Leukocyte Profiles Reflect Geographic Range Limits in a Widespread Neotropical Bat.

Daniel J Becker,Anne Lavergne,Germán Botto,Erik Winiarski,Carlos Tello,Elizabeth Loza-Rubio,Daniel G Streicker,Jorge E Carrera,Marina Escalera-Zamudio,Benoit De Thoisy,Cecilia Nachtmann,Alex D Greenwood,Raina K Plowright,Maria L Méndez-Ojeda,Gábor Á Czirják,Hernan D Argibay,Sonia Altizer

doi:10.1093/icb/icz007

Abstract

Quantifying how the environment shapes host immune defense is important for understanding which wild populations may be more susceptible or resistant to pathogens. Spatial variation in parasite risk, food and predator abundance, and abiotic conditions can each affect immunity, and these factors can also manifest at both local and biogeographic scales. Yet identifying predictors and the spatial scale of their effects is limited by the rarity of studies that measure immunity across many populations of broadly distributed species. We analyzed leukocyte profiles from 39 wild populations of the common vampire bat (Desmodus rotundus) across its wide geographic range throughout the Neotropics. White blood cell differentials varied spatially, with proportions of neutrophils and lymphocytes varying up to six-fold across sites. Leukocyte profiles were spatially autocorrelated at small and very large distances, suggesting that local environment and large-scale biogeographic factors influence cellular immunity. Generalized additive models showed that bat populations closer to the northern and southern limits of the species range had more neutrophils, monocytes, and basophils, but fewer lymphocytes and eosinophils, than bats sampled at the core of their distribution. Habitats with access to more livestock also showed similar patterns in leukocyte profiles, but large-scale patterns were partly confounded by time between capture and sampling across sites. Our findings suggest that populations at the edge of their range experience physiologically limiting conditions that predict higher chronic stress and greater investment in cellular innate immunity. High food abundance in livestock-dense habitats may exacerbate such conditions by increasing bat density or diet homogenization, although future spatially and temporally coordinated field studies with common protocols are needed to limit sampling artifacts. Systematically assessing immune function and response over space will elucidate how environmental conditions influence traits relevant to epidemiology and help predict disease risks with anthropogenic disturbance, land conversion, and climate change.

Highlights

Environmental changes such as climatic shifts and deforestation alter patterns of infectious disease in wildlife (Acevedo-Whitehouse and Duffus 2009; Brearley et al 2013)
Our spatial analysis of leukocyte profiles in a widely distributed bat species shows that white blood cell (WBC) were autocorrelated at small and large scales, suggesting that local environmental conditions and conditions shared by the extremes of the host distribution predict cellular aspects of the immune system
Comparison among environmental covariates suggested that the latitudinal range limits and local livestock biomass were stronger predictors of WBC variation than local abiotic conditions or coastal range margins

Summary

Introduction

Environmental changes such as climatic shifts and deforestation alter patterns of infectious disease in wildlife (Acevedo-Whitehouse and Duffus 2009; Brearley et al 2013). Environmental variation in host immune phenotypes can arise through various spatial processes that occur at small and large scales, including parasite risk, abiotic conditions, food availability, and predator abundance (Morand et al 2010; Albery et al 2018). At large spatial scales, variation in Lyme disease risk was associated with higher frequency of a protective gene variant of an innate immune receptor in bank vole populations across Europe (Tschirren 2015), and latitudinal gradients in parasite species richness likely have selected for greater host investment in immunity (Møller 1998; Stephens et al 2016). To identify the spatial scales at which the environment shapes immunity and to differentiate between these various hypothesized covariates, field studies of wild populations must capture environmental variation across habitat gradients; a narrow spatial extent is likely to generate low variation given the principle of spatial autocorrelation (Tobler 1970). Large-scale sampling efforts across broad geographic distributions are challenging for many wildlife

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