Body size affects immune cell proportions in birds and non-volant mammals, but not bats

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 likely 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 scaling framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells--lymphocytes, and granulocytes (neutr-/heterophils)--across 60 bat species, 414 bird species, and 256 non-volant mammal species. By using phylogenetically-informed statistical models on field-collected data from wild Neotropical bats, data gleaned from other wild bats available in the literature, and data from captive 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. 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.Summary statementPowered flight might constrain morphology such that certain immunological features are prioritized. We show that bats largely have similar cell proportions across body mass compared to strong allometric scaling relationships in birds and non-flying mammals.

Effects of host state and body condition on parasite infestation of bent-wing bats

“…In addition, the difference in the immune defense capability of hosts with varying BCIs may not be consistently correlated or sufficient in itself to account for differences in the observed parasite abundance [ 57 ]. For instance, in bats lymphocyte and neutrophil proportions are generally similar irrespective of their body mass [ 58 ], which may explain why bats with lower BCI may not be more vulnerable to parasites than those in better condition [ 10 ].…”

Bat cellular immunity varies by year and dietary habit in an increasingly fragmented landscape

“…The absolute number of each white blood cell type was then determined by multiplying its relative abundance by the estimated TWBC count (Becker et al 2021a). A subset of the hematology data from 2017 and 2018 were published previously (Becker et al 2021a;Cornelius Ruhs et al 2021).…”

Homo medicus: The transition to meat eating, increased pathogen pressure, and the constitutive and inducible use of pharmacological plants in Homo

“…Evidence of increased investment in at least some types of immunity in larger animals is also beginning to emerge. An investigation of the association of immune cell concentrations with body mass in over 250 mammalian species found that neutrophils, part of the innate immune system, scaled hypermetrically (concentrations were positively associated with body mass) whereas lymphocytes, which participate in both the innate and adaptive immune systems, scaled nearly isometrically (concentrations were slightly negatively associated with body mass) (Downs, Dochtermann, et al, 2020;Ruhs, Becker, et al, 2020; see also Ruhs, Martin, et al, 2020). A study examining the antibacterial activity in serum against three bacterial species -Escherichia coli, Salmonella enterica, and Micrococcus luteus -in over 160 terrestrial mammals found that antibacterial activity scaled isometrically with body size, which is more than would be predicted by the hypometric scaling of metabolic rates (Downs, Schoenle, et al, 2020).…”