frequency-dependent (vector-borne) and density-dependent (aerial spore transmission) mechanisms. Our 13-year study reveals rapid declines in population abundance without a compensatory decrease in disease prevalence. We apply a stochastic, spatial model of disease spread that accommodates spatial habitat heterogeneity to investigate how the population dynamics depend on multimodal (frequency-dependent and density-dependent) transmission. We found that the observed rate of population decline can be readily explained by multimodal transmission, but is unlikely to be explained by either frequency-dependent or density-dependent mechanisms alone. Multimodal disease transmission rates high enough to explain the observed decline predicted that eventual local extinction of the host species is highly likely. Our results add to a growing body of literature showing how multimodal transmission can constrain species distributions in nature. Open ResearchAll scripts associated with the analyses in this manuscript, as well as the data we collected, are available at https://github.com/uricchio/antherSmutDis.

ecology↗

bioRxiv2021

The Evolutionary Dynamics of Hyperparasites

Evolutionary theory has typically focused on pairwise interactions, such as those between hosts and parasites, with relatively little work on more complex interactions including hyperparasites: parasites of parasites. Hyperparasites are common in nature, with the chestnut blight fungus virus CHV-1 a well-known natural example, but also notably include the phages of important human bacterial diseases. Theory on hyperparasitism has mostly focused on their impact on the evolution of virulence of their parasite host and relatively little is known about evolutionary trajectories of hyperparasites themselves. Our general modeling framework highlights the central role the that ability of a hyperparasite to be transmitted with its parasite plays in their evolution. Hyperparasites which transmit with their parasite hosts (hitchhike) will be selected for lower virulence, trending towards hypermutualism or hypercommensalism and select against causing a reduction in parasite virulence (hypovirulence). We examine the impact on the evolution of hyperparasite systems a of a wide range of host and parasite traits showing, for example, that high parasite virulence selects for higher hyperparasite virulence feeding back into selection for hypovirulence in the parasite. Our results have implications for hyperparasite research, both as biocontrol agents and for understanding of how hyperparasites shape community ecology and evolution.

evolutionary biology↗

bioRxiv2021

The Evolution of Host Specialization in an Insect Pathogen

Niche breadth coevolution between biotic partners underpins theories of diversity and co-existence and influences patterns of disease emergence and transmission in host-parasite systems. Despite these broad implications, we still do not fully understand how the breadth of parasites infectivity evolves, the nature of any associated costs, or the genetic basis of specialization. Here, we serially passage a granulosis virus on multiple inbred populations of its Plodia interpunctella host to explore the dynamics and outcomes of specialization. In particular, we collect time series of phenotypic and genetic data to explore the dynamics of host genotype specialization throughout the course of experimental evolution and examine two fitness components. We find that the Plodia interpunctella granulosis virus consistently evolves increases in overall specialization, but that our two fitness components evolve independently such that lines specialize in either productivity or infectivity. Furthermore, we find that specialization in our experiment is a highly polygenic trait best explained by a combination of evolutionary mechanisms including conditionally positive fitness asymmetries and mutation accumulation. These results are important for understanding the evolution of specialization in host-parasite interactions and its broader implications for co-existence, diversification, and infectious disease management.

evolutionary biology↗

bioRxiv2021

Reservoir host immunology and life history shape virulence evolution in zoonotic viruses

The management of future pandemic risk requires a better understanding of the mechanisms that determine the virulence of emerging zoonotic viruses. Meta-analyses suggest that the virulence of emerging zoonoses is correlated with but not completely predictable from reservoir host phylogeny, indicating that specific characteristics of reservoir host immunology and life history may drive the evolution of viral traits responsible for cross-species virulence. In particular, bats host viruses that cause higher case fatality rates upon spillover to humans than those derived from any other mammal, a phenomenon that cannot be explained by phylogenetic distance alone. In order to disentangle the fundamental drivers of these patterns, we develop a nested modeling framework that highlights mechanisms which underpin the evolution of viral traits in reservoir hosts that cause virulence following cross-species emergence. We apply this framework to generate virulence predictions for viral zoonoses derived from diverse mammalian reservoirs, successfully recapturing corresponding virus-induced human mortality rates reported in the literature. Notably, our work offers a mechanistic explanation for the extreme virulence of bat-borne zoonoses and, more generally, demonstrates how key differences in reservoir host longevity, viral tolerance, and constitutive immunity impact the evolution of viral traits that cause virulence following spillover to humans. Our theoretical framework offers a series of testable questions and hypotheses designed to stimulate future work comparing cross-species virulence evolution in zoonotic viruses derived from diverse mammalian hosts.

