Review on Disease Ecology
Regassa T and Rebuma T
Published on: 2024-07-19
Abstract
Disease ecology investigates how host behaviors, ecological factors, and pathogen biology interact to shape disease dynamics in human and animal populations. Wildlife, a significant source of novel pathogens, poses threats to biodiversity and public health due to high virulence and host susceptibility. Recent outbreaks like influenza and SARS underscore the urgency of understanding these dynamics. Host behaviors crucially influence pathogen transmission, while eco-evolutionary feedback and social interactions further shape disease spread. This review highlights the complexities of disease ecology, focusing on genetic diversity, biotic and abiotic influences, co-infections, and multi-host interactions. It synthesizes current understanding and identifies research gaps, emphasizing the need for advanced ecological models to mitigate emerging infectious diseases effectively.
Keywords
Disease; Ecology; Emergence; Pathogen; TransmissionIntroduction
Ecology studies the interactions and linkages that exist between different creatures and their surroundings. Wildlife is the source of about 43% of newly discovered human parasites and infections [1]. Emerging infectious illnesses are a major concern for biodiversity because they can have substantial population impacts due to high levels of parasite virulence and host susceptibility resulting from a lack of co-evolutionary history between hosts and parasites [2]. Increased research on infections that have spread from wildlife to humans has resulted from a growing realization in recent decades of the impact wildlife illnesses have on human health. Various influenza viruses, SARS, the West Nile virus, and HIV are a few notable instances that have accelerated progress in the field of disease ecology [3,4].
Almost every aspect of an animal's behavior involves exposure to some type of parasite. Mating behavior is crucial for the transmission of sexually transmitted bacteria, protozoa, and viruses; foraging can lead to infection by environmental and tropically transmitted bacteria and helminths; and social behavior aids in the spread of various contact-transmitted infectious agents [5]. Additionally, behavior plays a key role in how hosts defend themselves against parasites and has been described as the first line of defense against infection [6]. Conversely, host behaviors often change when infected with parasites. These behavioral changes can occur for various reasons: parasites may manipulate host behavior to enhance their fitness, or changes in host behavior may result from the immunological or pathological consequences of parasite infection [7].
Eco-evolutionary feedback is a result of the mutual interaction between ecological and evolutionary processes [8]. This feedback happens when changes in one species' ecology, like a rise in predator density, influence the evolution of features that help prey defend themselves in another species. The ecology of the predator is thus impacted by these evolutionary changes [9]. Social contacts have an impact on an individual's risk of infection [10], and interactions among individuals can have a major impact on how illnesses propagate through a population [11].
As an example, the disease dynamics of devil facial tumor disease in Tasmanian devils [12] are influenced by seasonal variations in social structure. Likewise, disparities in interpersonal connections between people are linked to bovine tuberculosis infection in European badgers [13].
In our time, there is a limitation to further understanding of disease ecology, even if so much research has been conducted on the ordinary topic under different circumstances and aptitudes. Therefore, the objective of this review is:
- To state the effects of host genetic diversity, biotic and abiotic factors, and the maintenance of host-agent interaction; and
- To discuss ecology concerning co-infection and multi-host disease complexes, setting a gap for future research trends.
Disease Ecology
For over a century, there has been a mutually beneficial interaction between epidemiological theory and empirical research, leading to a deep understanding of host-pathogen relationships and the complexities determining transmission dynamics and host ecology [14]. Much of this progress has been made in systems with relatively simple ecologies, often focusing on infectious diseases of humans and non-human animals. However, the rise of zoonotic emerging infectious diseases [1] has increased our awareness of the ecological context of contagious diseases and highlighted the gap between standard theory and biological reality. Greater ecological sophistication in epidemiological theory is necessary to explain zoonoses, identify determinants of pathogen spillover [15], and understand the joint impacts of infectious diseases and biodiversity [16].
