Marco A. Juarez-Estrada
Danielle Graham
Xochitl Hernandez-Velasco
Guillermo Tellez-Isaias- 1Department of Medicine and Zootechnics of Birds, College of Veterinary Medicine and Zootechnics, National Autonomous University of Mexico, Mexico City, Mexico
- 2Division of Agriculture, Department of Poultry Science, University of Arkansas, Fayetteville, AR, United States
Editorial on the Research Topic
Parasitism: the good, the bad and the ugly
Parasitism is a tight association between species in which one organism, the parasite, lives on or inside the host, causing it harm, and is structurally adapted to this way of life (1). Until the twenty-first century, parasitism was studied by parasitologists, rather than ecologists or evolutionary biologists. Today, parasitism is a major element of evolutionary ecology, as nearly all free-living animals, are hosts to at least one parasite species (2, 3). Since it is in the parasite's evolutionary interest for its host to flourish, long-term coevolution can lead to a stable relationship bordering on mutualism (1, 4). According to Lynn Margulis, when resources are scarce, natural selection moves relationships from parasitism to mutualism, as was brilliantly illustrated in Margulis' endosymbiosis theory, where eukaryotic mitochondria and chloroplasts descended from formerly free-living prokaryotes (5).
While worm parasitism clearly affects animals, it may also reduce the prevalence and severity of autoimmune diseases in animal hosts, including humans (6). Helminth infections might safeguard hosts from immune-mediated illnesses like allergies and autoimmune disease, as well as suppress detrimental inflammatory host's reaction. In this symbiotic relationship, the helminth, and the host benefit from each other's presence (7–9). The boundary between mutualism, symbiosis, and pathological parasitism is narrow and is frequently overlapping without a theory to clearly explain this relationship between the parasite, host, and ecological niche (10–12). Parasites are frequently seen as dangerous and primarily viewed as harmful to the host (3, 13). However, removing them entirely would be detrimental to the host, the environment, and the parasites themselves (3). Complex natural ecosystems with diverse species and their interactions are the result of a long evolutionary history (12, 14). Parasites make up half of life's diversity and play vital ecological roles (3, 15). Parasites allow for inter-species DNA exchange, allowing for evolutionary change (16). To complete their life cycles, many parasites rely on predator-prey or other stable ecological interactions (12, 17). At individual and species levels, hosts have developed adaptations to their coevolving parasites (10, 11, 15, 18). Often, the expression of normal behavior or the development of a healthy immune system depends on parasite infections (8). In instances where parasites are not present, hosts may occasionally exhibit phenotypes that are less than ideal (14). Conserving parasite species is supported by their evolutionary heritage and potential, their role in ecosystem services, and their value as indicators of ecosystem quality (3, 19). Parasites imply a healthy ecology (20). Researchers have highlighted the functional significance of parasites in preserving the health of individual hosts, host populations, and entire ecosystems in order to raise awareness of parasite conservation (3, 14). For individual hosts, parasites impose energetic demands that reduce growth, fecundity, and survival (21, 22), but these apparent negative effects on host fitness may be compensated by positive consequences, such as improving normal host immune system function (8, 9, 23), regulating their host's microbiome (7, 8, 24–26), inducing specific interaction between gut microbiota and host immune responses (27–29), and providing protection against pollutants such as heavy metals (20, 30, 31). Even though parasites decrease host fitness, they could potentially maintain host population viability by controlling host population size (18, 32, 33), and increasing genetic variety while avoiding the detrimental effects of inbreeding (21). Parasites can act as keystone species, allowing competing species to coexist while lowering the dominance of superior competitors (17). Parasites may mediate predatory and competitive interactions among free-living species at higher levels of organization, adjusting community structure and diversity, food web complexity, and energy flow throughout the entire ecosystem (20, 34–36). While parasites typically remain absent from food web representations, they consistently hold the top position (15).
With 220 million people affected annually by malaria, measures such as prophylaxis, eradicating mosquito vectors using pesticides, and developing a malaria vaccine, have been attempted to stop malaria transmission (37). Nonetheless, medication resistance, mosquito pesticide resistance, and vaccination failures due to parasite mutations or parasite immune manipulation have all been issues (38–40). Similar problems have been observed with other economically significant groups of parasites that cause disease in livestock, poultry, and domestic animals, such as protozoa, helminths, and ectoparasites (41, 42).
