Ticks are obligate, bloodsucking, nonpermanent ectoparasitic arthropods. Among them, Ixodes ricinus is a classic example of an extreme generalist tick, presenting a highly permissive feeding behavior using different groups of vertebrates as hosts, such as mammalian (including humans), avian and reptilian species (Hoogstraal & Aeschlimann, 1982; Dantas-Torresa & Otranto, 2013). This ecological adaptation can account for the broad geographical distribution of I. ricinus populations, which extends from the western end of the European continent to the Ural Mountains in Russia, and from northern Norway to the Mediterranean basin, including the North African countries - Morocco, Algeria and Tunisia (https://ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/tick-maps). The contact with different hosts also promotes the exposure/acquisition and transmission of various pathogenic agents (viruses, bacteriae, protists and nematodes) of veterinary and medical relevance (Aeschlimann et al., 1979). As one of the prime ticks found on humans, this species is implicated in diseases such as Lyme borreliosis, Spotted Fever Group rickettsiosis, Human Anaplasmosis, Human Babesiosis and Tick-borne Encephalitis (Velez et al., 2023). 

The climate change projections drawn for I. ricinus, in the scenario of global warming, point for the expansion/increase activity in both latitude and altitude (Medlock et al., 2013). The adequacy of vector modeling is relaying in the proper characterization of complex biological systems. Thus, it is essential to increase knowledge on I. ricinus, focusing on aspects such as genetic background, ecology and eco-epidemiology on a microscale but also at a country and region level, due to possible local adaptations of tick populations and genetic drift. 

In the present systematic revision, Perez et al. (2023) combine old and recently published data (mostly up to 2020) regarding I. ricinus distribution, phenology, host range and pathogen association in continental France and Corsica Island. Based on a keyword search of peer-reviewed papers on seven databases, as well as other sources of grey literature (mostly, thesis), the authors have synthesized information on: 1) Host parasitism to detect potential differences in host use comparing to other areas in Europe; 2) The spatiotemporal distribution of I. ricinus, to identify possible geographic trends in tick density, variation in activity patterns and the influence of environmental factors; 3) Tick-borne pathogens detected in this species, to better assess their spatial distribution and variation in exposure risk. 

As pointed out by both reviewers, this work clearly summarizes the information regarding I. ricinus and associated microorganisms from European France. This review also identifies remaining knowledge gaps, providing a comparable basis to orient future research. This is why I chose to recommend Perez et al (2023)'s preprint for Peer Community Infections. 

REFERENCES

Aeschlimann, A., Burgdorfer, W., Matile, H., Peter, O., Wyler, R. (1979) Aspects nouveaux du rôle de vecteur joué par Ixodes ricinus L. en Suisse. Acta Tropica, 36, 181-191.

Dantas-Torresa, F., Otranto, D. (2013) Seasonal dynamics of Ixodes ricinus on ground level and higher vegetation in a preserved wooded area in southern Europe. Veterinary Parasitology, 192, 253- 258.
https://doi.org/10.1016/j.vetpar.2012.09.034

Hoogstraal, H., Aeschlimann, A. (1982) Tick-host specificity. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 55, 5-32.

Medlock, J.M., Hansford, K.M., Bormane, A., Derdakova, M., Estrada-Peña, A., George, J.C., Golovljova, I., Jaenson, T.G.T., Jensen, J.K., Jensen, P.M., Kazimirova, M., Oteo, J.A., Papa, A., Pfister, K., Plantard, O., Randolph, S.E., Rizzoli, A., Santos-Silva, M.M., Sprong, H., Vial, L., Hendrickx, G., Zeller, H., Van Bortel, W. (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites and Vectors, 6. https://doi.org/10.1186/1756-3305-6-1

Perez, G., Bournez, L., Boulanger, N., Fite, J., Livoreil, B., McCoy, K., Quillery, E., René-Martellet, M., Bonnet, S. (2023) The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review. bioRxiv, ver. 1 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.04.18.537315

