Data-driven predictions and novel hypotheses about zoonotic tick vectors from the genus Ixodes
Tóm tắt
With the resurgence of tick-borne diseases such as Lyme disease and the emergence of new tick-borne pathogens such as Powassan virus, understanding what distinguishes vectors from non-vectors, and predicting undiscovered tick vectors is a crucial step towards mitigating disease risk in humans. We aimed to identify intrinsic traits that predict which Ixodes tick species are confirmed or strongly suspected to be vectors of zoonotic pathogens. We focused on the well-studied tick genus Ixodes from which many species are known to transmit zoonotic diseases to humans. We apply generalized boosted regression to interrogate over 90 features for over 240 species of Ixodes ticks to learn what intrinsic features distinguish zoonotic vectors from non-vector species. In addition to better understanding the biological underpinnings of tick vectorial capacity, the model generates a per species probability of being a zoonotic vector on the basis of intrinsic biological similarity with known Ixodes vector species. Our model predicted vector status with over 91% accuracy, and identified 14 Ixodes species with high probabilities (80%) of transmitting infections from animal hosts to humans on the basis of their traits. Distinguishing characteristics of zoonotic tick vectors of Ixodes tick species include several anatomical structures that influence host seeking behavior and blood-feeding efficiency from a greater diversity of host species compared to non-vectors. Overall, these results suggest that zoonotic tick vectors are most likely to be those species where adult females hold a fecundity advantage by producing more eggs per clutch, which develop into larvae that feed on a greater diversity of host species compared to non-vector species. These larvae develop into nymphs whose anatomy are well suited for more efficient and longer feeding times on soft-bodied hosts compared to non-vectors, leading to larger adult females with greater fecundity. In addition to identifying novel, testable hypotheses about intrinsic features driving vectorial capacity across Ixodes tick species, our model identifies particular Ixodes species with the highest probability of carrying zoonotic diseases, offering specific targets for increased zoonotic investigation and surveillance.
Tài liệu tham khảo
Durden LA. Taxonomy, host associations, life cycles and vectorial importance of ticks parasitizing small mammals. In: Morand S, Krasnov BR, Poulin R, editors. Micromammals and macroparasites. Tokyo: Springer; 2006. p. 91–102. http://www.springerlink.com/index/10.1007/978-4-431-36025-4_6. Accessed 8 June 2016.
GIDEON. Global infectious diseases and epidemiology online network; 1994. http://gideononline.com. Accessed 10 Feb 2018.
Levi T, Keesing F, Oggenfuss K, Ostfeld RS. Accelerated phenology of blacklegged ticks under climate warming. Phil Trans R Soc B. 2015;370(1665):20130556.
Elith J, Leathwick JR, Hastie T. A working guide to boosted regression trees. J Anim Ecol. 2008;77:802–13.
Ridgeway G. gbm: generalized boosted regression models; 2013. http://cran.r-project.org/web/packages/gbm/index.html. Accessed 15 Aug 2013.
Hastie T, Tibshirani R, Friedman JH. The elements of statistical learning: data mining, inference, and prediction. 2nd ed. New York: Springer; 2009 (Springer Series in Statistics).
Berger SA. GIDEON: a comprehensive Web-based resource for geographic medicine. Int J Health Geogr. 2005;4:10.
Han BA, Schmidt JP, Bowden SE, Drake JM. Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci. 2015;112(22):7039–44.
Han BA, Schmidt JP, Alexander LW, Bowden SE, Hayman DTS, Drake JM. Undiscovered bat hosts of filoviruses. PLOS Negl Trop Dis. 2016;10(7):e0004815.
R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2014. http://www.R-project.org/. Accessed 10 Feb 2018.
Davies TJ, Pedersen AB. Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc R Soc B Biol Sci. 2008;275(1643):1695–701.
Woolhouse MEJ, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis. 2005;11(12):1842–7.
