Spatial and temporal factors affecting parasite genotypes encountered by hosts: Empirical data from American dog ticks (Dermacentor variabilis) parasitising raccoons (Procyon lotor)

The American dog tick (Dermacentor variabilis) is an important vector of numerous pathogens of humans and animals. In this study, we analysed population genetic patterns in D. variabilis at scales of the host individual (infrapopulation) and population (component population) to elucidate fine-scale spatial and temporal factors influencing transmission dynamics. We genotyped D. variabilis collected from raccoons (Procyon lotor) trapped in two habitat patches (located in Indiana, USA) which were spatially proximate (5.9 km) and limited in size (10.48 Ha and 25.47 Ha, respectively). Despite the fine spatial sampling scale, our analyses revealed significant genetic differentiation amongst component populations and infrapopulations (within each component population), indicating a non-random pattern of encountering tick genotypes by raccoons at both scales evaluated. We found evidence for male-biased dispersal in the ticks themselves (in one component population) and an age-bias in spatial scales at which raccoons encountered ticks in the environment. At the scale of the component population, our analyses revealed that raccoons encountered ticks from a limited number of D. variabilis family groups, likely due to high reproductive variance amongst individual ticks. Finally, we found evidence for a temporal effect with raccoons encountering ticks in the environment as “clumps” of related individuals. While the genetic structure of parasite populations are increasingly being investigated at small spatial scales (e.g. the infrapopulation), our data reveal that genetic structuring can originate at scales below that of the infrapopulation, due to the interaction between temporal and biological factors affecting the encounter of parasites by individual hosts. Ultimately, our data indicate that genetic structure in parasites must be viewed as a consequence of both spatial and temporal variance in host-parasite interactions, which in turn are driven by demographic factors related to both the host and parasite.     

Dispersal and distribution of the tick Ixodes uriae within and among seabird host populations: the need for a population genetic approach

The aim of this study was to characterize the spatial distribution of the tick Ixodes uriae within and among populations of its seabird hosts and to consider the potential insight that could be gained by a population genetic approach to the issue of dispersal of this tick. Analyses of data collected around the Avalon Peninsula, Newfoundland, indicated that both the prevalence and mean abundance of ticks varied significantly among sample locations. Whereas ticks were found on all 4 host species examined (Rissa tridactyla, Uria aalge, Alca torda, Fratercula arctica), infestation prevalence and mean abundance differed among the species. On R. tridactyla, ticks were significantly aggregated at the among-nest scale and nestling infestation was spatially autocorrelated. Conversely, ticks were not aggregated among chicks within nests. These results enabled us to make a priori predictions regarding tick dispersal and host specificity and suggest there may be spatial structure of Ixodes uriae populations at both macro- and microgeographic scales. Investigating the population genetic structure of ticks within and among populations of hosts with different breeding biologies should provide direct insight into the metapopulation dynamics of such a spatially structured system.     

History and structure of sub-Saharan populations of Drosophila melanogaster

Drosophila melanogaster is an important model organism in evolutionary genetics, yet little is known about the population structure and the demographic history of this species within sub-Saharan Africa, which is thought to contain its ancestral range. We surveyed nucleotide variation at four 1-kb fragments in 240 individual lines representing 21 sub-Saharan and 4 Palearctic population samples of D. melanogaster. In agreement with recent studies, we find a small but significant level of genetic differentiation within sub-Saharan Africa. A clear geographic pattern is observed, with eastern and western African populations composing two genetically distinct groups. This pattern may have resulted from a relatively recent establishment of D. melanogaster in western Africa. Eastern populations show greater evidence for long-term stability, consistent with the hypothesis that eastern Africa contains the ancestral range of the species. Three sub-Saharan populations show evidence for cosmopolitan introgression. Apart from those cases, the closest relationships between Palearctic and sub-Saharan populations involve a sample from the rift zone (Uganda), suggesting that the progenitors of Palearctic D. melanogaster might have come from this region. Finally, we find a large excess of singleton polymorphisms in the full data set, which is best explained by a combination of population growth and purifying selection.     