Velez, R., De Meeûs, T., Beati, L., Younsi, H., Zhioua, E., Antunes, S., Domingos, A., Ataíde Sampaio, D., Carpinteiro, D., Moerbeck, L., Estrada-Peña, A., Santos-Silva, M.M., Santos, A.S. (2023) Development and testing of microsatellite loci for the study of population genetics of Ixodes ricinus Linnaeus, 1758 and Ixodes inopinatus Estrada-Peña, Nava & Petney, 2014 (Acari: Ixodidae) in the western Mediterranean region. Acarologia, 63, 356-372. https://doi.org/10.24349/bvem-4h49

​​Diptera-borne pathogens rank among the most serious health threats to vertebrate organisms around the world, particularly in tropical areas undergoing strong human impacts – e.g., urbanization and farming –, where social unrest and poor economies exacerbate the risk (Allen et al. 2017; Robles-Fernández et al. 2022). Although scientists have acquired a detailed knowledge on the life-history of malaria parasites (Pacheco and Escalante 2023), they still do not have enough information about their insect vectors to make informed management and preventive decisions (Santiago-Alarcon 2022).

In this sense, I am pleased to recommend the study of Vantaux et al. (2023), where authors conducted an experimental and theoretical study to analyzed how the diversity of blood sources (i.e., human, cattle, sheep, and chicken) affected the fitness of the human malaria parasite – Plasmodium falciparum – and its mosquito vector – Anopheles gambiae s.l.

The study was conducted in Burkina Faso, West Africa. Interestingly, authors did not find a significant effect of blood meal source on parasite development, and a seemingly low impact on the fitness of mosquitoes that were exposed to parasites. However, mosquitoes’ feeding rate, survival, fecundity, and offspring size were negatively affected by the type of blood meal ingested. In general, chicken blood represented the worst meal source for the different measures of mosquito fitness, and sheep blood seems to be the least harmful. This result was supported by the theoretical model, where vectorial capacity was always better when mosquitoes fed on sheep blood compared to cow and chicken blood. Thus, the knowledge generated by this study provides a pathway to reduce human infection risk by managing the diversity of farm animals. For instance, transmission to humans can decrease when chickens and cows represent most of the available blood sources in a village.

These results along with other interesting details of this study, represent a clear example of the knowledge and understanding of insect vectors that we need to produce in the future, particularly to manage and prevent hazards and risks (sensu Hoseini et al. 2017).

REFERENCES

Allen T., et al., Global hotspots and correlates of emerging zoonotic diseases. Nat. Commun. 8, 1124. (2017). https://doi.org/10.1038/s41467-017-00923-8

Hosseini P.R., et al., Does the impact of biodiversity differ between emerging and endemic pathogens? The need to separate the concepts of hazard and risk. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160129 (2017). https://doi.org/10.1098/rstb.2016.0129

Pacheco M.A., and Escalante, A.A., Origin and diversity of malaria parasites and other Haemosporida. Trend. Parasitol. (2023) https://doi.org/10.1016/j.pt.2023.04.004

Robles-Fernández A., et al., Wildlife susceptibility to infectious diseases at global scales. PNAS 119: e2122851119. (2022). https://doi.org/10.1073/pnas.2122851119

Santiago-Alarcon D. A meta-analytic approach to investigate mosquitoes’ (Diptera: Culicidae) blood feeding preferences from non-urban to urban environments. In: Ecology and Control of Vector-borne Diseases, vol. 7 (R.G. Gutiérrez-López, J.G. Logan, Martínez-de la Puente J., Eds). Pp. 161-177. Wageningen Academic Publishers. eISBN: 978-90-8686-931-2 | ISBN: 978-90-8686-379-2 (2022).

Vantaux A. et al. Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Infections (2023). https://doi.org/10.1101/2023.02.10.527988

Worldwide, ticks and tick-borne diseases are a persistent example of problems at the One Health interface between humans, wildlife, and environment (1, 2). The management and prevention of ticks and tick-borne diseases require a better understanding of host, tick and pathogen interactions and thus get a better view of the tick-borne pathosystems.

