Trends in Immunology
OpinionVector Immunity and Evolutionary Ecology: The Harmonious Dissonance
Section snippets
An Evolving Outlook for Arthropod Vector Immunity
Have we reached an inflection point in the relative merits of minimizing biological variation? What about the virtues of mechanistic depth over breadth in arthropod vector immunity? Recent research embracing ecological principles in invertebrate immunology have underscored the need to account for natural phenomena such as multiple microbial exposures, the many tradeoffs of arthropod fitness traits, and the role of evolution in shaping close associations between vectors and microbes.
Drosophila
How Evolution Affects Arthropod Vector Immunity
Despite the superficially affable coexistence between arthropod vectors and microbes, immunity is active against pathogens, limiting their transmission. In ticks, phagocytosis and the IMD and JAK/STAT pathways curb the growth of Borrelia burgdorferi and Anaplasma phagocytophilum, the causative agents of Lyme disease and granulocytic anaplasmosis 23, 24, 25, 26, 27. In cat fleas (Ctenocephalides felis), the IMD pathway suppresses the burden of the murine typhus-causing bacterium Rickettsia typhi
Trained Immunity in Mammals: The Molecular Immunology View
Trained immunity is a phenomenon that describes memory conferred by innate immune defenses 21, 55, 56, 57, 58, 59, 60, 61. The mechanisms orchestrating trained immunity remain largely undefined, but it is deemed to be regulated by metabolic as well as epigenetic changes 56, 60, 62 (Figure 4).
Cellular function directly correlates with metabolism 63, 64. Mammalian inflammatory macrophages (also known as M1 in the literature) are largely dependent on glycolysis and exhibit disruption in the
Arthropod Trained Immunity: The Evolutionary Ecology View
While mammalian studies have illuminated many of the elements coordinating trained immunity, the molecular mechanisms involved in arthropod trained immunity remain a frontier of investigation. Theory predicts that parasite exposure frequency, rather than host longevity, should influence the evolution of memory relative to constitutive resistance 76, 77. Evidence from invertebrates suggests that previous exposure to a microbe can enhance resistance and survival on subsequent exposure 26, 55, 78,
Concluding Remarks
Modern scientific approaches have contributed a swath of information in laboratory-reared, genetically inbred organisms for arthropod vector immunity. However, the outcome of this knowledge does not always translate into the complex interaction between a microbe and an arthropod vector in nature (Box 2). Moving forward, if one wants to successfully implement strategies to manage vector-borne diseases, the ecology and evolution of arthropod immunity must be considered (see Outstanding Questions).
Acknowledgments
We thank members of our laboratories for insightful discussions. We also acknowledge Holly Hammond for the schematic illustration describing contextual pathogenicity. This work was supported by grants from the National Institutes of Health (NIH) to U.P., E.F., and J.H.F.P. (P01AI138949), J.H.F.P. (R01AI116523, R01AI134696, and subcontract recipient for R01AI049424), D.K.S (R21AI139772), and E.F. (R01AI126033). E.F. is an Investigator with the Howard Hughes Medical Institute. The content is
Glossary
- Adaptive immunity
- immunity characterized by the presence of lymphocytes, major histocompatibility complex, and recombinant activating gene-dependent antigen receptors.
- Arthropod cellular immunity
- immune response conducted mainly by hemocytes in arthropods.
- Arthropod humoral immunity
- immune response mediated by components present in the fluids, which in arthropods lacks antibody-mediated features.
- Biomphalysin
- pore-forming toxin involved in Biophalaria glabrata immunity.
- Complement
- a series of proteins
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2020, CellCitation Excerpt :Our study of an innate immune factor from the blacklegged tick I. scapularis underscores the context-specific nature of relationships between animals and bacteria (Ehrlich et al., 2008). Ticks harbor microbes, such as B. burgdorferi, which are tolerated by their tick vector but are pathogenic to humans upon transmission (Shaw et al., 2018). Here, we have shown that the mirror opposite is also true: ticks are vulnerable to infection by bacterial commensals found on the skin of vertebrates they feed on.
Immunometabolism in Arthropod Vectors: Redefining Interspecies Relationships
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2020, Developmental and Comparative ImmunologyCitation Excerpt :To fully grasp the consequences of disease tolerance for pathogen spread, it is therefore important to quantify the extent of natural variation in infection tolerance, and test if more tolerant individuals have greater potential for disease transmission (Henschen and Adelman, 2019; Vale et al., 2013). Understanding the physiological mechanisms underlying disease tolerance phenotypes in mosquitos would be helpful in designing therapeutic interventions that aim to reduce their tolerance to vectored pathogens as a means of reducing their vectorial competence (Shaw et al., 2018). The most obvious candidates for such mechanisms are those which either prevent tissue damage from occurring or that are central in the process of repairing tissue damage (Martins et al., 2019; Soares et al., 2017, 2014).
Evolutionary Insights into the Tick Hologenome
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