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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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The impacts of body mass on immune cell concentrations in birds
Body mass affects many biological traits, but its impacts on immune defences are fairly unknown. Recent research on mammals found that neutrophil concentrations disproportionately increased (scaled hypermetrically) with body mass, a result not predicted by any existing theory. Although the scaling relationship for mammals might predict how leucocyte concentrations scale with body mass in other vertebrates, vertebrate classes are distinct in many ways that might affect their current and historic interactions with parasites and hence the evolution of their immune systems. Subsequently, here, we asked which existing scaling hypothesis best-predicts relationships between body mass and lymphocyte, eosinophil and heterophil concentrations—the avian functional equivalent of neutrophils—among more than 100 species of birds. We then examined the predictive power of body mass relative to life-history variation, as extensive literature indicates that the timing of key life events has influenced immune system variation among species. Finally, we ask whether avian scaling patterns differ from the patterns we observed in mammals. We found that an intercept-only model best explained lymphocyte and eosinophil concentrations among birds, indicating that the concentrations of these cell types were both independent of body mass. For heterophils, however, body mass explained 31% of the variation in concentrations among species, much more than life-history variation (4%). As with mammalian neutrophils, avian heterophils scaled hypermetrically ( b = 0.19 ± 0.05), but more steeply than mammals (approx. 1.5 ×; 0.11 ± 0.03). As such, we discuss why birds might require more broadly protective cells compared to mammals of the same body size. Overall, body mass appears to have strong influences on the architecture of immune systems.
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- PAR ID:
- 10220760
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 287
- Issue:
- 1934
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20200655
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2020.0655