evolutionary biology↗

bioRxiv2021

Bats host the most virulent--but not the most dangerous--zoonotic viruses

Identifying virus characteristics associated with the largest public health impacts on human populations is critical to informing zoonotic risk assessments and surveillance strategies. Efforts to assess "zoonotic risk" often use trait-based analyses to identify which viral and reservoir host groups are most likely to source zoonoses but have not fully addressed how and why the impacts of zoonotic viruses vary in terms of disease severity ( virulence), capacity to spread within human populations ( transmissibility), or total human mortality ( death burden). We analyzed trends in human case fatality rates, transmission capacities, and total death burdens across a comprehensive dataset of mammalian and avian zoonotic viruses. Bats harbor the most virulent zoonotic viruses even when compared to birds, which alongside bats, have been hypothesized to be "special" zoonotic reservoirs due to molecular adaptations that support the physiology of flight. Reservoir host groups more closely related to humans--in particular, Primates--harbor less virulent, but more highly transmissible viruses. Importantly, disproportionately high human death burden, arguably the most important metric of zoonotic risk, is not associated with any animal reservoir, including bats. Our data demonstrate that mechanisms driving death burdens are diverse and often contradict trait-based predictions. Ultimately, total human mortality is dependent on context-specific epidemiological dynamics, which are shaped by a combination of viral traits and conditions in the animal host population and across and beyond the human-animal interface. Understanding the conditions that predict high zoonotic burden in humans will require longitudinal studies of epidemiological dynamics in wildlife and human populations. Significance statementThe clear need to mitigate zoonotic risk has fueled increased viral discovery in specific reservoir host taxa. We show that a combination of viral and reservoir traits can predict zoonotic virus virulence and transmissibility in humans, supporting the hypothesis that bats harbor exceptionally virulent zoonoses. However, pandemic prevention requires thinking beyond zoonotic capacity, virulence, and transmissibility to consider collective burden on human health. For this, viral discovery targeting specific reservoirs may be inefficient as death burden correlates with viral, not reservoir, traits, and depends on context-specific epidemiological dynamics across and beyond the human-animal interface. These findings suggest that longitudinal studies of viral dynamics in reservoir and spillover host populations may offer the most effective strategy for mitigating zoonotic risk.

ecology↗

bioRxiv2021

Multi-morph eco-evolutionary dynamics in structured populations

Our understanding of the evolution of quantitative traits in nature is still limited by the challenge of including realistic trait distributions in the context of frequency-dependent selection and ecological feedbacks. We extend to class-structured populations a recently introduced "oligomorphic approximation" which bridges the gap between adaptive dynamics and quantitative genetics approaches and allows for the joint description of the dynamics of ecological variables and of the moments of multimodal trait distributions. Our theoretical framework allows us to analyse the dynamics of populations composed of several morphs and structured into distinct classes (e.g. age, size, habitats, infection status, species...). We also introduce a new approximation to simplify the eco-evolutionary dynamics using reproductive values. We illustrate the effectiveness of this approach by applying it to the important conceptual case of two-habitat migration-selection models. In particular, we show that our approach allows us to predict both the long-term evolutionary endpoints and the short-term transient dynamics of the eco-evolutionary process, including fast evolution regimes. We discuss the theoretical and practical implications of our results and sketch perspectives for future work.

evolutionary biology↗

bioRxiv2020

Ecological processes underlying the emergence of novel enzootic cycles--arboviruses in the neotropics as a case study

Pathogens originating from wildlife (zoonoses) pose a significant public health burden, comprising the majority of emerging infectious diseases. Efforts to control and prevent zoonotic disease have traditionally focused on animal-to-human transmission, or "spillover". However, in the modern era, increasing international mobility and commerce facilitate the spread of infected humans, non-human animals (hereafter animals), and their products worldwide, thereby increasing the risk that zoonoses will be introduced to new geographic areas. Imported zoonoses can potentially spill back to infect local wildlife--a danger magnified by urbanization and other anthropogenic pressures that increase contacts between human and wildlife populations. In this way, humans can function as vectors, dispersing zoonoses from their ancestral enzootic systems to establish reservoirs elsewhere in novel animal host populations. Once established, these enzootic cycles are largely unassailable by standard control measures and have the potential to feed human epidemics. Understanding when and why translocated zoonoses establish novel enzootic cycles requires disentangling ecologically complex and stochastic interactions between the zoonosis, the human population, and the natural ecosystem. We address this challenge by delineating potential ecological mechanisms affecting each stage of enzootic establishment--wildlife exposure, enzootic infection, and persistence--applying existing ecological concepts from epidemiology, invasion biology, and population ecology. We ground our study in the neotropics, where four arthropod-borne viruses (arboviruses) of zoonotic origin--yellow fever, dengue, chikungunya, and Zika viruses--have separately been introduced into the human population. This paper is a step towards developing a framework for predicting and preventing novel enzootic cycles in the face of zoonotic translocations.

