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 comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells--lymphocytes, and granulocytes (neutr-/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 suggest 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 tolerance of (zoonotic) infections.

Baseline of Physiological Body Temperature and Hematological Parameters in Captive Rousettus aegyptiacus and Eidolon helvum Fruit Bats

“…Although variations linked to immune-senescence and -maturation in circulating leukocytes have been validated in several chiropteran species, e.g., P. giganteus ( McLaughlin et al, 2007 ; Schneeberger et al, 2014 ) and P. poliocephalus ( Edson et al, 2018 ) and other mammals ( Aminzadeh and Parsa, 2011 ), we could not detect age-related differences for E. helvum or R. aegyptiacus . Interestingly, it has been recently demonstrated that the number of circulating immune cells (especially neutrophils and lymphocytes) is size-independent in bats and did not differ significantly among 64 different bat species ( Cornelius Ruhs et al, 2021 ). Bats are the only mammals capable of active flight, which represents a demanding way of locomotion with a high oxygen requirement.…”

Bat cellular immunity varies by year and dietary habit amidst land conversion

“…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, 2021 a ), and we derived NL ratios. A subset of the hematology data from 2017 and 2018 were published previously ( Cornelius Ruhs et al, 2021 ; Becker et al, 2021 a ).…”

Constitutive immune function is not associated with fuel stores in spring migrating passerine birds

“…Species and sex were added as covariates given their documented influence on variation in immune function (Arriero et al., 2015 ; Tieleman et al., 2005 ). The body mass index was also added as a covariate as mass and size can influence immune cell proportions and metabolic rate (Cornelius Ruhs et al., 2021 ). Finally, relative arrival date was added as a covariate as early migrating individuals may differ in immune function from late migrating individuals (Hegemann et al., 2022 ).…”