Climate of origin affects tick (Ixodes ricinus) host-seeking behavior in response to temperature: implications for resilience to climate change?

Climate warming is changing distributions and phenologies of many organisms and may also impact on vectors of disease-causing pathogens. In Europe, the tick Ixodes ricinus is the primary vector of medically important pathogens (e.g., Borrelia burgdorferi sensu lato, the causative agent of Lyme borreliosis). How might climate change affect I. ricinus host-seeking behavior (questing)? We hypothesize that, in order to maximize survival, I. ricinus have adapted their questing in response to temperature in accordance with local climates. We predicted that ticks from cooler climates quest at cooler temperatures than those from warmer climates. This would suggest that I. ricinus can adapt and therefore have the potential to be resilient to climate change. I. ricinus were collected from a cline of climates using a latitudinal gradient (northeast Scotland, North Wales, South England, and central France). Under laboratory conditions, ticks were subjected to temperature increases of 1°C per day, from 6 to 15°C. The proportion of ticks questing was recorded five times per temperature (i.e., per day). The theoretical potential to quest was then estimated for each population over the year for future climate change projections. As predicted, more ticks from cooler climates quested at lower temperatures than did ticks from warmer climates. The proportion of ticks questing was strongly associated with key climate parameters from each location. Our projections, based on temperature alone, suggested that populations could advance their activity season by a month under climate change, which has implications for exposure periods of hosts to tick-borne pathogens. Our findings suggest that I. ricinus have adapted their behavior in response to climate, implying some potential to adapt to climate change. Predictive models of I. ricinus dynamics and disease risk over continental scales would benefit from knowledge of these differences between populations.     

The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats

In Europe the most important hosts maintaining Ixodes ricinus tick populations are deer. Therefore, excluding deer by fencing or culling are potential tick management tools. Here we test the hypothesis that deer act as vehicles for moving ticks between two distinct habitats: forest and open heather moorland. We utilised an ideal “natural experiment” whereby forests were either fenced or unfenced to prevent or allow deer to move between habitats. We aimed to test the hypothesis that deer cause a net movement of ticks from high tick density areas, i.e. forests, to low tick density areas, i.e. open moorland. We recorded I. ricinus and host abundance in 10 unfenced and seven fenced forests and their respective surrounding heather moorland. We found that fenced forests had fewer deer and fewer I. ricinus nymphs than unfenced forests. However, we found no evidence that fencing forests reduced I. ricinus abundance on adjacent heather moorland. Thus there was insufficient evidence for our hypothesis that deer cause a net movement of ticks from forest onto adjacent moorland. However, we found that deer abundance generally correlates with I. ricinus abundance. We conclude that fencing can be used as a tool to reduce ticks and disease risk in forests, but that fencing forests is unlikely to reduce ticks or disease risk on adjacent moorland. Instead, reducing deer numbers could be a potential tool to reduce tick abundance with implications for disease mitigation.     

Birds are islands for parasites

Understanding the mechanisms driving the extraordinary diversification of parasites is a major challenge in evolutionary biology. Co-speciation, one proposed mechanism that could contribute to this diversity is hypothesized to result from allopatric co-divergence of host–parasite populations. We found that island populations of the Galápagos hawk (Buteo galapagoensis) and a parasitic feather louse species (Degeeriella regalis) exhibit patterns of co-divergence across variable temporal and spatial scales. Hawks and lice showed nearly identical population genetic structure across the Galápagos Islands. Hawk population genetic structure is explained by isolation by distance among islands. Louse population structure is best explained by hawk population structure, rather than isolation by distance per se, suggesting that lice tightly track the recent population histories of their hosts. Among hawk individuals, louse populations were also highly structured, suggesting that hosts serve as islands for parasites from an evolutionary perspective. Altogether, we found that host and parasite populations may have responded in the same manner to geographical isolation across spatial scales. Allopatric co-divergence is likely one important mechanism driving the diversification of parasites.     