Due to their potential benefits in numerous ecosystems, parasites should not be eliminated from Earth's environments (3). Nonetheless, some parasites do represent a serious threat to human and animal health; therefore, we must find an appropriate equilibrium between parasite burden, human and animal fitness, and ecosystem quality, all while adhering to the current one health concept (14, 27, 33, 43–46). To achieve this equilibrium, parasite managements must rely on suitable treatment, prevention and control strategies, and their appropriate implementation at field (3, 29, 38, 47). Studies on parasites management can serve as a link between health and environmental sciences, enabling accomplish the objective of the one health concept through an interdisciplinary and holistic approach (14, 44, 48).
Several issues regarding holistic approaches to parasite management have aroused the interest of scientific community, with resulting in several investigations and publications to answer if parasites are good, bad, or ugly for human's and animal's health. This Research Topic contains all various initiatives to harness knowledge, such as the following:
1. Genetic studies for both ecto- and endo parasites. Generated mitochondrial genome data provided further flea taxonomic and epidemiological studies (Liu et al.). Genetic analysis of Fasciola hepatica, demonstrated population structure in South America not previously realized using nuclear and mitochondrial markers (Garcia-Corredor et al.).
2. Innovative lab procedures. Currently, it is feasible to use harmless methods for preserving avian Eimeria sp. sporulated oocysts for challenge testing or live coccidiosis vaccines (Laverty et al.). Isolates of live-attenuated Histomonas meleagridis were successfully obtained by serial passaging in a lab setting (Beer et al.). These attenuated vaccine strains proved to be immunoprotective against challenge with virulent H. meleagridis. However, commercial application of these attenuated vaccines is not currently feasible from a production, labor, and economic standpoint. Nowdays, the identification of E. tenella antigens through novel immunological approaches is crucial for the development of successful genetically engineered vaccines (Juárez-Estrada et al.). Lab procedures indicates that Ferritin 2 has emerged as a promising antigen for a universal vaccination against avian mites (Win et al.).
3. Bibliometric analysis for screening assistance. Bibliometric data provides insight for the selection and evolution of anticoccidial drugs and, contributes to understand anticoccidial medication utilization trends (Kandeel et al.).
4. Experimental infection models are necessary to mimic complex multi-factorial interactions. An experimental mixed avian Eimeria sp. challenge model that particularly evaluates performance, intestinal permeability, and dysbiosis is suitable to analyse different strategies for avian coccidiosis control (Graham et al.). An experimental model revealed that horizontal transmission of H. meleagridis could vary depending on the pathogenicity of the challenge strain and Turkey diet composition (Barros et al.). Turkeys experimentally vaccinated with a candidate E. meleagrimitis strain with or without amprolium intervention showed altered ileal and cecal microbiome (Trujillo-Peralta et al.). In an experimental model of priming/challenge, an E. meleagrimitis strain candidate vaccine caused a moderate infection that induced protective immunity (Trujillo-Peralta et al.). Coccidiosis infection in lambs impacts rumen fermentation in a way that is independent of plane nutrition, but this effect does not translate to performance response (Sujani et al.).
5. Alternatives to antibiotics. As demand rises to decrease (eliminate) antibiotic use in poultry; natural resources such as Yucca schidigera and Trigonella foenum are promising coccidiosis control options (Benarbia et al.). Soybean lecithin has also been linked to increased resilience in several animal species to physical and chemical stressors (Wee et al.).
Novel research on parasitology contributes to identify new prevention and control measures that we need now more than ever front to current climate changing (43, 49, 50).