Matuschka FR, Fischer P, Heiler M, Blümcke S, Spielman A. Stage-associated risk of transmission of the Lyme disease spirochete by European Ixodes ticks. Parasitol Res. 1992;78(8):695–8.
Sonenshine DE, Roe RM. Biology of Ticks. Vol. 1. OUP USA; 2013. 504 p.
Richter D, Matuschka F-R, Spielman A, Mahadevan L. How ticks get under your skin: insertion mechanics of the feeding apparatus of Ixodes ricinus ticks. Proc R Soc B Biol Sci. 2013;280(1773):20131758.
Reuben Kaufman W. Ticks: physiological aspects with implications for pathogen transmission. Ticks TickBorne Dis. 2010;1(1):11–22.
Shine R. The evolution of large body size in females: a critique of Darwin’s “fecundity advantage” model. Am Nat. 1988;131(1):124–31.
Oliver JH Jr. Biology and systematics of ticks (Acari: Ixodida). Annu Rev Ecol Syst. 1989;20:397–430. https://doi.org/10.1146/annurev.es.20.110189.002145.
Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world. Dordrecht: Springer; 2014. http://link.springer.com/10.1007/978-94-007-7497-1. Accessed 8 June 2016.
Doby JM, Bigaignon G, Launay H, Costil C, Lorvellec O. Presence of Borrelia burgdorferi, agent of tick spirochaetosis, in Ixodes (Exopalpiger) trianguliceps Birula, 1895 and Ixodes (Ixodes) acuminatus Neumann, 1901 (Acari: Ixodidae) and in Ctenophthalmus baeticus arvernus Jordan, 1931 and Megabothris turbidus (Rothschild, 1909) (Insecta: Siphonaptera), ectoparasites of small mammals in forests in western France. Bull Société Fr Parasitol. 1990;8(2):311–22.
Fourie LJ, Petney TN, Horak IG, De Jager C. Seasonal incidence of Karoo paralysis in relation to the infestation density of female Ixodes rubicundus. Vet Parasitol. 1989;33(3–4):319–28.
Sezzere MC, Barry RG. Processes and impacts of arctic amplification: a research synthesis. Global Planet Change. 2011;17:85–96.
Civitello DJ, et al. Biodiversity inhibits parasites: broad evidence for the dilution effect. Proc Natl Acad Sci USA. 2015;112:8667–71.
Keesing F, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468:647–52.
Horak IG, Fourie LJ, Heyne H, Walker JB, Needham GR. Ixodid ticks feeding on humans in South Africa: with notes on preferred hosts, geographic distribution, seasonal occurrence and transmission of pathogens. Exp Appl Acarol. 2002;27:113–36.
Hillyard P. Ticks of north-west Europe—keys and notes for identification of species. Synopses of the British fauna no. 52. Field Studies Council, Shrewsbury, United Kingdom; 1996.
Piksa K, Nowak-Chmura M, Siuda K. First case of human infestation by the tick Ixodes vespertilionis (Acari: Ixodidae). Int J Acarol. 2013;39:1–2.
Salkeld DJ, Eisen RJ, Antolin MF, Stapp P, Eisen L. Host usage and seasonal activity patterns of Ixodes kingi and I. sculptus (Acari: Ixodidae) nymphs in a Colorado prairie landscape, with a summary of published North American host records for all life stages. J Vector Ecol. 2006;31:168–80.
Fedorov VG. Ixodoidea ticks on men in Western Siberia. Med Parazitol. 1968;37:615–6.
Merten HA, Durden LA. A state-by-state survey of ticks recorded from humans in the United States. J Vector Ecol. 2000;25:102–13.
Filippova NA. Ixodid ticks (Ixodinae). Fauna USSR New Ser. 4 (4). Nauka, Moscow, Leningrad; 1977.
Emchuk EM. Certain biological peculiarities of Ixodes redikorzevi Olen; 1968.
Bursali A, Keskin A, Tekin S. A review of the ticks (Acari: Ixodida) of Turkey: species diversity, hosts and geographical distribution. Exp Appl Acarol. 2012;57:91–104.