Genetic variation of ticks (Ixodes ricinus L.) in the Lithuanian and Norwegian populations

RAPD markers were used to measure the genetic diversity of 119 individuals of Ixodes ricinus collected from Lithuania and Norway. The samples were analysed within and also between the populations. We analysed 74 loci in each of 6 populations. Our results show high levels of diversity within the populations. The percentage of polymorphic loci of the six analysed populations: Birzai, Vilnius, Kretinga, Tjore, Kjosvik and Odderoya were 68.9%, 58.1%, 78.38%, 62.2%, 44.6% and 68.9%, respectively. The percentage of polymorphic loci in the Lithuanian populations was 93.2%, and in the Norwegian populations 81.08%. The genetic distance ranged from 0.019 to 0.079 within Norwegian populations and from 0.005 to 0.0967 within Lithuanian populations and between the countries from 0.022 to 0.146. The genetic variation of I. ricinus among Norwegian populations was lower than among Lithuanian populations. The highest part of genetic variation in I. ricinus ticks depends on variation within Kretinga (Lithuania) and Odderoya (Norway) populations situated in coastal areas where many migratory and sea birds are aggregated.     

Geographic differentiation of genomic DNA of <Emphasis Type="Italic">Chironomus plumosus</Emphasis> (Diptera,Chironomidae) in natural holarctic populations

Using RAPD markers, polymorphism and differentiation of genomic DNA was examined in seven natural populations of Chironomus plumosus from Europe, Siberia, and North America. All these populations showed high polymorphism of genomic DNA. The Palearctic and Nearctic populations of this species were not statistically significantly different in the genomic DNA polymorphism level. The genetic distance (GD), which characterizes the extent of intraspecific differentiation of population genetic structure, was determined among the natural populations of C. plumosus. The genetic distance was on average 0.245. It was demonstrated that genetic structures of the Palearctic and Nearctic populations of C. plumosus was differentiated to a higher extent than in Palearctic. However, the genetic distances between the populations from different zoogeographical zones (0.313) did not exceed the level characteristic of the among-population differences, which do not disturb the species genetic integrity.     

Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races

Abstract Despite the fact that parasite dispersal is likely to be one of the most important processes influencing the dynamics and coevolution of host-parasite interactions, little information is available on the factors that affect it. In most cases, opportunities for parasite dispersal should be closely linked to host biology. Here we use microsatellite genetic markers to compare the population structure and dispersal of two host races of the seabird tick Ixodes uriae at the scale of the North Atlantic. Interestingly, tick populations showed high within-population genetic variation and relatively low population differentiation. However, gene flow at different spatial scales seemed to depend on the host species exploited. The black-legged kittiwake ( Rissa tridactyla ) had structured tick populations showing patterns of isolation by distance, whereas tick populations of the Atlantic puffin ( Fratercula arctica ) were only weakly structured at the largest scale considered. Host-dependent rates of tick dispersal between colonies will alter infestation probabilities and local dynamics and may thus modify the adaptation potential of ticks to local hosts. Moreover, as I. uriae is a vector of the Lyme disease agent Borrelia burgdorferi sensu lato in both hemispheres, the large-scale movements of birds and the subsequent dispersal of ticks will have important consequences for the dynamics and coevolutionary interactions of this microparasite with its different vertebrate and invertebrate hosts.     