In this study (3), the tick-borne pathosystem included three component species: first a seabird host, the Yellow-legged gull (YLG - Larus michahellis, Laridae), second a soft nidicolous tick (Ornithodoros maritimus, Argasidae, syn. Alectorobius maritimus) known to infest this host and third a blood parasite (Babesia sp. YLG, Piroplasmidae). In this pathosystem, authors investigated the role of the soft tick, Ornithodoros maritimus, as a potential vector of Babesia sp. YLG. They analyzed the transmission of Babesia sp. YLG by collecting different tick life stages from YLG nests during 4 consecutive years on the islet of Carteau (Gulf of Fos, Camargue, France). Ticks were dissected and organs were analyzed separately to detect the presence of Babesia sp DNA and to evaluate different transmission pathways.

While the authors detected Babesia sp. YLG DNA in the salivary glands of nymphs, females and males, this result reveals a strong suspicion of transmission of the parasite by the soft tick. Babesia sp. YLG DNA was also found in tick ovaries, which could indicate possible transovarial transmission. Finally, the authors detected Babesia sp. YLG DNA in several male testes and in endospermatophores, and notably in a parasite-free female (uninfected ovaries and salivary glands). These last results raise the interesting possibility of sexual transmission from infected males to uninfected females.

As pointed out by both reviewers, this is a nice study, well written and easy to read. All the results are new and allow to better understand the role of the soft tick, Ornithodoros maritimus, as a potential vector of Babesia sp. YLG. They finally question about the degree to which the parasite can be maintained locally by ticks and the epidemiological consequences of infection for both O. maritimus and its avian host. For all these reasons, I chose to recommend this article for Peer Community In Infections.

References

1. Dantas-Torres et al (2012). Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol. 28:437. https://doi.org/10.1016/j.pt.2012.07.003 
2. Johnson N et al (2022). One Health Approach to Tick and Tick-Borne Disease Surveillance in the United Kingdom. Int J Environ Res Public Health. 19:5833. https://doi.org/10.3390/ijerph19105833
3. Bonsergent C, Vittecoq M, Leray C, Jouglin M, Buysse M, McCoy KD, Malandrin L. A soft tick vector of Babesia sp. YLG in Yellow-legged gull (Larus michahellis) nests. bioRxiv, 2023.03.24.534071, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.03.24.534071

Ticks are amongst the most important pathogen vectors in medical and veterinary clinical settings worldwide (Dantas-Torres et al., 2012). Like other holobionts, ticks live in association with a diverse microbiota. It includes tick-borne pathogens (TBP) and other microorganisms that have a beneficial or detrimental effect on the physiology of the host and can also affect the transmission of TBP to animals or humans. In this microbiota, primary endosymbionts, which are obligatory and inheritable, play a role in tick reproduction, the host defense and adaptation to varying environmental conditions (Duron et al., 2018). However, the effect of the microbiota structure and of the endosymbionts on tick fitness and reproduction is not well known. The soft tick Ornithodoros moubata, a parasite known to transmit African swine fever virus (Vial, 2009), is known to host Francisella-like and Rickettsia endosymbionts (Duron et al., 2018). These endosymbionts carry genes involved in B vitamin synthesis which may be supplemented to the host (Bonnet & Pollet, 2021). 

Here, the authors investigated the role of endosymbionts on the reproductive fitness of Ornithodoros moubata by conducting two experiments (Taraveau et al., 2023). First, they tested the effect of antibiotic treatment of 366 first-stage nymphs on the main endosymbionts Francisella-like and Rickettsia, and measured the endosymbionts presence overtime by qPCR. Second, they surveyed the effect of antibiotic treatment with or without the addition of B vitamins on the survival and reproductive fitness of 132 females over 50 days. This second experiment intended to identify whether the endosymbionts have an effect on the host reproduction or on its nutrition. The supplementation of B vitamin did not have a drastic effect on tick fitness or reproductive traits. However, antibiotic treatments reduced the presence of endosymbionts while increasing tick survival, suggesting a potential cost of hosting endosymbionts on the tick fitness.

