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  1. Abstract Background

    Effectively controlling heartworm disease—a major parasitic disease threatening animal health in the US and globally—requires understanding the local ecology of mosquito vectors involved in transmission. However, the key vector species in a given region are often unknown and challenging to identify. Here we investigate (i) the key vector species associated with transmission of the parasite,Dirofilaria immitis, in California and (ii) the climate and land cover drivers of vector presence.

    Methods

    To identify key mosquito vectors involved in transmission, we incorporated long-term, finely resolved mosquito surveillance data and dog heartworm case data in a statistical modeling approach (fixed-effects regression) that rigorously controls for other unobserved drivers of heartworm cases. We then used a flexible machine learning approach (gradient boosted machines) to identify the climate and land cover variables associated with the presence of each species.

    Results

    We found significant, regionally specific, positive associations between dog heartworm cases and the abundance of four vector species:Aedes aegypti(Central California),Ae. albopictus(Southern California),Ae. sierrensis(Central California), andCuliseta incidens(Northern and Central California). The proportion of developed land cover was one of the most important ecological variables predicting the presence or absence of the putative vector species.

    Conclusion

    Our results implicate three previously under-recognized vectors of dog heartworm transmission in California and indicate the land cover types in which each putative vector species is commonly found. Efforts to target these species could prioritize surveillance in these land cover types (e.g. near human dwellings in less urbanized settings forAe. albopictusandCs. incidens) but further investigation on the natural infection prevalence and host-biting rates of these species, as well as the other local vectors, is needed.

    Graphical Abstract 
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  2. A vector's susceptibility and ability to transmit a pathogen—termed vector competency—determines disease outcomes, yet the ecological factors influencing tick vector competency remain largely unknown. Ixodes pacificus, the tick vector of Borrelia burgdorferi (Bb) in the western U.S., feeds on rodents, birds, and lizards. Rodents and birds are reservoirs for Bb and infect juvenile ticks, while lizards are refractory to Bb and cannot infect feeding ticks. Additionally, the lizard bloodmeal contains borreliacidal properties, clearing previously infected feeding ticks of their Bb infection. Despite I. pacificus feeding on a range of hosts, it is undetermined how the host identity of the larval bloodmeal affects future nymphal vector competency. We experimentally evaluate the influence of larval host bloodmeal on Bb acquisition by nymphal I. pacificus. Larval I. pacificus were fed on either lizards or mice and after molting, nymphs were fed on Bb-infected mice. We found that lizard-fed larvae were significantly more likely to become infected with Bb during their next bloodmeal than mouse-fed larvae. We also conducted the first RNA-seq analysis on whole-bodied I. pacificus and found significant upregulation of tick antioxidants and antimicrobial peptides in the lizard-fed group. Our results indicate that the lizard bloodmeal significantly alters vector competency and gene regulation in ticks, highlighting the importance of host bloodmeal identity in vector-borne disease transmission and upends prior notions about the role of lizards in Lyme disease community ecology. 
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  3. null (Ed.)
    The potential for adaptive evolution to enable species persistence under a changing climate is one of the most important questions for understanding impacts of future climate change. Climate adaptation may be particularly likely for short-lived ectotherms, including many pest, pathogen, and vector species. For these taxa, estimating climate adaptive potential is critical for accurate predictive modeling and public health preparedness. Here, we demonstrate how a simple theoretical framework used in conservation biology—evolutionary rescue models—can be used to investigate the potential for climate adaptation in these taxa, using mosquito thermal adaptation as a focal case. Synthesizing current evidence, we find that short mosquito generation times, high population growth rates, and strong temperature-imposed selection favor thermal adaptation. However, knowledge gaps about the extent of phenotypic and genotypic variation in thermal tolerance within mosquito populations, the environmental sensitivity of selection, and the role of phenotypic plasticity constrain our ability to make more precise estimates. We describe how common garden and selection experiments can be used to fill these data gaps. Lastly, we investigate the consequences of mosquito climate adaptation on disease transmission using Aedes aegypti -transmitted dengue virus in Northern Brazil as a case study. The approach outlined here can be applied to any disease vector or pest species and type of environmental change. 
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  4. Insight into the composition and function of the tick microbiome has expanded considerably in recent years. Thus far, tick microbiome studies have focused on species and life stages that are responsible for transmitting disease. In this study we conducted extensive field sampling of six tick species in the far-western United States to comparatively examine the microbial composition of sympatric tick species: Ixodes pacificus, Ixodes angustus, Dermacentor variabilis, Dermacentor occidentalis, Dermacentor albipictus, and Haemaphysalis leporispalustris. These species represent both common vectors of disease and species that rarely encounter humans, exhibiting a range of host preferences and natural history. We found significant differences in microbial species diversity and composition by tick species and life stage. The microbiome of most species examined were dominated by a few primary endosymbionts. Across all species, the relative abundance of these endosymbionts increased with life stage while species richness and diversity decreased with development. Only one species, I. angustus, did not show the presence of a single dominant microbial species indicating the unique physiology of this species or its interaction with the surrounding environment. Tick species that specialize in a small number of host species or habitat ranges exhibited lower microbiome diversity, suggesting that exposure to environmental conditions or host blood meal diversity can affect the tick microbiome which in turn may affect pathogen transmission. These findings reveal important associations between ticks and their microbial community and improve our understanding of the function of non-pathogenic microbiomes in tick physiology and pathogen transmission. 
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  5. Abstract