Author contributions
MJ-E: Conceptualization, Data curation, Writing—original draft, Writing—review and editing. GT-I: Conceptualization, Data curation, Funding acquisition, Writing—original draft, Writing—review and editing. DG: Conceptualization, Data curation, Writing—original draft, Writing—review and editing. XH-V: Data curation, Visualization, Writing—review and editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by USDA-NIFA Sustainable Agriculture Systems, Grant No. 220199-690122-29905. Title of Project: Empowering United States Broiler Production for Transformation and Sustainability USDA-NIFA (Sustainable Agriculture Systems): No. 220199-690122-29905. The research was also supported by the National Autonomous University of Mexico (UNAM)-Technological Innovation, Research Projects Support Program (PAPIIT) Project Number: IN217022, Alternative Strategies for Prophylaxis of Avian Coccidiosis in México.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
1. Rózsa L, Garay J. Definitions of parasitism, considering its potentially opposing effects at different levels of hierarchical organization. Parasitol. (2023) 150:761–68. doi: 10.1017/S0031182023000598
2. Santiago MFM, King KC, Drew GC. Interactions between insect vectors and plant pathogens span the parasitism–mutualism continuum. Biol Lett. (2023) 19:20220453. doi: 10.1098/rsbl.2022.0453
3. Lymbery AJ, Smit NJ. Conservation of parasites: a primer. Int J Parasitol Parasites Wildl. (2023) 21:255–63. doi: 10.1016/j.ijppaw.2023.07.001
4. Hasik AZ, de Angeli Dutra D, Doherty JF, Duffy MA, Poulin, R, Siepielski AM. Resetting our expectations for parasites and their effects on species interactions: a meta-analysis. Ecol Lett. (2023) 26:184–99. doi: 10.1111/ele.14139
5. López-García P, Moreira D. The symbiotic origin of the eukaryotic cell. C R Biol. (2023) 346:55–73. doi: 10.5802/crbiol.118
6. Abu-Shakra M, Shoenfeld Y. For debate parasitic infection and autoimmunity. Autoimmunity. (1991) 9:337–44. doi: 10.3109/08916939108997136
7. Loke P, Lim YAL. Helminths and the microbiota: parts of the hygiene hypothesis. Parasite Immunol. (2015) 37:314–23. doi: 10.1111/pim.12193
8. Ramanan D, Bowcutt R, Lee SC, Tang MS, Kurtz ZD, Ding Y, et al. Helminth infection promotes colonization resistance via type 2 immunity. Science. (2016) 352:608–12. doi: 10.1126/science.aaf3229
9. Atagozli T, Elliott DE, Ince MN. Helminth lessons in inflammatory bowel diseases (IBD). Biomedicine. (2023) 11:1200. doi: 10.3390/biomedicines11041200
10. Taraschewski H. Hosts and parasites as aliens. J Helminthol. (2006) 80:99–128. doi: 10.1079/JOH2006364
11. Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL. Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl. (2014) 3:171–77. doi: 10.1016/j.ijppaw.2014.04.002
12. Best A, Ashby B. How do fluctuating ecological dynamics impact the evolution of hosts and parasites? Phil Trans R Soc B. (2023) 378:20220006. doi: 10.1098/rstb.2022.0006
13. Vilcinskas A. Pathogens as biological weapons of invasive species. PLoS Pathog. (2015) 11:e1004714. doi: 10.1371/journal.ppat.1004714
14. Selbach C, Mouritsen KN, Poulin R, Sures B, Smit NJ. Bridging the gap: aquatic parasites in the One Health concept. Trends Parasitol. (2022) 38:109–11. doi: 10.1016/j.pt.2021.10.007
15. Jephcott TG, Sime-Ngando T, Gleason FH, Macarthur DJ. Host–parasite interactions in food webs: Diversity, stability, and coevolution. Food Webs. (2016) 6:1–8. doi: 10.1016/j.fooweb.2015.12.001
