Canid hybridization: contemporary evolution in human‐modified landscapes

Contemporary evolution through human‐induced hybridization occurs throughout the taxonomic range. Formerly allopatric species appear especially susceptible to hybridization. Consequently, hybridization is expected to be more common in regions with recent sympatry owing to human activity than in areas of historical range overlap. Coyotes ( Canis latrans) and gray wolves ( C. lupus) are historically sympatric in western North America. Following European settlement gray wolf range contracted, whereas coyote range expanded to include eastern North America. Furthermore, wolves with New World (NW) mitochondrial DNA (mtDNA) haplotypes now extend from Manitoba to Québec in Canada and hybridize with gray wolves and coyotes. Using mtDNA and 12 microsatellite markers, we evaluated levels of wolf‐coyote hybridization in regions where coyotes were present (the Canadian Prairies, n = 109 samples) and absent historically (Québec, n = 154). Wolves with NW mtDNA extended from central Saskatchewan (51°N, 69°W) to northeastern Québec (54°N, 108°W). On the Prairies, 6.3% of coyotes and 9.2% of wolves had genetic profiles suggesting wolf‐coyote hybridization. In contrast, 12.6% of coyotes and 37.4% of wolves in Québec had profiles indicating hybrid origin. Wolves with NW and Old World ( C. lupus) mtDNA appear to form integrated populations in both regions. Our results suggest that hybridization is more frequent in historically allopatric populations. Range shifts, now expected across taxa following climate change and other human influence on the environment, might therefore promote contemporary evolution by hybridization.     

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.     

Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander

Urban development is a major cause of habitat loss and fragmentation. Few studies, however, have dealt with fragmentation in an urban landscape. In this paper, we examine the genetic structure of isolated populations of the eastern red-backed salamander (Plethodon cinereus) in a metropolitan area. We sampled four populations located on a mountain in the heart of Montréal (Québec, Canada), which presents a mosaic of forested patches isolated by roads, graveyards and buildings. We assessed the genetic structure of these populations using microsatellite loci and compared it to the genetic structure of four populations located in a continuous habitat in southern Québec. Our results indicate that allelic richness and heterozygosity are lower in the urban populations. Exact differentiation tests and pairwise F _ST also show that the populations found in the fragmented habitat are genetically differentiated, whereas populations located in the continuous habitat are genetically homogeneous. These results raise conservation concerns for these populations as well as for rare or threatened species inhabiting urban landscapes.     

Feeding of Ticks on Animals for Transmission and Xenodiagnosis in Lyme Disease Research

Transmission of the etiologic agent of Lyme disease, Borrelia burgdorferi, occurs by the attachment and blood feeding of Ixodes species ticks on mammalian hosts. In nature, this zoonotic bacterial pathogen may use a variety of reservoir hosts, but the white-footed mouse (Peromyscus leucopus) is the primary reservoir for larval and nymphal ticks in North America. Humans are incidental hosts most frequently infected with B. burgdorferi by the bite of ticks in the nymphal stage. B. burgdorferi adapts to its hosts throughout the enzootic cycle, so the ability to explore the functions of these spirochetes and their effects on mammalian hosts requires the use of tick feeding. In addition, the technique of xenodiagnosis (using the natural vector for detection and recovery of an infectious agent) has been useful in studies of cryptic infection. In order to obtain nymphal ticks that harbor B. burgdorferi, ticks are fed live spirochetes in culture through capillary tubes. Two animal models, mice and nonhuman primates, are most commonly used for Lyme disease studies involving tick feeding. We demonstrate the methods by which these ticks can be fed upon, and recovered from animals for either infection or xenodiagnosis.     

