Molecular and niche modeling approaches to identify potential amplifying hosts for an emerging tick-borne pathogen, Rickettsia rickettsii subsp. californica, the causative agent of Pacific Coast tick fever

Pacific Coast tick fever (PCTF) is a recently described zoonotic disease in California caused by a spotted fever group rickettsia (SFGR), Rickettsia rickettsii subsp. californica (formerly Rickettsia 364D) and transmitted by the Pacific Coast tick, Dermacentor occidentalis. Like many emerging vector-borne diseases, knowledge regarding the transmission cycle, contribution from potential amplifying hosts, and geographic distribution of R. rickettsii californica is limited. We paired molecular analysis with comparative spatial niche modeling to identify vertebrate hosts potentially involved the transmission cycle of this pathogen. We identified R. rickettsii californica DNA in three mammal species (Otospermophilus beecheyi, Lepus californicus, and Sylvilagus audubonii). This is the first record of R. rickettsii californica detected in mammals and may indicate potential amplifying hosts for this human pathogen. Species niche modeling of uninfected and infected D. occidentalis identified areas of high suitability along the coast and Sierra Nevada foothills of California. These findings support the hypothesis that amplifying host(s) may support higher infection prevalence in the infected tick regions compared to other parts of the tick’s range. Potential host species distribution models (SDM) were constructed from museum records and niche overlap statistics were used to compare habitat suitability with R. rickettsii californica-infected tick SDMs. We found higher than null overlap of infected ticks with California ground squirrels (O. beecheyii) and trending, but non-significant, overlap with two lagomorph species. Pairing molecular and niche modeling may be a useful approach to identify species that are involved in the maintenance of emerging tick-borne zoonoses.

Methods
Pathogen and host species distribution models

Species distribution models (SDM) for all D. occidentalis as well as infected D. occidentalis occurrences were generated using tick occurrence records and R. rickettsii californica infection status gathered from published studies and CDPH records (Paddock et al. 2018; Padgett et al. 2016). We georeferenced CDPH records based on zip code and county metadata associated with the tick samples by joining CDPH tick occurrence records with a 1999 US Census Bureau zip code gazetteer (Schuyler 2004). Mammal occurrence records were obtained through the VertNet database (http://vertnet.org) and observations that were not connected to an existing museum specimen were removed (California Academy of Sciences, UCLA-Dickey Bird and Mammal Collection, Field Museum of Natural History, Los Angeles County Museum, Museum of Vertebrate Zoology, Royal Ontario Museum, University of Kansas Biodiversity Institute, Yale Peabody Museum). For N. fuscipes, we used the occurrence records provided by a recent study which refined subspecies designations in museum records (Boria et al. 2020). We reduced sampling bias associated with collection data by spatially filtering occurrence points that were within a 5km radius of each other, due to the high spatial heterogeneity of California (Rissler et al, 2006),  using ENMTools (Warren et al. 2021) and spThin (Aiello-Lammens et al. 2015) in R (v4.0.4).