Human population increase, industrialization, and geopolitical problems accelerate global changes causing significant damage to biodiversity, extensive deterioration of ecosystems, and considerable migratory movement of both mankind and species in general. These rapid environmental changes are linked to the emergence and re-emergence of infectious and non-infectious diseases (Figure 1). Over recent years, certain zoonoses, such as bird flu or the Ebola and Zika viral epidemics, have illustrated this fact to the whole world demonstrating the interdependence of human health, animal health, and ecosystem health. Coming from the “One Medicine” concept (1) that advocates a combination of human medicine and veterinary medicine in response to zoonoses (2), the “One World - One Health” concept¹ was created in 2004. The novelty was the incorporation of the ecosystem health, including that of wild fauna. The “One Health” initiative² therefore constitutes a global strategy highlighting the need for an approach that is holistic and transdisciplinary and incorporates multisector expertise in dealing with the health of mankind, animals, and ecosystems (3) (Figure 2).

When one considers the multiple factors at play and the complexity of public health issues, it is clear that the “One Health” holistic approach (4) cannot be disassociated from the notion of ecological health (EcoHealth). The underlying premise is that the health and well-being of the human population will be more and more difficult to maintain on a polluted planet suffering from social or political instability and ever-diminishing resources. Supporting that view, the European ministers responsible for health and the environment as well as the World Health Organization (WHO) regional director for Europe met on June 15, 2017 in Ostrava, Czech Republic for the sixth ministerial conference on Environment and Health. They recognized that “environmental factors that could be avoided and/or eliminated cause 1.4 million deaths per year” in the WHO European Region. They declared that “public authority shares the common responsibility for safeguarding the global environment and for promoting and protecting human health for all environmental hazards across generation and in all policies.” Paving the way for ambitious integrative initiatives in the One Heath framework, researchers in “Ecohealth” and its practitioners implement systemic and integrated practices to promote sustainable ecosystemic services linked to the concept of health (human, animal, and ecosystem) and to social stability. Thus, the One Health concept provides a way of looking at complex systems and approaching processes leading to undesirable effects such as disease emergence, etc. It thus encourages and promotes the interdependence, coexistence, and evolution of living beings and their environment, which is itself in a state of constant transformation (5).

However, after just over 10 years in existence, the “One Health” concept, which predicted the integration of the interface with ecosystems in the “One Medicine” concept, has not quite completed its transformation (6). The documents and publications on the “One Health” approach, and the strategic framework developed around it, have largely focused on the battle against emerging zoonoses originating in domestic (7) or wildlife (8) and/or their interactions (9), without really considering the role of inclusive ecosystems (10). Thus, a quick review of scientific investigations claiming to adhere to the “One Health” concept clearly reveals that they only mention the environment and its biotic and abiotic components as the scene of transmission, often reduced to global planetary changes or the Anthropocene. Very few studies deal effectively with the ecology of transmission and the ecology of health meaning developing an ecological and progressive epidemiology linked to components of biodiversity, ranging from physiological stresses on populations to changes in habitat, or linked to ecosystem processes (11, 12, 13).

One of the major challenges in the successful integration of the environment alongside human and animal health in the “One Health” triptych is the capability to define the state of health of our ecosystems. Ecology researchers face a growing demand from administrators for detailed, relevant information on the health and desired equilibrium or dynamics of multifunction ecosystems to guide decision-making on sustainable development, species conservation, and human, animal, and plant health (14). This calls for the definition of shared indicators for ecosystem health (biodiversity, ecosystem services, desired “equilibrium”, and “evolutions” on relevant space–time scales, etc.).

When the “One Health” concept was conceived, initial collaboration between human medicine and veterinary medicine resulted in an inevitable research bias toward zoonotic diseases (15), temporarily ignoring the important question of chronic non-infectious diseases, which are the leading cause of global human mortality. Nowadays, the “One Health” concept hopes to extend to other fields, such as antimicrobial resistance, ecotoxicology, or health in urban environments.

In this review article, we discuss the need of incorporating ecological, evolutionary, and environmental sciences into One Health approaches for an innovative and effective control of both infectious and multifactorial non-communicable diseases. We next provide examples in which the integration of the ecosystemic component of the One Health concept enabled deciphering the processes underlying disease emergence and re-emergence. Finally, we discuss operational brakes that still limit the application of the concept, its ambitions, and future challenges.

