Outdoor worker knowledge of ticks and Lyme disease in Québec.

BACKGROUND AND AIMS: Lyme disease is a well-known occupational risk across North America caused by exposure to Borrelia burgdorferi via blacklegged ticks (Ixodes scapularis). As the geographic range of B. burgdorferi advances with the increasing distribution of blacklegged ticks, more outdoor workers are at risk of contracting Lyme disease. In this study, we examined the demography and personal perceptions of outdoor workers within one framework to better determine the overall risk for those working outdoors. METHODS AND RESULTS: We analysed outdoor worker knowledge of ticks and of behaviours that can prevent tick bites and Lyme disease. We then compared these risk perceptions of individuals across age, sex, education, and industry, as well as time spent outdoors. We tested the hypothesis that the risk perception of an individual and their knowledge of Lyme disease transmission was dependent on their demographics, experience in their job, and the region in which they spend time outdoors. We estimated a knowledge-based risk score based on individuals' answers to a questionnaire on risk perception given to voluntary participants who work outdoors. Those who had higher risk scores were more at risk. We found that knowledge-based risk scores were correlated with geographic risk levels and with the number of hours per day spent outdoors. Those who work longer hours and who work in areas with mid-level risk had higher risk scores. Those who spend more time outdoors recreationally had lower risk scores. CONCLUSIONS: Further examination and acknowledgment of the reasoning behind why these factors are affecting workers' risks must be considered to recognize that it is not necessarily demographics or geographically high-risk areas that affect an individual's risk. Workers' knowledge of these risks is affected by several variables that should be taken into consideration when implementing safety measures and awareness programs.

High-resolution environmental and host-related factors impacting questing Ixodes scapularis at their northern range edge.

The geographic range of tick populations has expanded in Canada due to climate warming and the associated poleward range shifts of their vertebrate hosts. Abiotic factors, such as temperature, precipitation, and snow, are known to directly affect tick abundance. Yet, biotic factors, such as the abundance and diversity of mammal hosts, may also alter tick abundance and consequent tick-borne disease risk. Here, we incorporated host surveillance data with high-resolution environmental data to evaluate the combined impact of abiotic and biotic factors on questing Ixodes scapularis abundance in Ontario and Quebec, Canada. High-resolution abiotic factors were derived from remote sensing satellites and meteorological towers, while biotic factors related to mammal hosts were derived from active surveillance data that we collected in the field. Generalized additive models were used to determine the relative importance of abiotic and biotic factors on questing I. scapularis abundance. Combinations of abiotic and biotic factors were identified as important drivers of abundances of questing I. scapularis. Positive and negative linear relationships were found for questing I. scapularis abundance with monthly mean precipitation and accumulated snow, but no effect was found for the relative abundance of white-footed mice. Positive relationships were also identified between questing I. scapularis abundance with monthly mean precipitation and mammal species richness. Therefore, future studies that assess I. scapularis should incorporate host surveillance data with high-resolution environmental factors to determine the key drivers impacting the abundance and geographic spread of tick populations and tick-borne pathogens.

Historical associations and spatiotemporal changes of pathogen presence in ticks in Canada: A systematic review.

BACKGROUND: Starting in the early 20th century, ticks and their pathogens have been detected during surveillance efforts in Canada. Since then, the geographic spread of tick vectors and tick-borne pathogens has steadily increased in Canada with the establishment of tick and host populations. Sentinel surveillance in Canada primarily focuses on Ixodes scapularis, which is the main vector of Borrelia burgdorferi, the bacterium causing Lyme disease. Other tick-borne pathogens, such as Anaplasma, Babesia, and Rickettsia species, have lower prevalence in Canada, but they are emerging or re-emerging in tick and host populations. AIMS/MATERIALS & METHODS: Here, we assessed the historical associations between tick vectors, hosts and pathogens and identified spatiotemporal clusters of pathogen presence in ticks in Canada using data extracted from the literature. RESULTS: Approximately one-third of ticks were infected with a pathogen, and these ticks were feeding primarily on bird and mammal hosts. B. burgdorferi was the most detected pathogen and I. scapularis harboured the greatest number of pathogens. We identified several spatial outliers of high pathogen presence in ticks in addition to five spatiotemporal clusters in southern Canada, all of which have long-established tick populations. Six spatiotemporal clusters of high pathogen presence in ticks were also identified based on surveillance method, with four clusters associated with passive surveillance and two clusters associated with active surveillance. DISCUSSION: Our review represents the first systematic assessment of the literature that identifies historical associations and spatiotemporal changes in tick-host-pathogen disease systems in Canada over broad spatial and temporal scales. CONCLUSION: As distinct spatiotemporal clusters were identified based on surveillance method, it is imperative that surveillance efforts employ standardized methods and data reporting to comprehensively assess the presence, spread and risk of tick-borne pathogens in tick and host populations.

