Disease ecology and pathogeography: Changing the focus to better interpret and anticipate complex environment–host–pathogen interactions

Abstract

Over the past 15 years, disease ecology has become a discipline in its own right. It is fundamentally based on training in ecology and evolution, with solid theoretical foundations and skills in computational biology and statistics, and it differs from a medical approach to the interpretation of disease. It is concerned with how species interactions, including host–pathogen relationships and environmental conditions (e.g. temperature and rainfall), affect patterns and processes of disease presence and spread, how pathogens impact host individuals, populations, communities, and ultimately ecosystem function (Ostfeld et al. 2008). Initially rooted in parasite ecology, particularly among researchers working on transmission cycles and host–disease population dynamics, disease ecology mainly focuses on parasitic and infectious diseases but is not exclusive to them (Ostfeld 2018). A booming subfield currently concerns research linking different areas such as infectious transmission, agriculture development, and development aid policies, notably in the world's poorest countries (Ngonghala et al. 2014). Unlike ecologists, disease ecologists focus on understanding the causes and consequences of the maintenance and transmission of pathogens in animal species, including humans, plants, and communities of species. It has become much more widespread in studies among wild animal species, also in their contacts with domestic species, e.g. livestock, and their interactions with human populations, and much less so in plant diseases and their transmission, which in some respects are the focus of more plant-pathology molecular-orientated research (Guégan et al. 2023a). We cannot say that the development of disease ecology has involved the gradual integration of several distinct lines of inquiry because it is the heir of ecology. It has an ecosystem-based approach and takes into account natural complexity (Johnson et al. 2015, Hassell et al. 2021, Petrone et al. 2023); it develops experimental methods in the laboratory or mesocosms and has an essential background in statistical and mathematical analysis. The spatial scales of disease ecology study are experimental or local and, depending on the questions posed, can extend to the most global scales (Guernier et al. 2004, Jones et al. 2008, Allen et al. 2017, Carlson et al. 2022). In the temporal domain, these can be daily or weekly studies or multi-decadal investigations, such as in disease population dynamics (Keeling and Rohani 2007). By definition, disease ecology is concerned with understanding patterns and processes on large spatial and temporal scales. It integrates different levels of life organization, i.e. from genes to the global ecosystem, which is not the case, or only to a limited extent, of medical and veterinary approaches (Ezenwa et al. 2015). Over the years, however, disease ecology has gained the confidence of other disciplines, particularly the medical and veterinary ones, and is now published in top-leading generalist journals (Mahon et al. 2024, Pfenning-Butterworth et al. 2024, Chevillon et al. 2024). Today, disease ecology is also challenging established dogmas in human and veterinary medicine, reconsidering several aspects of infectious transmission in-depth, raising the question of possible larger host species spectra, and questioning the origin and nature of pathogen virulence (Chevillon et al. 2024).

We are happy to present this special issue on disease ecology in the journal Ecography. At least two other contributions recently published in Ecography could have contributed to this special issue in disease ecology. Both constitute remarkable illustrations of macro-scale studies on host–parasite interactions. They are: Latitudinal distributions of the species richness, phylogenetic diversity and functional diversity of fleas and their small mammalian hosts in four geographic quadrants by Krasnov and colleagues (Krasnov et al. 2023); and Continental-scale climatic gradients of pathogenic microbial taxa in birds and bats by Xu and coauthors (Xu et al. 2023). As illustrated in the different sections of this special issue, disease ecology is a highly interdisciplinary field, drawing on molecular biology and population genetics, immunology, epidemiology, time-series and spatial biostatistics, and ecological and epidemiological modeling. It takes an interdisciplinary approach, often questioning disease distribution, transmission, and intensity from another angle, and this with the wish to propose methods of surveillance, control, and research that are innovative sometimes breakthrough, and more in line with the complexity of the observations made.

In summary, the papers we present in this issue illustrate diverse scientific work and confirm the significant growth of disease ecology in the international research landscape.

The interdisciplinary field of disease ecology has significantly evolved over the past 15 years, establishing itself as a distinct discipline within ecology and evolution. This special issue of Ecography underscores the importance of understanding the ecological and evolutionary dynamics of diseases, emphasizing the intricate interactions between hosts, pathogens, and their environments. The studies presented herein reflect the diverse and growing body of research that characterizes modern disease ecology, spanning topics such as climate change, habitat alteration, and the complex interplay of ecological and disease processes.

The insights from this special issue suggest several areas warranting further exploration. Future research in disease ecology should prioritize integrating advanced climate models with data on ecological interactions to predict disease dynamics under changing environmental conditions. Such studies are likely to benefit from longitudinal studies tracking disease patterns over time, which are essential for identifying trends and informing management practices. Embracing interdisciplinary research that combines molecular biology, genetics, epidemiology, and ecological modeling will enhance our understanding of disease processes. Such an approach will foster innovative solutions for disease surveillance and control and for maintaining environmental health, for instance, by advancing our understanding of biodiversity's role in disease resilience. Interdisciplinary thinking applied to research on the human–wildlife interface (social science, ecology, and epidemiology) will be critical for mitigating spillover transmission risks to humans as human activities increasingly impact natural habitats.

Health geography and, a fortiori biogeography and pathogeography of infectious disease, have suffered a significant loss of importance over the last 30 years in human and veterinary medicine. It is very common in the medical world to speak of ecological studies to describe the finding of spurious correlations, which in medicine are not convincing compared with the gold standard of cohort analysis studies. At the heart of this discrepancy lies the subject of changes in spatial and temporal scales, and scale-dependency, which are major concerns for science in general. Several investigations have been developed to estimate biologically relevant spatial and temporal scales at which environmental conditions impact ecological patterns and processes in ecology (Pease 2024), but this is less common in disease ecology (Becker et al. 2019; but see Halliday et al. 2020, Liu et al. 2022). Temporal and/or spatial varying scales of effect are plausible in host–disease interactions, but they remain largely untested in both theoretical and empirical studies. The debate around the dilution effect is illustrative of this. Disease–biodiversity relationships reveal contrary relationships depending on different parameters, like disease transmission categories, land types or spatial scales. Temporal and/or spatial variation in scales of effect can strongly depend on available variables at scales of interest, making that host–pathogen interactions and changes can be best explained by changes in human development at local scale because these parameters are measured and available, and explained by climatic variables and climate change at largest scale, at which these variables can be obtained, i.e. the Elton's sound hypothesis (Chavy et al. 2019 for an illustration on human leishmaniasis in southern America). This also indicates an important issue about collected data since biotic and human behaviour and attitude data exist at lower scales and quasi-absent at largest scales when abiotic parameters, e.g. meteorological data, dominate. We strongly encourage disease ecologists towards this research avenue in order to elucidate host–pathogen and also tri-trophic interactions at specific scales of effect and deciphering their ecological and evolutionary drivers. This will help disease ecology to be better understood, taught in veterinary and medicine schools, and interpreted by disciplines that are either reticent or still too hegemonic, and to play a part in the process of aiding animal and public health efforts worldwide.

Disease ecology is poised for continued growth and impact in a world where change is visible at every observable scale. The advances in our field will be driven by the need to understand and take action to address the complex challenges of infectious diseases. This special issue highlights the current state of knowledge across numerous systems and scales, and sets the stage for future research to further unravel the web of interactions that define disease ecology.