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Abstract Changing climate has driven shifts in species phenology, influencing a range of ecological interactions from plant–pollinator to consumer–resource. Phenological changes in host–parasite systems have implications for pathogen transmission dynamics. The seasonal timing, or phenology, of peak larval and nymphal tick abundance is an important driver of tick‐borne pathogen prevalence through its effect on cohort‐to‐cohort transmission. Tick phenology is tightly linked to climatic factors such as temperature and humidity. Thus, variation in climate within and across regions could lead to differences in phenological patterns. These differences may explain regional variation in tick‐borne pathogen prevalence of the Lyme disease‐causingBorreliabacteria in vector populations in the United States. For example, one factor thought to contribute to high Lyme disease prevalence in ticks in the eastern United States is the asynchronous phenology of ticks there, where potentially infected nymphal ticks emerge earlier in the season than uninfected larval ticks. This allows the infected nymphal ticks to transmit the pathogen to hosts that are subsequently fed upon by the next generation of larval ticks. In contrast, in the western United States where Lyme disease prevalence is generally much lower, tick phenology is thought to be more synchronous with uninfected larvae emerging slightly before, or at the same time as, potentially infected nymphs, reducing horizontal transmission potential. Sampling larval and nymphal ticks, and their host‐feeding phenology, both across large spatial gradients and through time, is challenging, which hampers attempts to conduct detailed studies of phenology to link it with pathogen prevalence. In this study, we demonstrate through intensive within‐season sampling that the relative abundance and seasonality of larval and nymphal ticks are highly variable along a latitudinal gradient and likely reflect the variable climate in the far western United States with potential consequences for pathogen transmission. We find that feeding patterns were variable and synchronous feeding of juvenile ticks on key blood meal hosts was associated with mean temperature. By characterizing within‐season phenological patterns of the Lyme disease vector throughout a climatically heterogeneous region, we can begin to identify areas with high potential for tick‐borne disease risk and underlying mechanisms at a finer scale.
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Host blood meal identity modifies vector gene expression and competency
A vector's susceptibility and ability to transmit a pathogen—termed vector competency—determines disease outcomes, yet the ecological factors influencing tick vector competency remain largely unknown. Ixodes pacificus, the tick vector of Borrelia burgdorferi (Bb) in the western U.S., feeds on rodents, birds, and lizards. Rodents and birds are reservoirs for Bb and infect juvenile ticks, while lizards are refractory to Bb and cannot infect feeding ticks. Additionally, the lizard bloodmeal contains borreliacidal properties, clearing previously infected feeding ticks of their Bb infection. Despite I. pacificus feeding on a range of hosts, it is undetermined how the host identity of the larval bloodmeal affects future nymphal vector competency. We experimentally evaluate the influence of larval host bloodmeal on Bb acquisition by nymphal I. pacificus. Larval I. pacificus were fed on either lizards or mice and after molting, nymphs were fed on Bb-infected mice. We found that lizard-fed larvae were significantly more likely to become infected with Bb during their next bloodmeal than mouse-fed larvae. We also conducted the first RNA-seq analysis on whole-bodied I. pacificus and found significant upregulation of tick antioxidants and antimicrobial peptides in the lizard-fed group. Our results indicate that the lizard bloodmeal significantly alters vector competency and gene regulation in ticks, highlighting the importance of host bloodmeal identity in vector-borne disease transmission and upends prior notions about the role of lizards in Lyme disease community ecology.
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- PAR ID:
- 10319174
- Date Published:
- Journal Name:
- Molecular Ecology
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract BackgroundEctothermic arthropods, like ticks, are sensitive indicators of environmental changes, and their seasonality plays a critical role in the dynamics of tick-borne disease in a warming world. Juvenile tick phenology, which influences pathogen transmission, may vary across climates, with longer tick seasons in cooler climates potentially amplifying transmission. However, assessing juvenile tick phenology is challenging in arid climates because ticks spend less time seeking for blood meals (i.e. questing) due to desiccation pressures. As a result, traditional collection methods like dragging or flagging are less effective. To improve our understanding of juvenile tick seasonality across a latitudinal gradient, we examinedIxodes pacificusphenology on lizards, the primary juvenile tick host in California, and explored how climate factors influence phenological patterns. MethodsBetween 2013 and 2022, ticks were removed from 1527 lizards at 45 locations during peak tick season (March–June). Tick counts were categorized by life stage (larvae and nymphs) and linked with remotely sensed climate data, including monthly maximum temperature, specific humidity and Palmer Drought Severity Index (PDSI). Juvenile phenology metrics, including tick abundances on lizards, Julian date of peak mean abundance and temporal overlap between larval and nymphal populations, were analyzed along a latitudinal gradient. Generalized additive models (GAMs) were applied to assess climate-associated variation in juvenile abundance on lizards. ResultsMean tick abundance per lizard ranged from 0.17 to 47.21 across locations, with the highest abundance in the San Francisco Bay Area and lowest in Los Angeles, where more lizards had zero ticks attached. In the San Francisco Bay Area, peak nymphal abundance occurred 25 days earlier than peak larval abundance. Temporal overlap between larval and nymphal stages at a given location varied regionally, with northern areas showing higher overlap, possibly due to the bimodal seasonality of nymphs. We found that locations with higher temperatures and increased drought stress were linked to lower tick abundances, although the magnitude of these effects depended on regional location. ConclusionsOur study, which compiled 10 years of data, reveals significant regional variation in juvenileI. pacificusphenology across California, including differences in abundance, peak timing, and temporal overlap. These findings highlight the influence of local climate on tick seasonality, with implications for tick-borne disease dynamics in a changing climate. Graphical Abstractmore » « less
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Lyme disease is the most important vector-borne disease in the United States and is increasing in incidence and geographic range. In the Pacific west, the western black-legged tick, Ixodes pacificus Cooley and Kohls, 1943 is an important vector of the causative agent of Lyme disease, the spirochete, Borrelia burgdorferi. Ixodes pacificus life cycle is expected to be more than a year long, and all three stages (larva, nymph, and adult) overlap in spring. The optimal habitat consists of forest cover, cooler temperatures, and annual precipitation in the range of 200–500 mm. Therefore, the coastal areas of California, Oregon, and Washington are well suited for these ticks. Immature stages commonly parasitize Western fence lizards (Sceloporus occidentalis) and gray squirrels (Sciurus griseus), while adults often feed on deer mice (Peromyscus maniculatus) and black-tailed deer (Odocoileus h. columbianus). Ixodes pacificus carry several pathogens of human significance, such as Borrelia burgdorferi, Bartonella, and Rickettsiales. These pathogens are maintained in the environment by many hosts, including small mammals, birds, livestock, and domestic animals. Although a great deal of work has been carried out on Ixodes ticks and the pathogens they transmit, understanding I. pacificus ecology outside California still lags. Additionally, the dynamic vector–host–pathogen system means that new factors will continue to arise and shift the epidemiological patterns within specific areas. Here, we review the ecology of I. pacificus and the pathogens this tick is known to carry to identify gaps in our knowledge.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/mec.16413