Risky business: human-related data is lacking from Lyme disease risk models.

Used as a communicative tool for risk management, risk maps provide a service to the public, conveying information that can raise risk awareness and encourage mitigation. Several studies have utilized risk maps to determine risks associated with the distribution of Borrelia burgdorferi, the causal agent of Lyme disease in North America and Europe, as this zoonotic disease can lead to severe symptoms. This literature review focused on the use of risk maps to model distributions of B. burgdorferi and its vector, the blacklegged tick (Ixodes scapularis), in North America to compare variables used to predict these spatial models. Data were compiled from the existing literature to determine which ecological, environmental, and anthropic (i.e., human focused) variables past research has considered influential to the risk level for Lyme disease. The frequency of these variables was examined and analyzed via a non-metric multidimensional scaling analysis to compare different map elements that may categorize the risk models performed. Environmental variables were found to be the most frequently used in risk spatial models, particularly temperature. It was found that there was a significantly dissimilar distribution of variables used within map elements across studies: Map Type, Map Distributions, and Map Scale. Within these map elements, few anthropic variables were considered, particularly in studies that modeled future risk, despite the objective of these models directly or indirectly focusing on public health intervention. Without including human-related factors considering these variables within risk map models, it is difficult to determine how reliable these risk maps truly are. Future researchers may be persuaded to improve disease risk models by taking this into consideration.

Recent and rapid ecogeographical rule reversals in Northern Treeshrews.

Two of the most-studied ecogeographical rules describe patterns of body size variation within species. Bergmann's rule predicts that individuals have larger body sizes in colder climates (typically at higher latitudes), and the island rule predicts that island populations of small-bodied species average larger in size than their mainland counterparts (insular gigantism). These rules are rarely tested in conjunction or assessed across space and time simultaneously. We investigated these patterns in the Northern Treeshrew (Tupaia belangeri) using museum specimens collected across a wide spatial and temporal range. Contrary to Bergmann's rule, size increases with temperature in T. belangeri, a signal that is highly consistent across space and time. We also show that these rules are intertwined: Bergmann's rule is reversed on the mainland but holds on islands, and therefore the island rule is upheld at higher, but not lower, latitudes. Moreover, we demonstrate a rapid reversal of both rules over time. The mechanism behind these inversions remains unclear, though temperature and precipitation are significant predictors of body size. Ecogeographical rules rely on the assumption of a constant relationship between size and the factors driving its variation. Our results highlight the need to question this assumption and reevaluate these rules in the context of accelerating and uneven climate change.

Emerging Tick-Borne Pathogens in Central Canada: Recent Detections of Babesia odocoilei and Rickettsia rickettsii.

Background: The spread of emerging tick-borne pathogens has steadily increased in Canada with the widespread establishment of tick vectors and vertebrate hosts. At present, Borrelia burgdorferi, the bacterium causing Lyme disease, is the most common tick-borne pathogen in Canada and primarily transmitted by Ixodes scapularis. A low prevalence of other emerging tick-borne pathogens, such as Anaplasma phagocytophilum, Babesia species, Borrelia miyamotoi, and Francisella tularensis have also been detected through surveillance efforts in Canada. Although Rickettsia rickettsii has been historically detected in Haemaphysalis leporispalustris in Canada, the current prevalence and geographic extent of this pathogen is unknown. Material and Methods: In this study, we assessed the presence and prevalence of several emerging tick-borne pathogens in ticks and hosts collected through tick dragging and small mammal trapping in Central Canada. Results: Nested PCR testing detected three pathogen species in ticks, with Babesia odocoilei and B. burgdorferi in I. scapularis in addition to R. rickettsii in H. leporispalustris. Three pathogen species were detected in small mammals by nested PCR including B. odocoilei in Blarina brevicauda, Babesia microti in Peromyscus leucopus, and a Hepatozoon species in P. leucopus and Peromyscus maniculatus. B. burgdorferi and Babesia species were the pathogens most often detected in our samples, suggesting they are widely distributed across Central Canada. We also detected B. odocoilei and R. rickettsii beyond their known geographic distribution. Conclusions: Our results provide evidence that emerging tick-borne pathogens may be present outside defined risk areas identified by current surveillance efforts in Canada. As a result, emerging tick-borne pathogens introduced by the dispersal of infected ticks by migratory birds or maintained by hosts and vectors through cryptic transmission cycles may go undetected. More comprehensive testing including all tick life stages and additional tick-borne pathogens will help detect the spread and potential risk of emerging or re-emerging tick-borne pathogens for human and wildlife populations throughout Canada.