Monitoring the diel activity of Ixodes ricinus ticks in Hungary over three seasons

Ixodes ricinus is the most common tick species in Europe and vector of many diseases of humans. The risk of contracting such a disease is influenced by many factors, but one of the crucial points is questing activity of unfed ticks. In order to supplement the few literature data on patterns of diel activity of this tick species and to examine the correlations between data on diel activity of ticks and their small mammal hosts and some meteorological variables, a survey was performed. Diel activity of questing I. ricinus and small rodents was studied in a known natural tick-borne encephalitis virus focus over 7 months at one sampling day monthly. 1,063 I. ricinus ticks and 25 rodents were sampled. Air temperature and humidity data were also recorded in the 24 study plots at time of sampling. From April to October questing activity of nymphs increased in the 3-h-period after sunrise, comparing to activity of the 3 h before sunrise. Proportion of nymphs sampled 3 h after sunset compared to total sampled nymphs 3 h before and 3 h after sunset showed correlation to activity of rodents. In the period of April–July both nymphs and larvae showed stronger activity from sunrise to sunset, this turned to dominant nighttime activity in August–September, whereas activity changed to equal in day and night in October. Our results indicate that natural light and rodent population have positive effect on questing activity of I. ricinus.     

Demography and population models of ticks of the genus Ixodes with long-term life cycles

The most important parameters necessary for creation of population models for three-host species with long-term life cycles are discussed by the example of the ticks Ixodes persulcatus and I. ricinus. In these species, specimens of the same biological age may belong to different age cohorts and their calendar age may differ by several months or even years. Accurate estimation of the calendar age of singular individuals is difficult; it is based on the extrapolation by its possible biological age and by belonging to the certain age cohort of a natural population. In order to possess a prognostic value, the population models must predict a single-moment population density of activated hungry specimens of all the three developmental stages and the probability of host-finding in hungry ticks during the questing period. The daily mortality of ticks of different developmental stages and phases of each stage (questing, feeding, preparation for molting, and diapause) should also be known. The population density of questing hungry ticks in the ecosystem is determined by the balance between the recruitment of new individuals into the population, their removal from the population by hosts, the dying of ticks from starvation, and the consumption of ticks by predators. At present, unfortunately, only some of these parameters are sufficiently known.     

Rampant drift in artificially fragmented populations of the endangered tidewater goby (Eucyclogobius newberryi)

Habitat fragmentation and its genetic consequences are a critically important issue in evaluating the evolutionary penalties of human habitat modification. Here, we examine the genetic structure and diversity in naturally subdivided and artificially fragmented populations of the endangered tidewater goby (Eucyclogobius newberryi), a small fish restricted to discrete coastal lagoons and estuaries in California, USA. We use five naturally fragmented coastal populations from a 300‐ km spatial scale as a standard to assess migration and drift relative to eight artificially fragmented bay populations from a 30‐ km spatial scale. Using nine microsatellite loci in 621 individuals, and a 522‐base fragment of mitochondrial DNA control region from 103 individuals, we found striking differences in the relative influences of migration and drift on genetic variation at these two scales. Overall, the artificially fragmented populations exhibited a consistent pattern of higher genetic differentiation and significantly lower genetic diversity relative to the naturally fragmented populations. Thus, even in a species characterized by habitat isolation and subdivision, further artificial fragmentation appears to result in substantial population genetic consequences and may not be sustainable.     

Experiments on the transmission of Babesia divergens to cattle by the tick Ixodes ricinus

A modification of the method of rearing Ixodes ricinus gave a successful method of producing and reliably rearing adequate numbers of this tick for experimental work.Experiments on transmission of Babesia divergens by I. ricinus showed that infections could be initiated only in the adult stage of the tick. Whilst all stages of the F₁ generation of an infected female could transmit infection, larvae and nymphs could not acquire it. Infection persisted throughout the F₁ generation and sometimes up to the F₂ larval stage even when the ticks were maintained on hosts not susceptible to B. divergens. Both parasitaemic and premune carrier hosts were infective to ticks. A single infected adult or nymph could transmit infection.     