Some key examples illustrate the degree to which the adoption of a “One Health” approach is both consensual and particularly effective in deciphering the processes underlying the emergence and re-emergence of diseases.

Major barriers to the effective integration of “One Health” need to be removed (i) for the systematic implementation of a “One Health” strategy and (ii) for the development of operational solutions that both respect environmental health and its future and are realistic in the face of the urgency of medical care for patients.

A major barrier to the development of “One Health” approaches is very clearly the lack of communication between human and veterinary medicine, agronomy and ecological, environmental, and evolutionary science. Removing this major impediment implies the integration of sufficient understanding of other disciplines, multidisciplinary approaches, and the aims and conditions of their implementation. This can be formulated at different levels.

From a training point of view, it is essential to include ecology and evolution in any medical, veterinary, and agronomic training (109, 110). Although relatively recent, a number of these training courses are currently being developed around evolutionary medicine. This initiative should be supported and strengthened in the future.

From a research point of view, improved scientific cooperation requires the development of collaborative national and international research networks (including within Europe). The integration of southern countries, with their diverse intertropical ecosystems and biodiversity hot spots, is absolutely vital as they represent genuine natural laboratories for the implementation of the “One health” concept in the face of demographic and sanitary transition resulting from global changes. Networks must also include a maximum number of key players in research, representing various disciplines and specializing in different levels of organization of living beings, and spatial and temporal scales. They must work together toward the implementation of shared training programs, tools, and protocols with a shift from research generating basic and isolated knowledge to translational research leading to systems and implicational knowledge. This certainly needs a mentality change not only from researchers but also—and even more importantly—from research funding bodies. Scientific cooperation also needs better access to knowledge, which is currently partially blocked (intellectual property, patents), thereby depriving certain key players of diagnostic criteria or fundamental knowledge (81). Observation tools and data management programs should also be supported. Long-term monitoring of transmission or exposure systems must be organized and supported by appropriate means and measures, including outside peaks of visible emergence, taking into consideration the different spatial and temporal scales relevant to the organisms in question (e.g., multiannual demographic variations of organisms, landscape changes, practice changes, rearrangement of communities in response to these factors, etc.). This requires the implementation of policies to collect, capitalize, secure, and make available the data derived from ambitious research (database management, observatories, etc.). In addition, promoting multidisciplinary integrative approaches is needed for the development of a progressive health (human and animal) ecology, which is based on acquired expertise and methodology in immunoecology and endocrine-epidemiology (111) and links the study of proximal factors (mechanisms) to their ongoing evolutionary consequences (112, 113). It is also necessary to support work into the definition of ecosystem services for the regulation of infectious or toxic risk (contributing to the requests of the, Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services).

From a political point of view, it would appear necessary to implement a gradual reinforcement of biosecurity including production, transport, and transformation of biological resources. It is additionally absolutely essential to break down the sectoral partitioning that exists between public health, agronomy policy, and other sectors of activity (27). Indeed, current sectoral partitioning trends foster infectious risk. For instance, to date the agriculture/public health interface does not come under the competences of farmers nor vector control services, which increases the development of insect vectors resistant to agricultural insecticides. The synergy of a partnership between scientists, farmers, and the vector control services would initiate pluridisciplinary research programs whose goal would be to protect the crops while reducing the populations of vectors as much as possible. Similarly, sectoral partitioning increases the emergence and the spread of microorganisms that are antibiotic-resistant as a result of spreading slurry from farms using antibiotics or by the increase in size of host populations of pathogenic agents. It is therefore clear that a comprehensive review of industrial agriculture and farming practices is vitally urgent. Overall, significant efficacy gains can be achieved through intersectoral cooperation in a “One Health” approach. This should include a control at source, which is often more cost-effective than fighting a disease. This supposes (i) cooperation in terms of monitoring and diagnosis for a quicker and more precise diagnosis; (ii) cooperation in terms of preventative measures, such as vaccination, to increase coverage; and (iii) a detailed and immediate communication to reduce the number of cases (114).

Remarkably, a purely economic view also calls for a global approach of Health that relies on both “prevention at source” for animals and “control” for humans (115). It has been estimated that this two-sided approach would cost between 1.9 and 3.4 billion dollars per year to implement and optimize this approach, a sum which is far below the annual average of 6.7 billion dollars of economic losses historically suffered as a result of epidemics (114). These methods will require the consolidation of regional, national, and international approaches to biosecurity for the control of human, animal, and plant diseases and the implementation of an integrated, interdisciplinary, intersectoral approach to the monitoring of and investigation into diseases common to man and animal. A first necessary step is the development of a database that includes a corpus of essential statistics on demography, the sanitary situation, health determinants (human, animal, and ecosystem), and risk factors. These multi- and intersectoral collaborations, nourished by the results of relevant research, are also essential in identifying the bio-economically, socially, and ecologically acceptable compromises between (sometimes) contradictory management objectives (food production, health, biodiversity preservation, etc.).