The authors did a lot of work to thoroughly follow the propositions from Dr Raggi, Dr Aivelo and myself to reconstruct and to revise the manuscript. I believe that the manuscript now reads very well and the answers to the reviews also add some value to the manuscript. As Dr Aivelo pointed out, “this study follows the traditional path of so-called population perturbation studies, where ecologists have administered antibiotics or antihelminths to different animals and seen how the community changes and what effects this has on the host fitness and survival”. As both reviewers stated, results from this study are valuable and provide important basic knowledge that will likely help conduct future experiments on tick microbiota. This recommendation is the result of the thorough reviewing work of Dr Aivelo and Dr Raggi which I warmly thank.
 
References

Bonnet, S. I., & Pollet, T. (2021). Update on the intricate tango between tick microbiomes and tick‐borne pathogens. Parasite Immunology, 43(5), e12813. https://doi.org/10.1111/pim.12813

Dantas-Torres, F., Chomel, B. B., & Otranto, D. (2012). Ticks and tick-borne diseases: A One Health perspective. Trends in Parasitology, 28(10), 437–446. https://doi.org/10.1016/j.pt.2012.07.003

Duron, O., Morel, O., Noël, V., Buysse, M., Binetruy, F., Lancelot, R., Loire, E., Ménard, C., Bouchez, O., Vavre, F., & Vial, L. (2018). Tick-Bacteria Mutualism Depends on B Vitamin Synthesis Pathways. Current Biology, 28(12), 1896-1902.e5. https://doi.org/10.1016/j.cub.2018.04.038

Taraveau, F., Pollet, T., Duhayon, M., Gardès, L., & Jourdan-Pineau, H. (2023). Influence of endosymbionts on the reproductive fitness of the tick Ornithodoros moubata. bioRxiv, ver.3, peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.05.09.539061

Vial, L. (2009). Biological and ecological characteristics of soft ticks (Ixodida: Argasidae) and their impact for predicting tick and associated disease distribution. Parasite, 16(3), 191–202. https://doi.org/10.1051/parasite/2009163191

Mosquitoes are first vector of pathogen worldwide and transmit several arbovirus, most of them leading to major outbreaks (1). Chikungunya virus (CHIKV) is a perfect example of the “explosive type” of arbovirus, as observed in La Réunion Island in 2005-2006 (2-6) and also in the outbreak of 2007 in Italy (7), both vectorized by Ae. albopictus. Being able to better understand CHIKV intra-vector dynamics is still of major interest since not all chikungunya strain are explosive ones (8). 

In this study (9), the authors have evaluated the vector competence of a local strain of Aedes albopictus (collected in Lyon, France) for CHIKV. They evaluated infection, dissemination and transmission dynamics of CHIKV using different dose of virus in individual mosquitoes from day 2 to day 20 post exposure, by titration and quantification of CHIKV RNA load in the saliva. As highlighted by both reviewers, the most innovative idea in this study was the use of three different oral doses trying to span human viraemia detected in two published studies (10-11), doses that were estimated through their model of human CHIKV viremia in the blood.  They have found that CHIKV dissemination from the Ae. albopictus midgut depends on the interaction between time post-exposure and virus dose (already highlighted by other international publications).  Then their results were implemented in the agent-based model nosoi to estimate the epidemic potential of CHIKV in a French population of Ae. albopictus, using realistic vectorial capacity parameters.

To conclude, the authors have discussed the importance of other parameters that could influence vector competence as mosquito microbiota and temperature, parameters that need also to be estimated in local mosquito population to improve the risk assessment through modelling.  

As pointed out by both reviewers, this is a nice study, well written and easy to read. These results allow filling in another gap of our understanding of CHIKV intra-vector dynamics and highlight the epidemic potential of CHIKV upon transmission by Aedes albopictus in mainland France. For all these reasons, I chose to recommend this article for Peer Community In Infections.