Genomic Signatures of Selection along a Climatic Gradient in the Northern Range Margin of the White-Footed Mouse (Peromyscus leucopus).

Identifying genetic variation involved in thermal adaptation is likely to yield insights into how species adapt to different climates. Physiological and behavioral responses associated with overwintering (e.g., torpor) are thought to serve important functions in climate adaptation. In this study, we use 2 isolated Peromyscus leucopus lineages on the northern margin of the species range to identify single nucleotide polymorphisms (SNPs) showing a strong environmental association and test for evidence of parallel evolution. We found signatures of clinal selection in each lineage, but evidence of parallelism was limited, with only 2 SNPs showing parallel allele frequencies across transects. These parallel SNPs map to a gene involved in protection against iron-dependent oxidative stress (Fxn) and to a gene with unknown function but containing a forkhead-associated domain (Fhad1). Furthermore, within transects, we find significant clinal patterns in genes enriched for functions associated with glycogen homeostasis, synaptic function, intracellular Ca2+ balance, H3 histone modification, as well as the G2/M transition of cell division. Our results are consistent with recent literature on the cellular and molecular basis of climate adaptation in small mammals and provide candidate genomic regions for further study.

A global synthesis of the small-island effect in habitat islands.

Habitat loss and fragmentation are considered to be the leading drivers of biodiversity loss. The small-island effect (SIE) can be used to predict species extinctions resulting from habitat loss and has important implications for species conservation. However, to date, no study has explicitly evaluated the prevalence of SIEs in habitat islands. Here, we compiled 90 global datasets to systematically investigate the prevalence and underlying factors determining the ubiquity of SIEs in habitat island systems. Among the 90 datasets, SIEs were unambiguously detected in 36 cases. We found significant effects of habitat island types and taxon groups on the threshold area of SIEs. The number of islands, area range, species range, island type and taxon group were key variables that determined the prevalence of SIEs. Our study demonstrates that SIEs occur in 40% of cases and thus are common in habitat islands. We conclude that conservation biologists and applied ecologists should consider the prevalence of SIEs when making management strategies in fragmented landscapes.

Rule reversal: Ecogeographical patterns of body size variation in the common treeshrew (Mammalia, Scandentia).

There are a number of ecogeographical "rules" that describe patterns of geographical variation among organisms. The island rule predicts that populations of larger mammals on islands evolve smaller mean body size than their mainland counterparts, whereas smaller-bodied mammals evolve larger size. Bergmann's rule predicts that populations of a species in colder climates (generally at higher latitudes) have larger mean body sizes than conspecifics in warmer climates (at lower latitudes). These two rules are rarely tested together and neither has been rigorously tested in treeshrews, a clade of small-bodied mammals in their own order (Scandentia) broadly distributed in mainland Southeast Asia and on islands throughout much of the Sunda Shelf. The common treeshrew, Tupaia glis, is an excellent candidate for study and was used to test these two rules simultaneously for the first time in treeshrews. This species is distributed on the Malay Peninsula and several offshore islands east, west, and south of the mainland. Using craniodental dimensions as a proxy for body size, we investigated how island size, distance from the mainland, and maximum sea depth between the mainland and the islands relate to body size of 13 insular T. glis populations while also controlling for latitude and correlation among variables. We found a strong negative effect of latitude on body size in the common treeshrew, indicating the inverse of Bergmann's rule. We did not detect any overall difference in body size between the island and mainland populations. However, there was an effect of island area and maximum sea depth on body size among island populations. Although there is a strong latitudinal effect on body size, neither Bergmann's rule nor the island rule applies to the common treeshrew. The results of our analyses demonstrate the necessity of assessing multiple variables simultaneously in studies of ecogeographical rules.