Effects of a zoonotic pathogen,Borrelia burgdorferi,on the behavior of a key reservoir host

Most emerging infectious diseases of humans are transmitted to humans from other animals. The transmission of these “zoonotic” pathogens is affected by the abundance and behavior of their wildlife hosts. However, the effects of infection with zoonotic pathogens on behavior of wildlife hosts, particularly those that might propagate through ecological communities, are not well understood. Borrelia burgdorferi is a bacterium that causes Lyme disease, the most common vector‐borne disease in the USA and Europe. In its North American range, the pathogen is most frequently transmitted among hosts through the bite of infected blacklegged ticks (Ixodes scapularis). Using sham and true vaccines, we experimentally manipulated infection load with this zoonotic pathogen in its most competent wildlife reservoir host, the white‐footed mouse, Peromyscus leucopus, and quantified the effects of infection on mouse foraging behavior, as well as levels of mouse infestation with ticks. Mice treated with the true vaccine had 20% fewer larval blacklegged ticks infesting them compared to mice treated with the sham vaccine, a significant difference. We observed a nonsignificant trend for mice treated with the true vaccine to be more likely to visit experimental foraging trays (20%–30% effect size) and to prey on gypsy moth pupae (5%–20% effect size) compared to mice treated with the sham vaccine. We observed no difference between mice on true‐ versus sham‐vaccinated grids in risk‐averse foraging. Infection with this zoonotic pathogen appears to elicit behavioral changes that might reduce self‐grooming, but other behaviors were affected subtly or not at all. High titers of B. burgdorferi in mice could elicit a self‐reinforcing feedback loop in which reduced grooming increases tick burdens and hence exposure to tick‐borne pathogens.     

UNCOORDINATED PHYLOGEOGRAPHY OF BORRELIA BURGDORFERI AND ITS TICK VECTOR,IXODES SCAPULARIS

Vector‐borne microbes necessarily co‐occur with their hosts and vectors, but the degree to which they share common evolutionary or biogeographic histories remains unexplored. We examine the congruity of the evolutionary and biogeographic histories of the bacterium and vector of the Lyme disease system, the most prevalent vector‐borne disease in North America. In the eastern and midwestern US, Ixodes scapularis ticks are the primary vectors of Borrelia burgdorferi, the bacterium that causes Lyme disease. Our phylogeographic and demographic analyses of the 16S mitochondrial rDNA suggest that northern I. scapularis populations originated from very few migrants from the southeastern US that expanded rapidly in the Northeast and subsequently in the Midwest after the recession of the Pleistocene ice sheets. Despite this historical gene flow, current tick migration is restricted even between proximal sites within regions. In contrast, B. burgdorferi suffers no barriers to gene flow within the northeastern and midwestern regions but shows clear interregional migration barriers. Despite the intimate association of B. burgdorferi and I. scapularis, the population structure, evolutionary history, and historical biogeography of the pathogen are all contrary to its arthropod vector. In the case of Lyme disease, movements of infected vertebrate hosts may play a larger role in the contemporary expansion and homogenization of the pathogen than the movement of tick vectors whose populations continue to bear the historical signature of climate‐induced range shifts.     

Landscape resistance and habitat combine to provide an optimal model of genetic structure and connectivity at the range margin of a small mammal

We evaluated the effect of habitat and landscape characteristics on the population genetic structure of the white‐footed mouse. We develop a new approach that uses numerical optimization to define a model that combines site differences and landscape resistance to explain the genetic differentiation between mouse populations inhabiting forest patches in southern Québec. We used ecological distance computed from resistance surfaces with Circuitscape to infer the effect of the landscape matrix on gene flow. We calculated site differences using a site index of habitat characteristics. A model that combined site differences and resistance distances explained a high proportion of the variance in genetic differentiation and outperformed models that used geographical distance alone. Urban and agriculture‐related land uses were, respectively, the most and the least resistant landscape features influencing gene flow. Our method detected the effect of rivers and highways as highly resistant linear barriers. The density of grass and shrubs on the ground best explained the variation in the site index of habitat characteristics. Our model indicates that movement of white‐footed mouse in this region is constrained along routes of low resistance. Our approach can generate models that may improve predictions of future northward range expansion of this small mammal.     