References

1.       Marine Viglietta, Rachel Bellone, Adrien Albert Blisnick, Anna-Bella Failloux. (2021). Vector Specificity of Arbovirus Transmission. Front Microbiol Dec 9;12:773211. https://doi.org/10.3389/fmicb.2021.773211

2.       Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney M-C, Lavenir R, Pardigon N, Reynes J-M, Pettinelli F, Biscornet L, Diancourt L, Michel S, Duquerroy S, Guigon G, Frenkiel M-P, Bréhin A-C, Cubito N, Desprès P, Kunst F, Rey FA, Zeller H, Brisse S. (2006). Genome Microevolution of Chikungunya viruses Causing the Indian Ocean Outbreak. 2006. PLoS Medicine, 3, e263. https://doi.org/10.1371/journal.pmed.0030263

3.       Bonilauri P, Bellini R, Calzolari M, Angelini R, Venturi L, Fallacara F, Cordioli P, 687 Angelini P, Venturelli C, Merialdi G, Dottori M. (2008). Chikungunya Virus in Aedes albopictus, Italy. Emerging Infectious 689 Diseases, 14, 852–854. https://doi.org/10.3201/eid1405.071144

4.       Pagès F, Peyrefitte CN, Mve MT, Jarjaval F, Brisse S, Iteman I, Gravier P, Tolou H, Nkoghe D, Grandadam M. (2009). Aedes albopictus Mosquito: The Main Vector of the 2007 Chikungunya Outbreak in Gabon. PLoS ONE, 4, e4691. https://doi.org/10.1371/journal.pone.0004691

5.       Paupy C, Kassa FK, Caron M, Nkoghé D, Leroy EM (2012) A Chikungunya Outbreak Associated with the Vector Aedes albopictus in Remote Villages of Gabon. Vector-Borne and Zoonotic Diseases, 12, 167–169. https://doi.org/10.1089/vbz.2011.0736

6.       Mombouli J-V, Bitsindou P, Elion DOA, Grolla A, Feldmann H, Niama FR, Parra H-J, Munster VJ. (2013). Chikungunya Virus Infection, Brazzaville, Republic of Congo, 2011. Emerging Infectious Diseases, 19, 1542–1543. https://doi.org/10.3201/eid1909.130451

7.       Venturi G, Luca MD, Fortuna C, Remoli ME, Riccardo F, Severini F, Toma L, Manso MD, Benedetti E, Caporali MG, Amendola A, Fiorentini C, Liberato CD, Giammattei R, Romi R, Pezzotti P, Rezza G, Rizzo C. (2017). Detection of a chikungunya outbreak in Central Italy, August to September 2017. Eurosurveillance, 22, 17–00646. https://doi.org/10.2807/1560-7917.es.2017.22.39.17-00646

8.       de Lima Cavalcanti, T.Y.V.; Pereira, M.R.; de Paula, S.O.; Franca, R.F.d.O. (2022). A Review on Chikungunya Virus Epidemiology, Pathogenesis and Current Vaccine Development. Viruses 2022, 14, 969. https://doi.org/10.3390/v14050969

9.       Barbara Viginier, Lucie Cappuccio, Celine Garnier, Edwige Martin, Carine Maisse, Claire Valiente Moro, Guillaume Minard, Albin Fontaine, Sebastian Lequime, Maxime Ratinier, Frederick Arnaud, Vincent Raquin. (2023). Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier permissiveness and supports local epidemic potential. medRxiv, ver.3, peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2022.11.06.22281997

10.     Appassakij H, Khuntikij P, Kemapunmanus M, Wutthanarungsan R, Silpapojakul K (2013) Viremic profiles in CHIKV-infected cases. Transfusion, 53, 2567–2574. https://doi.org/10.1111/j.1537-2995.2012.03960.x

11.     Riswari SF, Ma’roef CN, Djauhari H, Kosasih H, Perkasa A, Yudhaputri FA, Artika IM, Williams M, Ven A van der, Myint KS, Alisjahbana B, Ledermann JP, Powers AM, Jaya UA (2015) Study of viremic profile in febrile specimens of chikungunya in Bandung, Indonesia. Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology, 74, 61–5. https://doi.org/10.1016/j.jcv.2015.11.017