In addition to prevention, ecology today must be able to offer the authorities innovative solutions to vector control (antivector fight) and pathogenic infectious agents (remediation) that are more ambitious and less destructive to biodiversity and ecosystems than those currently deployed. With regard to antibiotic resistance, research programs working on the identification of new anti-infectives must henceforth consider the risk of resistance emergence from the moment that new therapeutic agents are developed.

The insufficient consideration of certain key components in the implementation of the “One Health” concept can be highlighted. Particularly, the wildlife component and numerous related ecological issues (community ecology and evolutionary ecophysiology) are still neglected (116), as are certain environmental science components (soil and climate) (117). Additionally, social, legal, and economic sciences are similarly marginalized (118).

However, social sciences play a major role in the construction of the problems facing “One Health” research. The understanding of infectious or toxic risks cannot simply be reduced to its biological or chemical components. It is also essential to take into consideration the vulnerability, variability, and susceptibility of human societies as well as the different ways they interact with animals and ecosystems. The “One Health” concept, which promotes an interdisciplinary and intersectoral approach, must therefore engage at different levels of health governance, from a global level right down to a local level, by encouraging participative approaches that bring together communities, scientific experts, administrations, and other key players (NGOs, industry, legal experts, etc.). Infectious and toxic risks must also be addressed through their perceptions and impacts to contribute to the improvement of surveillance and prevention systems and the resilience of societies in the face of sanitary crises.

The issue of plant health as a full component of “One Health” concept is a challenge to be urgently resolved (119). In fact, human health and animal health are directly or indirectly dependent on plant health, as the latter is essential as food resources, phytomedecine, land management, etc. In terms of basic knowledge, investigations in plant ecology and epidemiology have provided useful data for understanding the mechanisms of virulence and adaptation of pathogens in humans and animals. A renowned example is the discovery by botanists of interfering RNA as a key component in gene regulation, including host–pathogen interactions (120). While some plant pathogens may pass the species barrier and cause nosocomial diseases, such as the Burkholderia complex bacteria responsible for human cystic fibrosis (121), others belonging to enteric bacteria (Salmonella, Escherichia coli, Shigella, etc.) are plant inhabitants that can cause food contaminants that are harmful to human (122). Thus, raising the concept of “One Health” to a realization requires also access to a good plant health through a productive (yield, quality, nutritional value, and biosafety) and sustainable (reducing pesticides and chemical fertilizers, encouraging culture rotation practice, biofertilization, etc.) agriculture.

The question of ethics should also be more widely integrated into the “One Health” concept. If ethics are referred to essentially through bioethics and the ethics of animal health, other components are often neglected. This is the case for environmental and biodiversity ethics, social science ethics, and the ethics of various legal concepts, such as human rights, the rights of indigenous people, environmental justice, and animal rights. The Nagoya Protocol to the Convention on Biological Diversity is one of the ethical and legal frameworks which are legally binding on scientific research, generating new consequences on the access to and sharing of microorganisms, human, animal and plant samples, data, and traditional and local knowledge and skills. Far from being a new constraint, it is an opportunity to reflect on the role of scientific research in our societies (123).

This review illustrates how crucial it is to consider ecological, evolutionary, and environmental sciences in (i) understanding the emergence and re-emergence of infectious and non-communicable chronic diseases and (ii) in creating innovative control strategies. However, the actual organization of research and the sectoral allocation of resources in our societies still limit the development of transdisciplinary approaches and integrated operational actions. Removing the interdisciplinary barriers that still separate ecological, environmental, and evolutionary sciences from human and animal medicine is a major challenge to the implementation of the “One Health” concept, which moves beyond science and impacts politics (health, agriculture, aquaculture, land management, urbanism, and biological conservation), law, and ethics. There is a need to provide evidence on the added value of “One Health” approach for governments, researchers, funding bodies, and stakeholders (124). Finally, promoting the integrative benefits expected of the “One Health” concept requires a new interface with human, social, and legal sciences that remains to be built.

All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.