How did common ragweed (Ambrosia artemisiifolia L.) spread in Québec? A historical analysis using herbarium records

Aim To reconstruct the spread of common ragweed (Ambrosia artemisiifolia L.; Asteraceae) using herbarium specimens to document whether the habitat preferences of this plant have shifted through time. Location Southern Québec. Methods Herbarium specimens stored in the main herbaria of southern Québec were used to reconstruct the spread of common ragweed. All data (sampling location, year of sampling, habitat characteristics, etc.) were incorporated into a geographical information system. Maps indicating the spatial distribution of common ragweed were produced for four time periods. The cumulative number of locations was plotted against time to construct invasion curves. The sequence of habitats where herbarium specimens were collected was also reconstructed. Results A data base incorporating 707 common ragweed herbarium specimens was constructed for this study. The spread of common ragweed in most regions of southern Québec was initiated at the beginning of the 20th century. Herbarium specimens suggest that common ragweed first spread along river corridors. Specimens of common ragweed were not collected in agricultural fields before the mid‐1920s, nor along roads and railways before the mid‐1930s. The colonization of a large number of agricultural fields by common ragweed probably began with seed‐contaminated crops, but was certainly accelerated by the dispersal of seeds from populations growing along nearby roads. Main conclusions Herbarium specimens suggest that common ragweed has been present in southern Québec for at least 200 years, but the species was probably restricted to the Montréal area during the 19th century. It is likely that the development of the road network in Québec since the mid‐1930s significantly contributed to the spread of common ragweed. Controlling common ragweed solely in agricultural fields would not prevent the re‐infestation of crops, because roadsides would act as refuges for the weed.     

The dynamic proteome of Lyme disease Borrelia

The proteome of the spirochete bacterium Borrelia burgdorferi, the tick-borne agent of Lyme disease, has been characterized by two different approaches using mass spectrometry, providing a launching point for future studies on the dramatic changes in protein expression that occur during transmission of the bacterium between ticks and mammals.     

Aversion of the invasive Asian longhorned tick to the white-footed mouse,the dominant reservoir of tick-borne pathogens in the U.S.A.

The Asian longhorned tick (Haemaphysalis longicornis) was reported for the first time in the U.S.A. in 2017 and has now spread across 12 states. The potential of this invasive tick vector to transmit pathogens will be determined through its association to hosts, such as the white-footed mouse (Peromyscus leucopus), which is the primary reservoir for the causative agent of Lyme disease (Borrelia burgdorferi) and other zoonotic pathogens. Larval H. longicornis were placed on P. leucopus; 65% of the larvae (n = 40) moved off the host within a short period of time, and none engorged. By contrast, larval blacklegged ticks (Ixodes scapularis) did not move from where they were placed in the ear of the mouse. A laboratory behavioural assay was then conducted to assess the interaction of H. longicornis with the hair of potential mammalian host species in the U.S.A. H. longicornis larvae were significantly less likely to enter the hair zone of P. leucopus and humans compared to the hair of domestic cats, domestic dogs and white-tailed deer. This study identifies a tick–host interaction behaviour, which can be quantified in a laboratory assay to predict tick–host associations and provides insights into how ticks select a host.     

Dynamic Changes in Lyme Disease Spirochetes During Transmission by Nymphal Ticks

Ticks are not crawling needles, merely delivering infectious agents to vertebrate hosts. A sophisticated interplay takes place between ticks, pathogens, and vertebrate hosts. The relationship between Ixodes ticks and the Lyme disease spirochetes they transmit involves subtle changes in spirochete populations that maximize their chances of being transmitted. An understanding of this complex interplay will, hopefully, allow the development of new tools to block transmission of tick-borne agents. This revised version was published online in July 2006 with corrections to the Cover Date.     

Perpetuation of the Lyme Disease Spirochete Borrelia lusitaniae by Lizards

To determine whether the Lyme disease spirochete Borrelia lusitaniae is associated with lizards, we compared the prevalence and genospecies of spirochetes present in rodent- and lizard-associated ticks at a site where this spirochete frequently infects questing ticks. Whereas questing nymphal Ixodes ricinus ticks were infected mainly by Borrelia afzelii, one-half of the infected adult ticks harbored B. lusitaniae at our study site. Lyme disease spirochetes were more prevalent in sand lizards (Lacerta agilis) and common wall lizards (Podarcis muralis) than in small rodents. Although subadult ticks feeding on rodents acquired mainly B. afzelii, subadult ticks feeding on lizards became infected by B. lusitaniae. Genetic analysis confirmed that the spirochetes isolated from ticks feeding on lizards are members of the B. lusitaniae genospecies and resemble type strain PotiB2. At our central European study site, lizards, which were previously considered zooprophylactic for the agent of Lyme disease, appear to perpetuate B. lusitaniae.     