The Genetic Signature of Range Expansion in a Disease Vector-The Black-Legged Tick.

Monitoring and predicting the spread of emerging infectious diseases requires that we understand the mechanisms of range expansion by its vectors. Here, we examined spatial and temporal variation of genetic structure among 13 populations of the Lyme disease vector, the black-legged tick, in southern Quebec, where this tick species is currently expanding and Lyme disease is emerging. Our objective was to identify the primary mode of tick movement into Canada based on observed spatial and temporal genetic patterns. Upon genotyping 10 microsatellite loci from 613 tick specimens, we found multiple genetic signatures of frequent long-distance dispersal events, supporting the hypothesis that migratory birds are the primary carriers of black-legged ticks into southern Quebec. When we compared results from analyses of pairwise differences among ticks collected from 8 different sites at different years between 2011 and 2014, we found that genetic variation observed among tick individuals appeared to be better explained by collection year than sampling locality. This suggests that while cohorts of black-legged ticks can rapidly invade large areas across southern Quebec, they also appear to be undergoing frequent turnover. Finally, the amount of genetic variation in tick populations across our study area appeared to be related to their degree of establishment, with established populations displaying a lower amount of temporal genetic variation than adventitious ones. Given that Lyme disease infection risk in a region can be influenced by the relative presence of established and/or adventitious tick populations, our results are useful for understanding both the seasonality and spatial variation of Lyme disease.

Microsatellite markers reveal low frequency of natural hybridization between the white-footed mouse (Peromyscus leucopus) and deer mouse (Peromyscus maniculatus) in southern Quebec, Canada.

In some parts of southern Quebec, two closely related rodent species - the white-footed mouse (Peromyscus leucopus) and the deer mouse (Peromyscus maniculatus) - have recently come in contact because of climate-driven changes in the distribution of the former. Both species share similar morphology, ecology, and life history traits, which suggests that natural hybridization may be possible. Hybridization among these two species can have important implications on the ecological roles these rodents play in disease transmission, yet few researchers have attempted to examine this phenomenon and results from previous hybridization experiments have remained inconclusive and conflicting. In this study, we attempt to investigate the occurrence of hybridization among white-footed mice and deer mice in southern Quebec by genotyping wild caught specimens with selectively neutral, polymorphic microsatellite markers. Our analyses suggest that hybridization may be occurring at extremely low frequency between both species in our study area. The presence of such hybridization events, even at low frequencies, may have implications on disease transmission risk in the region and further detailed studies are necessary.

Multi-taxa integrated landscape genetics for zoonotic infectious diseases: deciphering variables influencing disease emergence.

Zoonotic disease transmission systems involve sets of species interacting with each other and their environment. This complexity impedes development of disease monitoring and control programs that require reliable identification of spatial and biotic variables and mechanisms facilitating disease emergence. To overcome this difficulty, we propose a framework that simultaneously examines all species involved in disease emergence by integrating concepts and methods from population genetics, landscape ecology, and spatial statistics. Multi-taxa integrated landscape genetics (MTILG) can reveal how interspecific interactions and landscape variables influence disease emergence patterns. We test the potential of our MTILG-based framework by modelling the emergence of a disease system across multiple species dispersal, interspecific interaction, and landscape scenarios. Our simulations showed that both interspecific-dependent dispersal patterns and landscape characteristics significantly influenced disease spread. Using our framework, we were able to detect statistically similar inter-population genetic differences and highly correlated spatial genetic patterns that imply species-dependent dispersal. Additionally, species that were assigned coupled-dispersal patterns were affected to the same degree by similar landscape variables. This study underlines the importance of an integrated approach to investigating emergence of disease systems. MTILG is a robust approach for such studies and can identify potential avenues for targeted disease management strategies.

Phylogeographic Structure of the White-Footed Mouse and the Deer Mouse, Two Lyme Disease Reservoir Hosts in Québec.