    Lyme disease is the most common vector‐borne disease in temperate zones and a growing public health threat in the United States (US). The life cycles of the tick vectors and spirochete pathogen are highly sensitive to climate, but determining the impact of climate change on Lyme disease burden has been challenging due to the complex ecology of the disease and the presence of multiple, interacting drivers of transmission. Here we incorporated 18 years of annual, county‐level Lyme disease case data in a panel data statistical model to investigate prior effects of climate variation on disease incidence while controlling for other putative drivers. We then used these climate–disease relationships to project Lyme disease cases using CMIP5 global climate models and two potential climate scenarios (RCP4.5 and RCP8.5). We find that interannual variation in Lyme disease incidence is associated with climate variation in all US regions encompassing the range of the primary vector species. In all regions, the climate predictors explained less of the variation in Lyme disease incidence than unobserved county‐level heterogeneity, but the strongest climate–disease association detected was between warming annual temperatures and increasing incidence in the Northeast. Lyme disease projections indicate that cases in the Northeast will increase significantly by 2050 (23,619 ± 21,607 additional cases), but only under RCP8.5, and with large uncertainty around this projected increase. Significant case changes are not projected for any other region under either climate scenario. The results demonstrate a regionally variable and nuanced relationship between climate change and Lyme disease, indicating possible nonlinear responses of vector ticks and transmission dynamics to projected climate change. Moreover, our results highlight the need for improved preparedness and public health interventions in endemic regions to minimize the impact of further climate change‐induced increases in Lyme disease burden.

     
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  6. Abstract

    Vector‐borne diseases constitute a major global health burden and are increasing in geographic range and prevalence. Mounting evidence has demonstrated that the vector microbiome can impact pathogen dynamics, making the microbiome a focal point in vector‐borne disease ecology. However, efforts to generalize preliminary findings across studies and systems and translate these findings into disease control strategies are hindered by a lack of fundamental understanding of the processes shaping the vector microbiome and the interactions therein. Here, we use 16S rRNA sequencing and apply a community ecology framework to analyze microbiome community assembly and interactions inIxodes pacificus, the Lyme disease vector in the western United States. We find that vertical transmission routes drive population‐level patterns inI. pacificusmicrobial diversity and composition, but that microbial function and overall abundance do not vary over time or between clutches. Further, we find that theI. pacificusmicrobiome is not strongly structured based on competition but assembles nonrandomly, potentially due to vector‐specific filtering processes which largely eliminate all but the dominant endosymbiont,Rickettsia. At the scale of the individualI. pacificus, we find support for a highly limited internal microbial community, and hypothesize that the tick endosymbiont may be the most important component of the vector microbiome in influencing pathogen dynamics.

     
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  7. Abstract

    Vector‐borne diseases (VBDs) are embedded within complex socio‐ecological systems. While research has traditionally focused on the direct effects of VBDs on human morbidity and mortality, it is increasingly clear that their impacts are much more pervasive. VBDs are dynamically linked to feedbacks between environmental conditions, vector ecology, disease burden, and societal responses that drive transmission. As a result, VBDs have had profound influence on human history. Mechanisms include: (1) killing or debilitating large numbers of people, with demographic and population‐level impacts; (2) differentially affecting populations based on prior history of disease exposure, immunity, and resistance; (3) being weaponised to promote or justify hierarchies of power, colonialism, racism, classism and sexism; (4) catalysing changes in ideas, institutions, infrastructure, technologies and social practices in efforts to control disease outbreaks; and (5) changing human relationships with the land and environment. We use historical and archaeological evidence interpreted through an ecological lens to illustrate how VBDs have shaped society and culture, focusing on case studies from four pertinent VBDs: plague, malaria, yellow fever and trypanosomiasis. By comparing across diseases, time periods and geographies, we highlight the enormous scope and variety of mechanisms by which VBDs have influenced human history.

     
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