The Lyme Disease Pathogen Has No Effect on the Survival of Its Rodent Reservoir Host

Zoonotic pathogens that cause devastating morbidity and mortality in humans may be relatively harmless in their natural reservoir hosts. The tick-borne bacterium Borrelia burgdorferi causes Lyme disease in humans but few studies have investigated whether this pathogen reduces the fitness of its reservoir hosts under natural conditions. We analyzed four years of capture-mark-recapture (CMR) data on a population of white-footed mice, Peromyscus leucopus, to test whether B. burgdorferi and its tick vector affect the survival of this important reservoir host. We used a multi-state CMR approach to model mouse survival and mouse infection rates as a function of a variety of ecologically relevant explanatory factors. We found no effect of B. burgdorferi infection or tick burden on the survival of P. leucopus. Our estimates of the probability of infection varied by an order of magnitude (0.051 to 0.535) and were consistent with our understanding of Lyme disease in the Northeastern United States. B. burgdorferi establishes a chronic avirulent infection in their rodent reservoir hosts because this pathogen depends on rodent mobility to achieve transmission to its sedentary tick vector. The estimates of B. burgdorferi infection risk will facilitate future theoretical studies on the epidemiology of Lyme disease.     

Relative utilization of reptiles and rodents as hosts by immature Ixodes scapularis (Acari: Ixodidae) in the coastal plain of North Carolina,USA

The interaction of immature black-legged ticks, Ixodes scapularis, with reptiles and rodents was investigated in various woodland habitats in the coastal plain of North Carolina. Reptiles were sampled from April 1 to September 30, 1991. No ticks were found on 95 specimens representing 16 species of snakes. Ticks were found on 54 (36.7%) of 147 lizards. I. scapularis was the only tick recovered from lizards. Some lizards were collected in drift fence traps each month of the study except August. Capture rates averaged one lizard per 16 trap-days. Larvac and nymphs of I. scapularis were removed from the southeastern five-lined skink (Eumeces inexpectatus), the ground skink (Scincella lateralis), the broad-headed skink (E. laticeps) and the eastem glass lizard (Ophisaurus ventralis), but ticks were not found on three other lizard species. Tick infestation rates and loads for parasitized species are presented. Ticks were almost exlusively attached at the base or in the axils of forelimbs of skinks and in the lateral grooves of eastern glass lizards. Rodents were live-trapped at sites where lizards were sampled and at other sites from 1 July, 1990 to 30 January, 1992. Capture rates averaged one rodent per 47 trap-nights. Ticks were found on 23 (17.8%) of 129 animals inspected. Five species of rodents were examined but only four species were found to be tick-infested. In contrast to lizards, few I. scapularis were collected. Rodents, principally the white-footed mouse (Peromyscus leucopus) and cotton mouse (P. gossypinus) were most frequently infested with immature American dog ticks, Dermacentor variabilis, during winter and early spring months. Burdens of D. variabilis on these rodents averaged 0.3 ticks per rodent. Effects of the diversion of ticks from feeding on Peromyscus mice on the transmission of the Lyme disease spirochete are discussed.The use of trade names in this publication does not imply an endorsement by the North Carolina Agricultural Research Service or the College of Veterinary Medicine, North Carolina State University of the products named, nor criticism of similar ones not mentioned. Partial support for this research was provided by the U.S. Marine Corps, The Centers for Disease Control and Prevention, and the North Carolina Agricultural Research Service and College of Veterinary Medicine, North Carolina State University.     

