Trends in Immunology
Volume 39, Issue 11, November 2018, Pages 862-873
Journal home page for Trends in Immunology

Opinion
Vector Immunity and Evolutionary Ecology: The Harmonious Dissonance

https://doi.org/10.1016/j.it.2018.09.003Get rights and content

Highlights

Principles of evolutionary ecology and molecular signaling are integrated to stimulate a more holistic approach in the field of arthropod vector immunology.

Immune responses in arthropod vectors can induce collateral damage of tissues and are energetically costly. When the immune response is more valuable to the organism compared with pathogenicity induced by microbes, arthropod vectors can evolve tolerance to infection.

Life cycles of microbes transmitted by arthropod vectors dictate their relative pathogenicity and their effect on reproduction, survival, and development.

Both mammals and arthropods generate ‘trained immunity’ against previously encountered microbes. However, the identification of conserved mechanisms of trained immunity in arthropod vectors is complicated by the overrepresentation of studies in model organisms.

Recent scientific breakthroughs have significantly expanded our understanding of arthropod vector immunity. Insights in the laboratory have demonstrated how the immune system provides resistance to infection, and in what manner innate defenses protect against a microbial assault. Less understood, however, is the effect of biotic and abiotic factors on microbial-vector interactions and the impact of the immune system on arthropod populations in nature. Furthermore, the influence of genetic plasticity on the immune response against vector-borne pathogens remains mostly elusive. Herein, we discuss evolutionary forces that shape arthropod vector immunity. We focus on resistance, pathogenicity and tolerance to infection. We posit that novel scientific paradigms should emerge when molecular immunologists and evolutionary ecologists work together.

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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