ecology↗

bioRxiv2019

Within-host dynamics of virulent viruses in bat reservoirs for emerging zoonotic disease

Bats host virulent zoonotic viruses without experiencing disease. A mechanistic understanding of the impact of bats virus hosting capacities, including uniquely constitutive immune pathways, on cellular-scale viral dynamics is needed to elucidate zoonotic emergence. We carried out virus infectivity assays on bat cell lines expressing induced and constitutive immune phenotypes, then developed a theoretical model of our in vitro system, which we fit to empirical data. Best fit models recapitulated expected immune phenotypes for representative cell lines, supporting robust antiviral defenses in bat cells that correlated with higher estimates for within-host viral propagation rates. In general, heightened immune responses limit pathogen-induced cellular morbidity, which can facilitate the establishment of rapidly-propagating persistent infections within-host. Rapidly-replicating viruses that have evolved with bat immune systems will likely cause enhanced virulence following emergence into secondary hosts with immune systems that diverge from those unique to bats.

ecology↗

bioRxiv2019

The genomic basis of evolved virus resistance is dependent on environmental resources

Parasites impose strong selection on their hosts, but the level of resistance evolved may be constrained by the availability of resources. However, studies identifying the genomic basis of such resource mediated selection are rare, particularly in non-model organisms. Here, we investigated the role of nutrition in the evolution of resistance to a DNA virus (PiGV), and associated trade-offs, in a lepidopteran pest species (Plodia interpunctella). Through selection experiments and whole genome sequencing we identify putative mechanisms of resistance that depend on the nutritional environment during selection. We find that the evolution of resistance is specific to diet, with adaptation to a low nutrition diet constraining resistance when challenged with the pathogen on a high nutrition diet. Resistance in a low nutrition environment is negatively correlated with growth rate, consistent with an established trade-off between immunity and development. Whole genome resequencing of the host shows that resistance mechanisms are highly polygenic and suggests evidence for trade-offs at the genetic level. Critically when populations evolve in high resource conditions, resistance is linked to metabolic and immune pathways, however it is more closely associated with cytoskeleton organisation when selected under low nutrition. Our results emphasise the importance of resources on the evolution of resistance.

evolutionary biology↗

bioRxiv2018

More than a flying syringe: Using functional traits in vector borne disease research

Many important endemic and emerging diseases are vector-borne. The functional traits of vectors affect not just pathogen transmission rates, but also the fitness and population dynamics of these animals themselves. Increasing empirical evidence suggests that vector traits vary significantly at time scales relevant to transmission dynamics. Currently, an understanding of how this variation in key traits impacts transmission is hindered by a lack of both empirical data and theoretical methods for mechanistically incorporating traits into transmission models. Here, we present a framework for incorporating both intrinsic and environment-driven variation in vector traits into empirical and theoretical vector-borne disease research. This framework mechanistically captures the effect of trait variation on vector fitness, the correlation between vector traits, and how these together determine transmission dynamics. We illustrate how trait-based vector-borne disease modelling can make novel predictions, and identify key steps and challenges in the construction, empirical parameterisation and validation of such models, as well as the organization and prioritization of data collection efforts.

ecology↗

bioRxiv2018

Industrial bees: when agricultural intensification doesn’t impact local disease prevalence

O_LIAlthough it is generally thought that the intensification of farming will result in higher disease prevalences there is little specific modelling testing this idea. We build multi-colony models to inform how apicultural intensification is predicted to impact honeybee pathogen epidemiology at the apiary scale.\nC_LIO_LICounter to the prevailing view, our models predict that intensification, captured though increased population sizes, changes in population network structure, and increased between-colony transmission, is likely to have little effect on disease prevalence within an apiary.\nC_LIO_LIThe greatest impacts of intensification are found for diseases with relatively low R0 (basic reproduction number), however, such diseases cause little overall disease prevalence and therefore the impacts of intensification are minor. Furthermore, the smallest impacts of intensification are found for diseases with high R0 values, which we argue are typical of important honeybee diseases.\nC_LIO_LIPolicy Implications: Our findings highlight a lack of support for the hypothesis that current and ongoing intensification leads to notably higher disease prevalences. More broadly, our work demonstrates the need for informative models of agricultural systems and management practices in order to understand the implications of management changes on diseases.\nC_LI

epidemiology↗