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ABSTRACT Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints probably have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells – lymphocytes and granulocytes (neutrophils/heterophils) – across 63 bat species, 400 bird species and 251 non-volant mammal species. By using phylogenetically informed statistical models on field-collected data from wild Neotropical bats and from captive bats, non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Our inability to distinguish bat lymphocyte scaling from birds and bat granulocyte scaling from all other taxa suggests there may be other ecological explanations (i.e. not flight related) for the cell proportion scaling patterns. Future comparative studies of wild bats, birds and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense and its role in the tolerance of (zoonotic) infections.
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Diverse hosts, diverse immune systems: Evolutionary variation in bat immunology
The ability of multiple bat species to host zoonotic pathogens without often showing disease has fostered a growing interest in bat immunology to discover the ways immune systems may differ between bats and other vertebrates. However, interspecific variation in immunological diversity among bats has only begun to be recognized. The order Chiroptera accounts for over 20% of all mammalian species and shows extreme diversity in a suite of correlated ecological traits, such that bats should not be expected to be immunologically homogenous. We review the ecological and evolutionary diversity of chiropteran hosts and highlight case studies emphasizing the range of immune strategies thus far observed across bat species, including responses to SARS‐CoV‐2. Next, we synthesize and propose hypotheses to explain this immunological diversity, focusing on pathogen exposure, biogeography, host energetics, and environmental stability. We then analyze immunology‐related citations across bat species to motivate discussions of key research priorities. Broad sampling is needed to remedy current biases, as only a fraction of bat species has been immunologically studied. Such work should integrate methodological advancements, in vitro and in vivo studies, and phylogenetic comparative methods to robustly test evolutionary hypotheses and understand the drivers and consequences of immunological diversity among bats.
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- Award ID(s):
- 2032157
- PAR ID:
- 10637332
- Publisher / Repository:
- Annals of the New York Academy of Sciences
- Date Published:
- Journal Name:
- Annals of the New York Academy of Sciences
- Volume:
- 1550
- Issue:
- 1
- ISSN:
- 0077-8923
- Page Range / eLocation ID:
- 151 to 172
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/nyas.15395