Modification of a species range is one of many consequences of climate change and is driving the emergence of Lyme disease in eastern Canada. The primary reservoir host of the bacteria responsible for Lyme disease, Borrelia burgdorferi, is the white-footed mouse (Peromyscus leucopus), whose range is rapidly shifting north into southern Québec. The deer mouse, P. maniculatus, is occurring over most Québec province and is a less competent host for B. burgdorferi. Here, we compared the phylogeographic structure of both Peromyscus species in Québec. Using a combination of multiple mitochondrial DNA markers and phylogeographic methods, we detected an ongoing and rapid expansion of P. leucopus, while P. maniculatus appears more stable. Haplotype and populations networks indicated that populations of P. maniculatus exhibit more genetic structure than P. leucopus across the study area. Furthermore, significant and consistent genetic divergences between populations of the two species on both sides of the St. Lawrence River suggest that distinct lineages of P. leucopus and P. maniculatus with different ancestral origins colonized Southern Québec following the Last Glacial Maximum. The phylogeographic structure of pathogens is expected to mirror the structure observed in their reservoir hosts. As different strains of Borrelia burgdorferi may be associated with different levels of pathogenicity and immune responses of their hosts, our results are helpful at better understanding the pattern of spread of Lyme disease in a zone of emergence, and associated risk for human populations.

Climate change and habitat fragmentation drive the occurrence of Borrelia burgdorferi, the agent of Lyme disease, at the northeastern limit of its distribution.

Lyme borreliosis is rapidly emerging in Canada, and climate change is likely a key driver of the northern spread of the disease in North America. We used field and modeling approaches to predict the risk of occurrence of Borrelia burgdorferi, the bacteria causing Lyme disease in North America. We combined climatic and landscape variables to model the current and future (2050) potential distribution of the black-legged tick and the white-footed mouse at the northeastern range limit of Lyme disease and estimated a risk index for B. burgdorferi from these distributions. The risk index was mostly constrained by the distribution of the white-footed mouse, driven by winter climatic conditions. The next factor contributing to the risk index was the distribution of the black-legged tick, estimated from the temperature. Landscape variables such as forest habitat and connectivity contributed little to the risk index. We predict a further northern expansion of B. burgdorferi of approximately 250-500 km by 2050 - a rate of 3.5-11 km per year - and identify areas of rapid rise in the risk of occurrence of B. burgdorferi. Our results will improve understanding of the spread of Lyme disease and inform management strategies at the most northern limit of its distribution.

Applying evolutionary concepts to wildlife disease ecology and management.

Existing and emerging infectious diseases are among the most pressing global threats to biodiversity, food safety and human health. The complex interplay between host, pathogen and environment creates a challenge for conserving species, communities and ecosystem functions, while mediating the many known ecological and socio-economic negative effects of disease. Despite the clear ecological and evolutionary contexts of host-pathogen dynamics, approaches to managing wildlife disease remain predominantly reactionary, focusing on surveillance and some attempts at eradication. A few exceptional studies have heeded recent calls for better integration of ecological concepts in the study and management of wildlife disease; however, evolutionary concepts remain underused. Applied evolution consists of four principles: evolutionary history, genetic and phenotypic variation, selection and eco-evolutionary dynamics. In this article, we first update a classical framework for understanding wildlife disease to integrate better these principles. Within this framework, we explore the evolutionary implications of environment-disease interactions. Subsequently, we synthesize areas where applied evolution can be employed in wildlife disease management. Finally, we discuss some future directions and challenges. Here, we underscore that despite some evolutionary principles currently playing an important role in our understanding of disease in wild animals, considerable opportunities remain for fostering the practice of evolutionarily enlightened wildlife disease management.

Climate warming and Bergmann's rule through time: is there any evidence?

Climate change is expected to induce many ecological and evolutionary changes. Among these is the hypothesis that climate warming will cause a reduction in body size. This hypothesis stems from Bergmann's rule, a trend whereby species exhibit a smaller body size in warmer climates, and larger body size under colder conditions in endotherms. The mechanisms behind this rule are still debated, and it is not clear whether Bergmann's rule can be extended to predict the effects of climate change through time. We reviewed the primary literature for evidence (i) of a decrease in body size in response to climate warming, (ii) that changing body size is an adaptive response and (iii) that these responses are evolutionary or plastic. We found weak evidence for changes in body size through time as predicted by Bergmann's rule. Only three studies investigated the adaptive nature of these size decreases. Of these, none reported evidence of selection for smaller size or of a genetic basis for the size change, suggesting that size decreases could be due to nonadaptive plasticity in response to changing environmental conditions. More studies are needed before firm conclusions can be drawn about the underlying causes of these changes in body size in response to a warming climate.