Lack of resistance against the tick Ixodes ricinus in two related passerine bird species

Although many wild bird species may act as reservoir hosts for tick-transmitted diseases and/or support long-distance dispersal of infected ticks, to date no research has been done on the extent to which songbirds may acquire resistance to ixodid ticks. Here we investigate whether two passerine species belonging to the family Paridae, the blue tit (Cyanistes caeruleus) and the great tit (Parus major), are able to acquire resistance after repeated infestations with Ixodes ricinus nymphs. As blue tits are less frequently exposed to I. ricinus in the wild than great tits, we expected I. ricinus to be less adapted towards the blue tit’s resistance mechanisms. Over the three infestation sessions we observed consistently high tick attachment rates and yields, high engorgement weights, and short engorgement and moulting durations, indicating that neither of the two songbird species is able to mount effective immune responses against I. ricinus nymphs after repeated infestations. As a consequence of the lack of resistance, birds were unable to prevent the direct harm (acute blood depletion) caused by tick feeding. Birds compensated the erythrocyte loss without reduction in general body condition (body mass corrected for tarsus length). The lack of resistance suggests that I. ricinus has a long co-evolutionary history with both avian hosts, which enables the tick to avoid or suppress the host’s resistance responses.     

Linking genetic and ecological differentiation in an ungulate with a circumpolar distribution

Genetic differentiation among populations may arise from the disruption of gene flow due to local adaptation to distinct environments and/or neutral accumulation of mutations and genetic drift resulted from geographical isolation. Quantifying the role of these processes in determining the genetic structure of natural populations remains challenging. Here, we analyze the relative contribution of isolation‐by‐resistance (IBR), isolation‐by‐environment (IBE), genetic drift and historical isolation in allopatry during Pleistocene glacial cycles on shaping patterns of genetic differentiation in caribou/reindeer populations Rangifer tarandus across the entire distribution range of the species. Our study integrates analyses at range‐wide and regional scales to partial out the effects of historical and contemporary isolation mechanisms. At the circumpolar scale, our results indicate that genetic differentiation is predominantly explained by IBR and historical isolation. At a regional scale, we found that IBR, IBE and population size significantly explained the spatial distribution of genetic variation among populations belonging to the Euro‐Beringian lineage within North America. In contrast, genetic differentiation among populations within the North American lineage was predominantly explained by IBR and population size, but not IBE. We also found discrepancies between genetic and ecotype designation across the Holarctic species distribution range. Overall, these results indicate that multiple isolating mechanisms have played roles in shaping the spatial distribution of genetic variation across the distribution range of a large mammal with high potential for gene flow. Considering multiple spatial scales and simultaneously testing a comprehensive suite of potential isolating mechanisms, our study contributes to understand the ecological and evolutionary processes underlying organism–landscape interactions.     

An experimental test to compare potential and realised specificity in ticks with different ecologies

The majority of studies on ecological specialisation rely on data reflecting realised specificity, without considering species’ potential specificity. Most species of ticks, a large family of hematophagous ectoparasites, have a narrow host range in nature, but it is unclear whether this is due to host-driven adaptations or other processes (such as off-host abiotic environment). We investigated the potential specificity of two tick species with contrasting ecology by infesting three avian host species that occur in the same off-host macrohabitat but are unequally infested by the ticks in nature (i.e. have contrasting realised specificity). The endophilic specialist tick Ixodes arboricola resides inside the hosts’ nest and has high realised host specificity, whereas the exophilic generalist tick I. ricinus encounters hosts in the field and has very low realised specificity. As hosts, we used great tits (frequently infested by both tick species), blackbirds (frequently infested by I. ricinus but never by I. arboricola) and great spotted woodpeckers (no ticks of either species have been reported). If realised specificity is constrained by host-driven adaptations there should be no differences between potential and realised specificity, whereas if realised specificity is constrained by other processes potential specificity and realised specificity should be different. We found that attachment rates and weight during feeding of I. arboricola were lower on blackbirds than on great tits, whereas there were no such differences for I. ricinus. No ticks of either species attached to woodpeckers. These results indicate that realised host specificity of ticks is, at least partially, constrained by host-driven adaptations. This specificity therefore strongly depends on the ticks’ encounter rates with particular host types, which are affected by the ticks’ off-host ecological requirements, behaviour and life-history characteristics.     