16. Combes C. Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago: University of Chicago Press Chicago, USA. (2001).
17. Ramesh A, Hall SR. Niche theory for within-host parasite dynamics: Analogies to food web modules via feedback loops. Ecol Lett. (2023) 26:351–68. doi: 10.1111/ele.14142
18. Papkou A, Gokhale CS, Traulsen A, Schulenburg H. Host–parasite coevolution: why changing population size matters. Zoology. (2016) 119:330–38. doi: 10.1016/j.zool.2016.02.001
19. Almeida D, Cruz A, Llinares C, Torralva M, Lantero E, Fletcher DH, et al. Fish morphological and parasitological traits as ecological indicators of habitat quality in a Mediterranean coastal lagoon. Aquatic Conserv: Mar Freshw Ecosyst. (2023) 2023:1–16. doi: 10.1002/aqc.3996
20. Marcogliese DJ. Parasites of the superorganism: are they indicators of ecosystem health? Inter J Parasitol. (2005) 35:705–16. doi: 10.1016/j.ijpara.2005.01.015
21. Coltman DW, Pilkington JG, Smith JA, Pemberton JM. Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evol. (1999) 53:1259–67. doi: 10.2307/2640828
22. Marcogliese DJ. Parasites: Small players with crucial roles in the ecological theater. Ecohealth. (2004) 1:151–64. doi: 10.1007/s10393-004-0028-3
23. Sorci G, Guivier E, Lippens C, Faivre B. Microbes, Parasites and Immune Diseases. In: Alvergne A, Jenkinson C, Faurie C, editors. Evolutionary Thinking in Medicine: From Research to Policy and Practice. Cham: Springer International Publishing. (2016) p. 211–23.
24. Giacomin P, Agha Z, Loukas A. Helminths and intestinal flora team up to improve gut health. Trends Parasitol. (2016) 32:664–66. doi: 10.1016/j.pt.2016.05.006
25. Partida-Rodríguez O, Serrano-Vázquez A, Nieves-Ramírez ME, Moran P, Rojas L, Portillo T, et al. Human intestinal microbiota: Interaction between parasites and the host immune response. Arch Med Res. (2017) 48:690–700. doi: 10.1016/j.arcmed.2017.11.015
26. Llewellyn MS, Leadbeater S, Garcia C, Sylvain FE, Custodio M, Ang KP, et al. Parasitism perturbs the mucosal microbiome of Atlantic Salmon. Sci Rep. (2017) 7:43465. doi: 10.1038/srep43465
27. Mutapi F. The gut microbiome in the helminth infected host. Trends Parasitol. (2015) 31:405–06. doi: 10.1016/j.pt.2015.06.003
28. Li C, Liu Y, Liu X, Bai X, Jin X, Xu F, et al. The gut microbiota contributes to changes in the host immune response induced by Trichinella spiralis. PLoS Negl Trop Dis. (2023) 17:e0011479. doi: 10.1371/journal.pntd.0011479
29. Boisseau M, Dhorne-Pollet S, Bars-Cortina D, Courtot É, Serreau D, Annonay G, et al. Species interactions, stability, and resilience of the gut microbiota - Helminth assemblage in horses. iScience. (2023) 26:106044. doi: 10.1016/j.isci.2023.106044
30. Sánchez MI, Pons I, Martínez-Haro M, Taggart MA, Lenormand T, Green AJ. When parasites are good for health: Cestode parasitism increases resistance to arsenic in brine shrimps. PLoS Pathog. (2016) 12:e1005459. doi: 10.1371/journal.ppat.1005459
31. Keke UN, Mgbemena AS, Arimoro FO, Omalu ICJ. Biomonitoring of effects and accumulations of heavy metals insults using some helminth parasites of fish as bio-indicators in an Afrotropical stream. Front Environ Sci. (2020) 2:576080. doi: 10.3389/fenvs.2020.576080
32. Hudson PJ, Dobson AP, Newborn D. Prevention of population cycles by parasite removal. Science. (1998) 282:2256–58. doi: 10.1126/science.282.5397.2256
33. Scott ME. Helminth-host-environment interactions: Looking down from the tip of the iceberg. J Helminthol. (2023) 97:e59. doi: 10.1017/S0022149X23000433
34. Hudson PJ, Dobson AP, Lafferty KD. Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol. (2006) 21:381–85. doi: 10.1016/j.tree.2006.04.007