At a theoretical wildlife-livestock-human crossing point, abiotic and biotic changes create conditions suitable for disease emergence at different scales. Abiotic factors, such as climate, resources, pollution, and habitat alteration, exist at multiple scales and can either facilitate or inhibit the survival of new and existing wildlife species within the reservoir community. This influences the structural congregation and fitness of hosts. On a broader scale, these abiotic factors affect the biotic niche and the dynamics of pathogens within the system. Abiotic changes can directly impact the microbiota, for example, by driving antimicrobial resistance [17]. Host diversity, density, phylogenetic structure (including ecological, physiological, and genetic similarity), immuno-competence, and the immunological history of individuals are crucial in host-pathogen interactions [18].
For instance, not all conspecifics will be competent hosts for a given parasite, and as ‘dead-end’ hosts, they can play a role in regulating infection, while direct ecological interactions such as predation or competition will affect the population dynamics and distribution of competent reservoir hosts. Reperant, [19] has considered these factors as applied to the theory of island biogeography, where abiotic drivers influence the degree of interactions within source areas (sources of parasites such as wildlife reservoirs) and island areas (the recipient or target hosts) and the source-island distance (interactions between sources of parasites and recipient host populations that can drive spillover). From an ecosystem perspective, anthropogenic pressures result in the fragmentation of natural biomes, leaving a composite mix of different habitats. Remnant fragments that are representative of the original biome can be thought of as patches that exist within a matrix of habitats that are unlike the original [20].
Interfaces between patches and the matrix exist at local scales and can be classified as ecotones transition zones between adjacent ecological systems where "biophysical factors, biological activity, and ecological evolutionary processes are concentrated and intensified" [21]. Expanding ecotones by interspersing human landscapes, such as farmland and settlements, with natural landscapes can alter pathogen niches. This expansion brings humans, vectors, and reservoir hosts (wildlife or domestic animals) into closer contact, increasing the risk of disease transmission and spread [20].
The Effect of Host Genetic Diversity
Genetic variation in susceptibility, where all hosts are susceptible to some degree, does not significantly impact the basic reproductive number (R0) [22]. However, genetic variation among hosts for their self- and non-self-recognition systems could reduce mortality if different parasite strains infect different host genotypes. Such polymorphic systems do exist, even in organisms without the sophisticated immune responses of vertebrates. Detailed information from a broader array of organisms would be highly valued. There is also a need for more field and laboratory studies that experimentally examine the notion that genetic diversity can reduce disease prevalence and mortality. While this idea has support from agricultural systems, experiments involving natural populations are rare [23].
These concepts relate specifically to trade-offs in host immunity [24], where resistance against parasites can deplete the host’s energetic reserves and cause collateral harm to the host’s tissues [25]. The cost of immunity can potentially reduce the survival or fecundity of resistant hosts in nature. When the risk of exposure is low, the costs of immunity may even outweigh the costs of parasitism. Consequently, the cost-benefit ratio for resistance alleles that confer strong immune responses is expected to fluctuate with the risk of exposure. Natural selection is therefore expected to maintain susceptibility alleles in host populations. However, much remains to be done to determine the generality of immunity costs as diversity drivers in natural systems and whether feedbacks with epidemiological dynamics act to maintain resistance variation in nature [26].
Effects of Biotic and Abiotic Factors
Global climate change predictions indicate far-reaching effects on the population dynamics and distributions of livestock parasites, raising concerns about potential increases in disease incidence and production losses. Climate change is altering host-parasite interactions and influencing disease emergence. However, understanding these impacts is challenging due to numerous complicating biological and socio-economic factors [27].
There is a noticeable shift in the incidence of parasitic diseases influenced by environmental factors such as vector prevalence, temperature changes, climate variability, shifting habits, and urbanization. Governments, like that of India, are taking steps to assess vulnerability and implement adaptation measures to combat climate change's impact on vector-borne diseases [28]. Thompson, [29] identifies several other factors contributing to the emergence of parasitic diseases, including poor housing conditions, socioeconomic factors, inadequate surveillance, hunting practices, vaccination of wild animals for disease control, medical treatments for wild hosts, insufficient control of domestic hosts, and changes in landscapes. These factors collectively influence the dynamics and spread of parasitic diseases worldwide.