Large‐ and small‐scale geographic structures affecting genetic patterns across populations of an Alpine butterfly

Understanding factors influencing patterns of genetic diversity and the population genetic structure of species is of particular importance in the current era of global climate change and habitat loss. These factors include the evolutionary history of a species as well as heterogeneity in the environment it occupies, which in turn can change across time. Most studies investigating spatio‐temporal genetic patterns have focused on patterns across wide geographic areas rather than local variation, but the latter can nevertheless be important particularly in topographically complex areas. Here, we consider these issues in the Sooty Copper butterfly (Lycaena tityrus) from the European Alps, using genome‐wide SNPs identified through RADseq. We found strong genetic differentiation within the Alps with four genetic clusters, indicating western, central, and eastern refuges, and a strong reduction of genetic diversity from west to east. This reduction in diversity may suggest that the southwestern refuge was the largest one in comparison to other refuges. Also, the high genetic diversity in the west may result from (a) admixture of different western refuges, (b) more recent demographic changes, or (c) introgression of lowland L. tityrus populations. At small spatial scales, populations were structured by several landscape features and especially by high mountain ridges and large river valleys. We detected 36 outlier loci likely under altitudinal selection, including several loci related to membranes and cellular processes. We suggest that efforts to preserve alpine L. tityrus should focus on the genetically diverse populations in the western Alps, and that the dolomite populations should be treated as genetically distinct management units, since they appear to be currently more threatened than others. This study demonstrates the usefulness of SNP‐based approaches for understanding patterns of genetic diversity, gene flow, and selection in a region that is expected to be particularly vulnerable to climate change.     

Patterns of genetic diversity in the polymorphic ground snake (Sonora semiannulata)

We evaluated the genetic diversity of a snake species with color polymorphism to understand the evolutionary processes that drive genetic structure across a large geographic region. Specifically, we analyzed genetic structure of the highly polymorphic ground snake, Sonora semiannulata, (1) among populations, (2) among color morphs (3) at regional and local spatial scales, using an amplified fragment length polymorphism dataset and multiple population genetic analyses, including F_ST-based and clustering analytical techniques. Based upon these methods, we found that there was moderate to low genetic structure among populations. However, this diversity was not associated with geographic locality at either spatial scale. Similarly, we found no evidence for genetic divergence among color morphs at either spatial scale. These results suggest that despite dramatic color polymorphism, this phenotypic diversity is not a major driver of genetic diversity within or among populations of ground snakes. We suggest that there are two mechanisms that could explain existing genetic diversity in ground snakes: recent range expansion from a genetically diverse founder population and current or recent gene flow among populations. Our findings have further implications for the types of color polymorphism that may generate genetic diversity in snakes.     

Contrasting genetic variation and differentiation on Hainan Island and the Chinese mainland populations of Dacrycarpus imbricatus (Podocarpaceae)

Dacrycarpus imbricatus is a vulnerable conifer in China whose geographical distribution encompasses large island but small mainland populations, providing a framework for contrasting the patterns of population genetic composition. In this study, seven populations on Hainan Island and the Chinese mainland were sampled throughout its distribution range and assessed using ISSR. The results did not show significant differences neither in genetic variation nor in genetic differentiation between the island and the mainland populations (P > 0.05). Severe bottlenecks were identified at population, island/mainland as well as range-wide scales. A relatively high level of variation but a low degree of differentiation was revealed. Ecological and life traits were suggested to play main roles in the shaping of genetic variation pattern. Of them long generation times could have exerted a lagging effect on both the genetic variation and differentiation. Our findings may contribute to establish management practices.