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

The question on the role of different alternative hosts in the life cycle of acanthocephalan parasites has not been fully resolved to date. There is some information on the use of fish hosts in the genus Pomphorhynchus (Perrot-Minnot et al. 2019). It is known that acanthocephalans of the genus Pomphorhynchus can infect a number of different amphipod species (e.g. Bauer et al. 2000; Cornet et al. 2010; Dezfuli et al. 1999) but it is not clear if some host species might be more “advantageous” for the parasite, or if the parasite is more virulent to some host species than to others. Bauer et al. (2024) investigated different well characterized cryptic lineages of Gammarus fossarum (Weiss et al. 2013) for their susceptibility for two Pomphorhynchus sp. The results show that there is a difference in susceptibility to acanthocephalans between different linages of G. fossarum. Additionally, a parasite species specific difference was detected: the difference in susceptibility was more pronounced for P. tereticollis than for P. laevis. P. tereticollis was less virulent and developed slower than P. laevis (in G. fossarum).

Besides the improved understanding of the biology of acanthocephalan parasites, this study clearly points out that we have to be careful with putting the “generalist” label on parasites simply due to the number of alternative host species we find them in. Instead, we should always have in mind that some of these hosts might be less suitable for the parasite than others when comparing quantitative data on the infection success.

I highly appreciate the experimental approach taken that allows more profound conclusions than evaluations of field data. Experiments and analyses have been conducted well. I think this paper is significantly enhancing our knowledge on the specificity for the intermediate host. I find it highly remarkable that this was even found among different host lineages.

References

Bauer, A., Trouve, S., Gregoire, A., Bollache, L., Cezilly, F. (2000) Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. International Journal for Parasitology, 30(14), 1453-1457. https://doi.org/10.1016/s0020-7519(00)00138-7

Bauer, A., Develay Nguyen, L., Motreuil, S., Teixeira, M., Debrosse, N., Rigaud, T. (2024) Experimental infections reveal differences in specificity, development time and virulence between the acanthocephalan parasite Pomphorhynchus tereticollis and its sympatric counterpart P. laevis, in two cryptic species of Gammarus fossarum. HAL, Ver. 2, Peer-Reviewed and Recommended by Peer Community in Infections, hal-04455823. https://hal.science/hal-04455823  

Cornet, S., Sorci, G., Moret, Y. (2010) Biological invasion and parasitism: invaders do not suffer from physiological alterations of the acanthocephalan Pomphorhynchus laevis. Parasitology, 137(1), 137-147. https://doi.org/10.1017/S0031182009991077 

Dezfuli, B.S., Rossetti, E., Bellettato, C.M., Maynard, B.J. (1999) Pomphorhynchus laevis in its intermediate host Echinogammarus stammeri in the River Brenta, Italy. Journal of Helminthology, 73(2), 95-102. https://doi.org/10.1017/S0022149X00700277 

Perrot-Minnot, M.J., Guyonnet, E., Bollache, L., Lagrue, C. (2019) Differential patterns of definitive host use by two fish acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis. International Journal for Parasitology: Parasites and Wildlife, 8, 135-144. https://doi.org/10.1016/j.ijppaw.2019.01.007 

Weiss, M., Macher, J.N., Seefeldt, M.A., Leese, F. (2013) Molecular evidence for further overlooked species within the Gammarus fossarum complex (Crustacea: Amphipoda). Hydrobiologia, 721(1), 165-184. https://doi.org/10.1007/s10750-013-1658-7

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

Effects of the seasonal variations on within-host parasitaemia are still not well understood and potentially due to numerous factors, e.g. host and parasite species, host sex or age, or geographical regions. In this study, over three years in Switzerland, Pigeault et al. (2024) collected data on great tits reproductive outputs – laying date, clutch size, fledging success – to determine whether they were associated with avian Plasmodium parasitaemia before (winter), during (spring) and after (autumn) the breeding season. They focused on two lineages from two species: a highly generalist lineage Plasmodium relictum (lineage SGS1; Bensch et al. 2009) and a more specialized lineage Plasmodium homonucleophilum (lineage SW2). As previously found, they showed that parasitaemia level is low during the winter and then increase in spring (Applegate, 1970; Applegate 1971). Spring recurrences have been intensively studied but are still not well understood since many non-exclusive factors can provoke them, i.e environmental stressors, reproductive hormones, co-infections or bites of mosquitoes (Cornet et al. 2014).

Interestingly, the parasitaemia level during the winter before and during the breeding season were not associated to the reproductive success, meaning that birds in their populations with low parasitaemia during the winter had not more fledglings than the ones with a higher parasitaemia. However, the individuals who invested the most in the reproduction with a higher number of fledglings had also a higher parasitaemia in the following autumn. The number of laid eggs was not associated with the parasitaemia during the following autumn, showing that the initial investment in the reproduction is less important than the parental care (e.g. chicks feeding) in terms of mid/long term cost. The originality here is that authors followed populations during three periods of the year, which is not an easy task and rarely done in natural populations. Their results highlight the mid/long-term effect of higher resource allocation into reproduction on individuals’ immune system and ability to control parasite replication. Further analyses on various lineages and bird populations from other geographical regions (i.e. different latitudes) would be the next relevant step.

References

Applegate JE (1971) Spring relapse of Plasmodium relictum infections in an experimental field population of English sparrows (Passer domesticus). Journal of Wildlife Diseases, 7, 37–42. https://doi.org/10.7589/0090-3558-7.1.37

Applegate JE, Beaudoin RL (1970) Mechanism of spring relapse in avian malaria: Effect of gonadotropin and corticosterone. Journal of Wildlife Diseases, 6, 443–447. https://doi.org/10.7589/0090-3558-6.4.443

Bensch S, Hellgren O, Pérez‐Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353-1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x

Cornet S, Nicot A, Rivero A, Gandon S (2014) Evolution of plastic transmission strategies in avian malaria. PLoS Pathogens, 10, e1004308. https://doi.org/10.1371/journal.ppat.1004308

Pigeault R, Cozzarolo CS, Wassef J, Gremion J, Bastardot M, Glaizot O, Christe P (2024) Spring reproductive success influences autumnal malarial load in a passerine bird. bioRxiv ver 3. Peer reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.07.28.550923