Single host-parasite pairings versus Multi host-parasite networks
Many hosts are susceptible to infection by multiple parasite species, and conversely, most parasites can infect numerous host species. Despite these common multihost-multiparasite interactions, empirical studies in this area are limited [30]. In reality, communities consist of diverse host and parasite species, each comprising multiple genotypes. This complexity significantly influences host-parasite interactions. For example, the presence of multiple parasite species can alter outcomes due to impacts on the immune system, such as mutual inhibition among different T cell subsets that clear different types of infections [31].
In this case, complementing species may be essentially dissimilar to adding extra genotypes of the identical species. Moreover, within-host community ecology can be abstracted as a tri-trophic system in which parasites must compete for resources and evade predation by the immune system [32]. Such a context has proven prognostic of the consequences of multispecies infections in both the lab [33] and the field [34]. Likewise, hypothetical studies of the evolution of multi-host parasites propose that the presence of multiple host species can bring about initially unexpected outcomes, such as decreased parasite virulence and increased host mortality in certain set-ups [30]. This clue has been explored in some depth within microbial communities, where bacteriophages are known to alter deceptive antagonism among their hosts [35], but is seldom addressed in eukaryotic organisms.
The role microbiota in determining disease ecology
Microbiota is communities of microorganisms that inhabit the bodies of eukaryotic hosts, influencing organismal fitness and mediating susceptibility to disease. For instance, research has shown that the gut microbiota of bumblebees plays a more significant role in susceptibility to the parasite Crithidia bombi than the host genotype itself [36]. Similarly, in humans and mice, the gut microbiota influences susceptibility to intestinal pathogens [37]. There is also evidence suggesting that the vaginal microbiota in humans protects against HIV infection [38], and microbial communities associated with the skin act as a crucial first line of defense against pathogen colonization and infection [39].
There is a significant likelihood that variation among hosts in the commensal microorganisms they harbor enhances effective host diversity within a population. Even when two hosts possess the same alleles conferring resistance, the outcome of infection can differ depending on their microbial community composition. Conversely, host genotype can influence the composition of the microbiota, which in turn affects disease resistance [40]. Commensal microbial communities are dynamic over time, leading to variations in disease susceptibility throughout a host's lifetime. Drivers of change in these communities include colonization patterns and evolution, influenced by factors such as bacteriophage viruses. For instance, the human gut microbiota hosts a significant presence of phages [41], and phages found on the leaves of horse chestnut trees demonstrate remarkable adaptation to their local bacterial hosts [42].
Shifts in the microbiota leading to dysbiosis can have harmful effects that are often challenging to reverse. Recent evidence suggests that a mismatch between the host genotype and the gut microbiota may contribute to the development of conditions like cancer [43], highlighting the complexity of interactions between hosts, including humans, and their microbiomes.
Co-infection and Multi-host complex
Understanding within-host infection patterns is a key challenge in disease ecology [44]. Multiple organisms can co-occur and interact within the same host, but within-host parasite groups are often not thoroughly investigated using eco-phylogenetic approaches [45]. Co-infection refers to the presence of multiple infections involving unrelated pathogens or distinct taxonomic units of the same pathogen within the same host. The importance of co-infections has been underscored, as host immune responses to parasites and ecological interactions between parasites can either facilitate or restrict infections with other pathogens. These interactions can be reciprocal, where one parasite enhances susceptibility to another, or asymmetrical, where one parasite suppresses the infectivity or growth of another. Studying these dynamics is crucial for understanding disease transmission and the overall health impacts on hosts in ecological and epidemiological contexts [46].
Within the realm of zoonotic diseases, a diverse array of infectious agents viral, bacterial, parasitic, fungal, and prion pathogens can cause diseases that are transmitted between animals and humans. Emerging diseases are closely linked to environmental and animal factors. Exogenous zoonotic pathogens often mutate and, upon crossing the species barrier, undergo adaptation to survive in hostile environmental conditions before spilling over to humans [47].
From a network perspective, the segmentation of networks has significant implications for disease spread. Networks that exhibit substantial substructure and higher modularity scores are generally less susceptible to rapid infection spread compared to networks that follow the assumption of random mixing used in many disease models. The modularity of network structure also influences how different network positions affect disease spread in disease ecology, highlighting the importance of network analysis in understanding and managing disease outbreaks across populations and species boundaries [11].