35. Dunn AM, Hatcher MJ. Parasites and biological invasions: parallels, interactions, and control. Trends Parasitol. (2015) 31:189–99. doi: 10.1016/j.pt.2014.12.003
36. Vannatta JT, Minchella DJ. Parasites and their impact on ecosystem nutrient cycling. Trend Parasitol. (2018) 34:452–55. doi: 10.1016/j.pt.2018.02.007
37. El Moustapha I, Ouldabdallahi Moukah M, Ould Ahmedou Salem MS, Brahim K, Briolant S, Basco L, et al. Malaria prevalence in Mauritania: a systematic review and meta-analysis. Malar. J. (2023) 22:146. doi: 10.1186/s12936-023-04569-4
38. Orwa T, Mbogo R, Luboobi L. Mathematical model for the in-host malaria dynamics subject to malaria vaccines. Lett Biomath. (2018) 5:22–251. doi: 10.30707/LiB5.1Orwa
39. Aidoo EK, Aboagye FT, Botchway FA, Osei-Adjei G, Appiah M, Duku-Takyi R, et al. Reactive case detection strategy for malaria control and elimination: a 12 year systematic review and meta-analysis from 25 malaria-endemic countries. Trop Med Inf Dis. (2023) 8:180. doi: 10.3390/tropicalmed8030180
40. Miyauchi E, Shimokawa C, Steimle A, Desai MS, Ohno H. The impact of the gut microbiome on extra-intestinal autoimmune diseases. Nat Rev Immunol. (2023) 23:9–23. doi: 10.1038/s41577-022-00727-y
41. Blake DP, Tomley FM. Securing poultry production from the ever-present Eimeria challenge. Trends Parasitol. (2014) 30:12–9. doi: 10.1016/j.pt.2013.10.003
42. Naz S, Abbasi SW, Cavezza S, Jaiswal AK, Azevedo V. Parasite Control Strategies: Immunoprophylaxis. In: Rizwan HM, Sajid MS, , editors. Parasitism and Parasitic Control in Animals. Oxfordshire: CABI. (2023) 231–47. doi: 10.1079/9781800621893.0015
43. Iacovino A, Randazzo L. Climate change and food security in the One Health perspective. BioLaw J. (2023) 2:293–314.
44. Díaz AV, Walker M, Webster JP. Reaching the World Health Organization elimination targets for schistosomiasis: the importance of a one health perspective. Phil Trans R Soc B. (2023) 378:20220274. doi: 10.1098/rstb.2022.0274
45. Douchet P, Gourbal B, Loker ES, Rey O. Schistosoma transmission: scaling-up competence from hosts to ecosystems. Trends Parasitol. (2023) 39:563–74. doi: 10.1016/j.pt.2023.04.001
46. Vicente-Santos A, Willink B, Nowak K, Civitello DJ, Gillespie TR. Host-pathogen interactions under pressure: a review and meta-analysis of stress-mediated effects on disease dynamics. Ecol Lett. (2023) 1–18. doi: 10.1111/ele.14319
47. Coates A. Research pre-empting parasite adaptation is key to sustainable disease management in aquaculture. Aquacult Environ Interact. (2023) 15:35–43. doi: 10.3354/aei00451
48. Hodžić A, Dheilly NM, Cabezas-Cruz A, Berry D. The helminth holobiont: a multidimensional host–parasite–microbiota interaction. Trends Parasitol. (2023) 39:91–100. doi: 10.1016/j.pt.2022.11.012
49. Hector TE, Gehman ALM, King KC. Infection burdens and virulence under heat stress: ecological and evolutionary considerations. Phil Trans R Soc B. (2023) 378:20220018. doi: 10.1098/rstb.2022.0018
Keywords: protozoa, helminths, ectoparasites, parasite vaccines, mutualism, inflammation
Citation: Juarez-Estrada MA, Graham D, Hernandez-Velasco X and Tellez-Isaias G (2023) Editorial: Parasitism: the good, the bad and the ugly. Front. Vet. Sci. 10:1304206. doi: 10.3389/fvets.2023.1304206
Received: 29 September 2023; Accepted: 06 October 2023;
Published: 17 October 2023.
Edited and reviewed by: Antoinette Marsh, The Ohio State University, United States
Copyright © 2023 Juarez-Estrada, Graham, Hernandez-Velasco and Tellez-Isaias. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Marco A. Juarez-Estrada, britoco@unam.mx; Guillermo Tellez-Isaias, gtellez@uark.edu