An example of phenotypic adherence to the island rule? – Anticosti gray jays are heavier but not structurally larger than mainland conspecifics

The island rule refers to the tendency of small vertebrates to become larger when isolated on islands and the frequent dwarfing of large forms. It implies genetic control, and a necessary linkage, of size and body‐mass differences between insular and mainland populations. To examine the island rule, we compared body size and mass of gray jays (Perisoreus canadensis) on Anticosti Island, Québec, located in the Gulf of St. Lawrence, with three mainland populations (2 in Québec and 1 in Ontario). Although gray jays on Anticosti Island were ca 10% heavier, they were not structurally larger, than the three mainland populations. This suggests that Anticosti jays are not necessarily genetically distinct from mainland gray jays and that they may have achieved their greater body masses solely through packing more mass onto mainland‐sized body frames. As such, they may be the first‐known example of a proposed, purely phenotypic initial step in the adherence to the island rule by an insular population. Greater jay body mass is probably advantageous in Anticosti's high‐density, intensely competitive social environment that may have resulted from the island's lack of mammalian nest predators.     

Influence of northern limit range on genetic diversity and structure in a widespread North American tree,sugar maple (Acer saccharum Marshall)

Due to climate change, the ranges of many North American tree species are expected to shift northward. Sugar maple (Acer saccharum Marshall) reaches its northern continuous distributional limit in northeastern North America at the transition between boreal mixed‐wood and temperate deciduous forests. We hypothesized that marginal fragmented northern populations from the boreal mixed wood would have a distinct pattern of genetic structure and diversity. We analyzed variation at 18 microsatellite loci from 23 populations distributed along three latitudinal transects (west, central, and east) that encompass the continuous–discontinuous species range. Each transect was divided into two zones, continuous (temperate deciduous) and discontinuous (boreal mixed wood), based on sugar maple stand abundance. Respective positive and negative relationships were found between the distance of each population to the northern limit (D_north), and allelic richness (A_R) and population differentiation (F_ST). These relations were tested for each transect separately; the pattern (discontinuous–continuous) remained significant only for the western transect. structure analysis revealed the presence of four clusters. The most northern populations of each transect were assigned to a distinct group. Asymmetrical gene flow occurred from the southern into the four northernmost populations. Southern populations in Québec may have originated from two different postglacial migration routes. No evidence was found to validate the hypothesis that northern populations were remnants of a larger population that had migrated further north of the species range after the retreat of the ice sheet. The northernmost sugar maple populations possibly originated from long‐distance dispersal.     

Why Lyme disease is common in the northern US,but rare in the south: The roles of host choice,host-seeking behavior,and tick density

Lyme disease is common in the northeastern United States, but rare in the southeast, even though the tick vector is found in both regions. Infection prevalence of Lyme spirochetes in host-seeking ticks, an important component to the risk of Lyme disease, is also high in the northeast and northern midwest, but declines sharply in the south. As ticks must acquire Lyme spirochetes from infected vertebrate hosts, the role of wildlife species composition on Lyme disease risk has been a topic of lively academic discussion. We compared tick–vertebrate host interactions using standardized sampling methods among 8 sites scattered throughout the eastern US. Geographical trends in diversity of tick hosts are gradual and do not match the sharp decline in prevalence at southern sites, but tick–host associations show a clear shift from mammals in the north to reptiles in the south. Tick infection prevalence declines north to south largely because of high tick infestation of efficient spirochete reservoir hosts (rodents and shrews) in the north but not in the south. Minimal infestation of small mammals in the south results from strong selective attachment to lizards such as skinks (which are inefficient reservoirs for Lyme spirochetes) in the southern states. Selective host choice, along with latitudinal differences in tick host-seeking behavior and variations in tick densities, explains the geographic pattern of Lyme disease in the eastern US.

Lyme disease is common in the northeastern United States, but rare in the southeast, even though the tick vector is found in both regions. This study shows that this is largely because the tick vectors attach abundantly to rodents (which are good hosts for the Lyme bacteria) in the north, and to lizards (which are relatively poor hosts for Lyme bacteria) in the south.     