Future Directions and Conclusion
Disease ecology illuminates the intricate interplay between host biology, ecological factors, and pathogen dynamics, profoundly influencing the health of both wildlife and human populations. The field's evolution has been driven by a growing recognition of wildlife as reservoirs for emerging infectious diseases, exemplified by recent outbreaks such as influenza and SARS. Understanding how host behaviors and environmental changes affect disease transmission is crucial for predicting and managing outbreaks. Moreover, the ecological and evolutionary feedbacks observed in disease systems underscore the need for integrated approaches that consider genetic diversity, biotic interactions, and environmental drivers.
- Develop and refine ecological models that incorporate genetic diversity, host interactions, and environmental factors.
- Implement robust surveillance systems that integrate ecological and epidemiological data to detect potential disease outbreaks early.
- Foster collaboration between ecologists, epidemiologists, geneticists, and public health experts to enhance understanding of complex disease dynamics.
- Protecting natural habitats and minimizing human-wildlife interactions can reduce opportunities for disease spillover.
References
- Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature. 2008; 451: 990-993.
- Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel AN, Beukema W, et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science. 2019; 363: 1459-1463.
- Wobeser GA. Disease in wild animals. Investigation and Management, 2nd edition Berlin, Germany: Springer. 2007.
- Ostfeld RS, Keesing F, Eviner VT. Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems. Princeton University Press. 2010.
- Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics. 2003; 34:517-547.
- Hart BL. Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Philosophical Transactions of the Royal Society B: Biological Sciences. 2011; 366: 3406-3417.
- Moore J. An overview of parasite-induced behavioral alterations–and some lessons from bats. J Experimental Biology. 2013; 216:11-17.
- Schoener TW. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science. 2011; 331: 426-429.
- Becks L, Ellner SP, Jones LE, Hairston Jr NG. The functional genomics of an eco-evolutionary feedback loop: linking gene expression, trait evolution, and community dynamics. Ecology letters. 2012; 15:492-501.
- White LA, Forester JD, Craft ME. Using contact networks to explore mechanisms of parasite transmission in wildlife. Biological Reviews. 2017; 92:389-409.
- Cross PC, Drewe J, Patrek V, Pearce G, Samuel MD, Delahay RJ. Wildlife population structure and parasite transmission: implications for disease management. Management of disease in wild mammals. 2009: 9-29.
- Hamede RK, Bashford J, McCallum H, Jones M. Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease. Ecology letters. 2009; 12: 1147-1157.
- Weber N, Carter SP, Dall SR, Delahay RJ, McDonald JL, Bearhop S, McDonald RA. Badger social networks correlate with tuberculosis infection. Current Biology. 2013; 23: 915-916.
- Keeling MJ, Rohani P. Modeling infectious diseases in humans and animals. Princeton university press; 2011.
- Woolhouse ME, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerging infectious diseases. 2005; 11: 1842-1847.
- Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010; 468: 647-652.
- Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. The Lancet infectious diseases. 2013; 13: 155-165.
- Pilosof S, Fortuna MA, Cosson JF, Galan M, Kittipong C, Ribas A, et al. Host–parasite network structure is associated with community-level immunogenetic diversity. Nature communications. 2014; 5: 5172.
- Reperant LA. Applying the theory of island biogeography to emerging pathogens: toward predicting the sources of future emerging zoonotic and vector-borne diseases. Vector-Borne and Zoonotic Diseases. 2010; 10:105-110.
- Reisen WK. Landscape epidemiology of vector-borne diseases. Annual review of entomology. 2010; 55: 461-483.
- Despommier D, Ellis BR, Wilcox BA. The role of ecotones in emerging infectious diseases. Eco-Health. 2006; 3: 281-289.
- Nath M, Woolliams JA, Bishop SC. Assessment of the dynamics of microparasite infections in genetically homogeneous and heterogeneous populations using a stochastic epidemic model. J Animal Science. 2008; 86: 1747-1757.
- Barribeau SM, Sadd BM, du Plessis L, Schmid-Hempel P. Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system. Proceedings of the National Academy of Sciences. 2014; 111: 3496-3501.
