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In comparison with medical immunology, which focuses on mechanistic descriptions of defense mechanisms against pathogens and parasites, ecological immunology hypothesizes that variation in immune defense, both within and among species, is a result of biotic and abiotic factors of an animal’s environment.
Macro-environment can greatly influence immunity in terms of both resources and pathogen pressure. In this thesis, I attempted to compare the immunity of animals living in different human-influenced environmental gradients. By using different study designs (comparative, experimental and correlative approaches), I examined whether captivity, colonization history and urbanization have an effect on the immunity of rodents. Rodents constitute the most diverse group of mammals, accounting for over 40% of all the extant mammalian species. They are one of the most important reservoirs for zoonotic emerging pathogens due in part to their life-history traits (e.g., short lifespan with multiple litters) and close proximity to human populations. Moreover, the vast majority of immunological knowledge has been generated by studies on laboratory model rodents (e.g., house mouse Mus musculus, lab rats Rattus rattus and R. norvegicus), and the developed immunological techniques and tools can be generally applied to free-living conspecifics.
Previous comparative eco-immunological studies have suggested that mating promiscuity is one of the main factors explaining the variation in basal immune investment (total and differential white blood cell (WBC) counts) in captive primates and carnivores. In Chapter 2, I examined whether this conclusion is generalizable to other mammalian groups, how the observed patterns are related to the living environment and if there are differences between free-living and captive animals. Using phylogenetic generalized least-squares statistical models considering non-independence resulting from shared ancestry, I confirmed that species with greater adult body mass averaged across sexes had elevated total and differential (neutrophils and lymphocytes) WBC counts, and found that captive animals presented higher lymphocyte numbers than free-ranging ones. However, I found that the total and differential WBC counts did not co-vary with the residual testes mass, a correlate of mating promiscuity, suggesting that previous conclusion generated from studies of captive primates and carnivores is not generalizable to all mammals. These results also emphasize the need for further comparative studies on free-ranging animals.
Parasites play an important role in the invasion processes and success of their hosts through multiple biological mechanisms such as ‘parasite release’, ‘immuno-competence advantage’ or ‘novel weapon’, among others. In Chapter 3, I examined whether colonization history had an effect on the immunity of western house mouse (M. m. domesticus). Using a common garden experimental approach of wild-derived outbred laboratory populations, I compared the cellular and humoral immunity of European and Iranian mice, representing the newly colonized and source populations respectively. I found that European mice had lower total WBC counts but higher immunoglobulin E concentrations than their Iranian counterparts, providing the first empirical evidence that successful invasive species downregulate their costly cellular immune mechanisms in new habitats, which is compensated by developing high antibody-mediated immunity. Invasive species capable of such immunological shift can be successful in novel habitats by increasing fitness both in term of survival (e.g., efficient immunity, low costs) and reproduction (e.g., investing more resources).
Since the beginning of last century, urbanization has had considerable global effects such as overpopulation and environmental pollution, favoring the emergence and re-emergence of various infectious agents, including those originating from wildlife. It is unclear, however, which physiological mechanisms are behind these emergence events. I attempted to address these questions in the Chapter 4 by measuring the morphological, physiological and pathophysiological traits (morphometry, allostatic load, immunity, parasite load) of free-living brown rats (R. norvegicus) sampled from forest-rural, agro-rural and urban areas along a gradient of increasing urbanization and human population density in Henan Province, China. Urban rats had increased body condition, but also relatively higher allostatic (stress) and parasite load compared to rural individuals, indicating the complex effect of urbanization on the physiology of wildlife.
The results of this dissertation demonstrate that anthropogenic activities (captive maintenance, colonization history, and urbanization) have a clear effect on the immuno- and reservoir-competence of rodents, information which may be crucial in the context of the ‘One Health’, concept which recognizes human, animal and environmental health as connected and interlinked.