Comparative population dynamics of <Emphasis Type="Italic">Peromyscus leucopus</Emphasis> in North America: influences of climate,food, and density dependence

Temporal variation in population size is regulated by both exogenous forces and density-dependent feedbacks. Furthermore, accumulating evidence indicates that temporal and spatial variation in climate and resources can modify the strength of density dependence in animal populations. We analyzed six long-term time series estimates of Peromyscus leucopus (white-footed mouse) abundance from Kansas, Ohio, Pennsylvania, Virginia, Vermont, and Maine, USA, using the Kalman filter. Model-averaged estimates of the strength of delayed density dependence increased from west to east and from south to north. The strength of direct and delayed density dependence was positively related to the annual number of days with minimum temperature below −17.8°C. Annual population growth rates of P. leucopus at the Maine site were positively related to acorn abundance and P. leucopus populations tracked the changes in red-oak acorn abundance. The populations of P. leucopus living in northern latitudes might be more dependent on northern red oak (Quercus rubra) acorns for winter food than P. leucopus in southern latitudes. Furthermore, northern red oak trees mast every 4–5 years. Thus, longer, colder winters in northerly latitudes might result in stronger delayed density dependence in mouse populations with a shortage of winter food. Mice might simply track the acorn fluctuations in a delayed autocorrelated manner; however, delayed density dependence remained in our models for the Maine mouse populations after accounting for acorns, suggesting additional sources for delayed density dependence. Our results suggest that, in seed-eating Peromyscus, cyclicity may be regulated, in part, from low to high trophic levels. Deceased: Jerry O. Wolff     

Borrelia burgdorferi Promotes the Establishment of Babesia microti in the Northeastern United States

Babesia microti and Borrelia burgdorferi, the respective causative agents of human babesiosis and Lyme disease, are maintained in their enzootic cycles by the blacklegged tick (Ixodes scapularis) and use the white-footed mouse (Peromyscus leucopus) as primary reservoir host. The geographic range of both pathogens has expanded in the United States, but the spread of babesiosis has lagged behind that of Lyme disease. Several studies have estimated the basic reproduction number (R ₀) for B. microti to be below the threshold for persistence (<1), a finding that is inconsistent with the persistence and geographic expansion of this pathogen. We tested the hypothesis that host coinfection with B. burgdorferi increases the likelihood of B. microti transmission and establishment in new areas. We fed I. scapularis larva on P. leucopus mice that had been infected in the laboratory with B. microti and/or B. burgdorferi. We observed that coinfection in mice increases the frequency of B. microti infected ticks. To identify the ecological variables that would increase the probability of B. microti establishment in the field, we integrated our laboratory data with field data on tick burden and feeding activity in an R ₀ model. Our model predicts that high prevalence of B. burgdorferi infected mice lowers the ecological threshold for B. microti establishment, especially at sites where larval burden on P. leucopus is lower and where larvae feed simultaneously or soon after nymphs infect mice, when most of the transmission enhancement due to coinfection occurs. Our studies suggest that B. burgdorferi contributes to the emergence and expansion of B. microti and provides a model to predict the ecological factors that are sufficient for emergence of B. microti in the wild.     

A comparison of methods for sampling the deer tick,Ixodes dammini,in a Lyme disease endemic area

The purpose of this study was to compare the trapping and examining of mice, drag sampling, and CO₂-baited traps for their ability to detect the presence and abundance of immature deer ticks,Ixodes dammini, in a Lyme disease endemic area in southern New York State. Eight study sites were sampled 14 times between 28 May and 31 August by setting 49 live-traps, four CO₂-baited traps, and drag sampling 500 m². A total of 1540 nymphs and 3079 larvae was collected during the study. Drag sampling collected the most nymphs (705), while more larvae were recovered from CO₂-baited traps (1105). Comparisons among the methods showed a significant difference in the numbers of both larval and nymphal ticks collected (P<0.01). There was a positive correlation between the numbers of nymphs collected by drag sampling and CO₂-baited tick traps (r _s=0.83,P<0.05), and between the numbers of larvae collected by drag sampling and mouse trapping (r _s=0.75,P<0.05). These results suggest that drag sampling would be the single most reliable method for quantitatively sampling immatureI. dammini populations in a Lyme disease endemic area.