- Demas G, Greives T, Chester E, French S. The energetics of immunity. Ecoimmunology. 2012; 1:259-296.
- Clatworthy MR, Willcocks L, Urban B, Langhorne J, Williams TN, Peshu N et al. Systemic lupus erythematosus-associated defects in the inhibitory receptor FcγRIIb reduce susceptibility to malaria. Proceedings of the National Academy of Sciences. 2007; 104: 7169-7174.
- Hayward AD, Garnier R, Watt KA, Pilkington JG, Grenfell BT, Matthews JB, et al. Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. The American Naturalist. 2014; 184: 58-76.
- Morgan ER, Wall R. Climate change and parasitic disease: farmer mitigation. Trends in parasitology. 2009; 25: 308-313.
- Dhiman RC, Pahwa S, Dash AP. Climate change and malaria in India: Interplay between temperature and mosquitoes. In Regional Health Forum 2008; 12: 27-31.
- Thompson RA. Parasite zoonoses and wildlife: one health, spillover and human activity. Int j parasitology. 2013; 43: 1079-1088.
- Rigaud T, Perrot-Minnot MJ, Brown MJ. Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society B: Biological Sciences. 2010; 277: 3693-3702.
- Van den Ham HJ, Andeweg AC, de Boer RJ. Induction of appropriate T h-cell phenotypes: cellular decision-making in heterogeneous environments. Parasite Immunology. 2013; 35: 318-330.
- Pedersen AB, Fenton A. Emphasizing the ecology in parasite community ecology. Trends in ecology and evolution. 2007; 22: 133-139.
- Graham AL. Ecological rules governing helminth–micro parasite co-infection. Proceedings of the National Academy of Sciences. 2008; 105: 566-570.
- Pedersen AB, Antonovics J. Anthelmintic treatment alters the parasite community in a wild mouse host. Biology letters. 2013; 9: 20130205.
- Koskella B, Brockhurst MA. Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS microbiology reviews. 2014; 38: 916-931.
- Koch H, Schmid-Hempel P. Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system. Ecology letters. 2012; 15: 1095-1103.
- Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nature Reviews Immunology. 2013; 13: 790-801.
- Petrova MI, van den Broek M, Balzarini J, Vanderleyden J, Lebeer S. Vaginal microbiota and its role in HIV transmission and infection. FEMS microbiology reviews. 2013; 37: 762-792.
- Naik S, Bouladoux N, Wilhelm C, Molloy MJ, Salcedo R, Kastenmuller W, et al. Compartmentalized control of skin immunity by resident commensals. Science. 2012; 337: 1115-1119.
- Olivares M, Laparra JM, Sanz Y. Host genotype, intestinal microbiota and inflammatory disorders. British journal of nutrition. 2013; 109: 76-80.
- Stern A, Mick E, Tirosh I, Sagy O, Sorek R. CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome research. 2012; 22: 1985-194.
- Koskella B. Bacteria-phage interactions across time and space: merging local adaptation and time-shift experiments to understand phage evolution. The American Naturalist. 2014; 184: 9-21.
- Kodaman N, Pazos A, Schneider BG, Piazuelo MB, Mera R, Sobota RS, et al. Human and Helicobacter pylori coevolution shapes the risk of gastric disease. Proceedings of the National Academy of Sciences. 2014; 111: 1455-1460.
- Buhnerkempe MG, Roberts MG, Dobson AP, Heesterbeek H, Hudson PJ, Lloyd-Smith JO. Eight challenges in modelling disease ecology in multi-host, multi-agent systems. Epidemics. 2015; 10: 26-30.
- Seabloom EW, Borer ET, Gross K, Kendig AE, Lacroix C, Mitchell CE, et al. The community ecology of pathogens: co-infection, coexistence and community composition. Ecology letters. 2015; 18: 401-415.
- Rynkiewicz EC, Pedersen AB, Fenton A. An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends in parasitology. 2015; 31: 212-221.
- Ellwanger JH, Chies JA. Zoonotic spillover and emerging viral diseases–time to intensify zoonoses surveillance in Brazil. Brazilian Journal of Infectious Diseases. 2018; 22: 76-78.