Leukocyte Profiles Reflect Geographic Range Limits in a Widespread Neotropical Bat

Author:

Becker Daniel J123ORCID,Nachtmann Cecilia1,Argibay Hernan D4,Botto Germán56,Escalera-Zamudio Marina78,Carrera Jorge E910,Tello Carlos1112,Winiarski Erik13,Greenwood Alex D714,Méndez-Ojeda Maria L15,Loza-Rubio Elizabeth16,Lavergne Anne17,de Thoisy Benoit17,Czirják Gábor Á7,Plowright Raina K5,Altizer Sonia12,Streicker Daniel G11819

Affiliation:

1. Odum School of Ecology, University of Georgia, Athens, GA 30602, USA

2. Center for the Ecology of Infectious Disease, University of Georgia, Athens, GA 30602, USA

3. Department of Biology, Indiana University, Bloomington, IN 47405, USA

4. Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires C1428EGA, Argentina

5. Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59715, USA

6. Departamento de Metodos Cuantitativos, Facultad de Medicina, Universidad de la República, Montevideo 11800, Uruguay

7. Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin 10315, Germany

8. Department of Zoology, University of Oxford, Oxford OX1 3SY, UK

9. Facultad de Ciencias, Universidad Nacional de Piura, Piura 20009, Peru

10. Programa de Conservación de Murciélagos de Perú, Piura Lima-1, Peru

11. Association for the Conservation and Development of Natural Resources, Lima 15037, Peru

12. Yunkawasi, Lima 15049, Peru

13. Departamento de Histología, Facultad de Medicina, Universidad de la República, Montevideo 11800, Uruguay

14. Department of Veterinary Medicine, Freie Universität Berlin, Berlin 14163, Germany

15. Facultad de Medicina Veterinaria y Zootecnia, Universidad Veracruzana, Veracruz 91710, Mexico

16. Centro Nacional de Investigación Disciplinaria en Microbiología Animal, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Mexico City 05110, Mexico

17. Laboratoire des Interactions Virus-Hôtes, Institut Pasteur de la Guyane, Cayenne, French Guiana F-97300, France

18. Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK

19. MRC—University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK

Abstract

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.

Funder

National Science Foundation

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Animal Science and Zoology

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