Congruent morphological and genetic differentiation as a signature of range expansion in a fragmented landscape.

Phenotypic differentiation is often interpreted as a result of local adaptation of individuals to their environment. Here, we investigated the skull morphological differentiation in 11 populations of the white-footed mouse (Peromyscus leucopus). These populations were sampled in an agricultural landscape in the Montérégie region (Québec, Canada), at the northern edge of the distribution of the white-footed mouse. We found a strong pattern of phenotypic differentiation matching the genetic structure across these populations. Landscape fragmentation and the presence of geographic barriers, in particular north-south oriented rivers, contribute to this differentiation and modulate the pattern of rapid ongoing northward range expansion of the white-footed mouse in response to climate warming. We conclude that while large rivers and postglacial recolonization routes have shaped the current pattern of distribution and differentiation of white-footed mouse populations, further local differentiation is occurring, at the scale of the landscape. We posit that the northern expansion of the white-footed mouse is achieved through successive independent founder events in a fragmented landscape at the northern range edge of the species. The phenotypic differentiation we observe is thus a result of a number of mechanisms operating at different spatial and temporal scales.

Poleward expansion of the white-footed mouse (Peromyscus leucopus) under climate change: implications for the spread of lyme disease.

The white-footed mouse (Peromyscus leucopus) is an important reservoir host for Borrelia burgdorferi, the pathogen responsible for Lyme disease, and its distribution is expanding northward. We used an Ecological Niche Factor Analysis to identify the climatic factors associated with the distribution shift of the white-footed mouse over the last 30 years at the northern edge of its range, and modeled its current and potential future (2050) distributions using the platform BIOMOD. A mild and shorter winter is favouring the northern expansion of the white-footed mouse in Québec. With more favorable winter conditions projected by 2050, the distribution range of the white-footed mouse is expected to expand further northward by 3° latitude. We also show that today in southern Québec, the occurrence of B. burgdorferi is associated with high probability of presence of the white-footed mouse. Changes in the distribution of the white-footed mouse will likely alter the geographical range of B. burgdorferi and impact the public health in northern regions that have yet to be exposed to Lyme disease.

Genetic structure of the white-footed mouse in the context of the emergence of Lyme disease in southern Québec.

The white-footed mouse (Peromyscus leucopus) has expanded its northern limit into southern Québec over the last few decades. P. leucopus is a great disperser and colonizer and is of particular interest because it is considered a primary reservoir for the spirochete bacterium that causes Lyme disease. There is no current information on the gene flow between mouse populations on the mountains and forest fragments found scattered throughout the Montérégie region in southern Québec, and whether various landscape barriers have an effect on their dispersal. We conducted a population genetics analysis on eleven P. leucopus populations using eleven microsatellite markers and showed that isolation by distance was weak, yet barriers were effective. The agricultural matrix had the least effect on gene flow, whereas highways and main rivers were effective barriers. The abundance of ticks collected from mice varied within the study area. Both ticks and mice were screened for the presence of the spirochete bacterium Borrelia burgdorferi, and we predicted areas of greater risk for Lyme disease. Merging our results with ongoing Lyme disease surveillance programs will help determine the future threat of this disease in Québec, and will contribute toward disease prevention and management strategies throughout fragmented landscapes in southern Canada.

Mammals evolve faster on smaller islands.

Island mammals often display remarkable evolutionary changes in size and morphology. Both theory and empirical data support the hypothesis that island mammals evolve at faster rates than their mainland congeners. It is also often assumed that the island effect is stronger and that evolution is faster on the smallest islands. I used a dataset assembled from the literature to test these assumptions for the first time. I show that mammals on smaller islands do indeed evolve more rapidly than mammals on larger islands, and also evolve by a greater amount. These results fit well the theory of an evolutionary burst due to the opening of new ecological opportunities on islands. This evolutionary burst is expected to be the strongest on the smallest islands where the contrast between the island and the mainland environments is the most dramatic.