Evolutionary perspectives on human infectious diseases: Challenges, advances, and promises

Modern biomedicine has contributed remarkably to the reduction of infectious diseases worldwide, including the eradication of smallpox and the control of common childhood diseases (e.g., polio, measles, rubella) that once claimed millions of lives and caused suffering of tens of millions. This has been made possible through improved diagnostics, surveillance, therapeutics, vaccines, and an associated health system infrastructure. These achievements can be largely credited to advances in biomedical sciences and their application in the 20th century. The spectacular advances in the biomedical sciences were in turn a consequence of the emergence and widespread acceptance of the biomedical paradigm, in which the discovery of microbes and establishment of 'germ theory' had played a central role. By the 1960s, a sense began to prevail that infectious diseases had been conquered, or were at least conquerable in the case of malaria, dengue, and other vector-borne diseases (VBD) that appeared to be "in retreat." Yet, by the 1980s, with the appearance of the HIV/AIDS pandemic and followed by new antimicrobial-resistant strains of bacterial pathogens, confidence began to erode. Major setbacks also increasingly became apparent in the efforts to control VBDs particularly with the resurgence of malaria and dengue worldwide (WHO, 2016). An increasing number of historically localized or otherwise geographically confined VBDs began to spread and even jump continents, with the arrival of West Nile virus and Zika virus in the Americas being the most prominent of many examples. Such pathogens, identified decades ago in their native habitat and hosts as part of natural history studies, were long considered to be of relatively little public health concern or apparent impact (Lederberg, Shope, & Oaks, 1992; Packard, 2007). Human population growth and anthropogenic environmental changes, accelerating with an unprecedented intensity and scale particularly since the mid-1900s, are increasingly recognized as underlying much of the emerging infectious diseases (EID) problem (Myers & Patz, 2009; Myers et al., 2013; Whitmee et al., 2015). These disease emergence drivers emblematic of the era of modern development can be seen as consequences of modern medical and hygiene interventions introduced a century earlier. Together, they radically modified (and continue to alter) landscapes and ecosystems worldwide producing what has become a continual state of social, ecological, and evolutionary imbalance (McNeill, 1976). Among the environmental changes, global climate change has become widely accepted among experts as a significant contributor to these imbalances that will increasingly influence infectious diseases transmission, yet in ways that are difficult to predict (Altizer, Ostfeld, Johnson, Kutz, & Harvell, 2013; Lafferty, 2009; McMichael & Wilcox, 2009). The complexity of factors and processes underlying infectious diseases and their transmission go well beyond the scope and analytic resolution of biomedicine (and conventional biomedical training), requiring a complementary framing approach capable of acknowledging and assessing cross-scale influences, context dependency, and the constant 'arms race' between co-evolving organisms (Van Valen, 1973). Evolutionary biology provides these scientific foundations to help refine our understanding of not only the meaning of health and disease (Stearns & Koella, 2008) from the standpoint of adaptation (or maladaptation), but also improve our understanding of the mechanisms underlying infectious disease transmission dynamics within social-ecological systems (Horwitz & Wilcox, 2005; Wilcox & Echaubard, 2016), context-dependent virulence and more effective treatment and control strategies (Echaubard, Sripa, Mallory, & Wilcox, 2016; Nesse, 2008; Restif, 2009). As such, evolutionary biology as a framing approach and methodological toolkit is a needed component of integrated disease control and prevention (Allegranzi et al., 2017) and sustainable health development aligning with the recently adopted sustainable development goals (SDGs), as part of the 2030 Agenda for Sustainable Development (Carroll et al., 2014). This special issue is an attempt to present an up-to-date appraisal of the challenges, current advances, and promising research avenues where evolutionary principles and their ecological corollaries can be applied in research as a basis for human infectious disease interventions. Accordingly, the contributions published in this special issue together present an illustration of the diverse benefits of combining biomedical and public health perspectives with evolutionary causation in the context of infectious diseases for major infectious agents (Table 1). A main challenge of mainstreaming evolution into medicine and public health lies in the often very pragmatic and urgent nature of these fields (e.g., outbreak mitigation; Nesse & Stearns, 2008) and the relatively time-consuming nature of framing questions, interventions, and policies following evolutionary principles, which imply a long-term preventive vision rather than a short-term curative domain of action. However, policy-oriented research and intervention informed by evolutionary biology have the potential to not only effectively mitigate urgent crises but also anticipate, minimize, and respond to the evolution of unwanted epidemiological traits (e.g., antimicrobial resistance). Accordingly, the articles compiled for this special issue present a selected panel of evolutionary applications for infectious disease control, together providing relevant avenues for future research and sustainable disease prevention strategies. The articles published in this special issue are organized based on their underlying evolutionary innovation and public health implications and not necessarily on the disease study systems the authors are using to address their research questions. A range of disease systems, from macroparasites to microparasites (sensu Anderson & May, 1981), are examined through modeling, experimental and observational research designs as well as describing novel framing approaches. As an opening paper, Kosoy and Kosoy (2017) explore the multiple dimensions and related complexity of host–pathogens interactions revealed by the novel genetic and genomic data, along with extensive environmental parameters being acquired using newly developed computational tools. They highlight the need for flexibility in studying natural systems of zoonotic pathogens with respect to how we choose perspectives within a continuum between unrestricted diversity of related parameters and well-defined roles played by infectious agents, potential and actual animal hosts, and environmental variables. They proposed a model of investigation that requires a dynamic shift of perspectives along the simplicity–complexity ('simplexity') dimension emphasizing the difficulty to accommodate dual representations of both the subjective nature of investigations of zoonotic pathogens and much more objectively derived information, for example, coded in the genetic structure of DNA or in observing the morphology or behavior of bacteria. This also speaks directly to the issue of "problem framing" alluded to in this introduction where tools and perceptions emerging from biomedical sciences do not necessarily accommodate evolutionary-based predictions or public health implications. Arguably the most widespread recognition of the importance of evolutionary biology for public health and medicine is in the context of the emergence of resistance to antimicrobials and insecticides. Sternberg and Thomas (2017) explore the overlaps between understanding and managing insecticide resistance in agriculture and in public health with the aim to identify best practices in resistance mitigation strategies in the context of vector-borne disease interventions. They argue that the success of insecticide resistance management strategies is strongly dependent on the biological specifics of each system and that the biological, operational, and regulatory differences between agriculture and public health limit the wholesale transfer of knowledge and practices from one system to the other. Nonetheless, the authors argue that there are some valuable insights from agriculture that could assist in advancing the existing Global Plan for Insecticide Resistance Management (IRM). Accordingly, the authors suggest that for IRM strategies to succeed in public health, there needs to be a shift away from choosing vector control tools or strategies based on direct cost, toward factoring in the benefit of preserving susceptibility. Focusing on Malaria, Huijben and Paaijmans (2017) analyze the evolutionary consequences of the way antimalarial drugs and insecticide-based interventions are currently implemented, which is leading to resistance and may ultimately lead to control failure. The authors describe how evolutionary principles can be applied to extend the lifespan of current and novel interventions highlighting in particular how understanding fitness costs arising from expressing, utilizing, and maintaining molecular or metabolic pathways of resistance will be essential to mitigate resistance evolution. They continue arguing that similar to insecticide resistance management strategies, large heterogeneity in drug exposure can be created in space (host mosaic) or time (drug rotation) or by deploying different compounds simultaneously (mixed treatment) and that better resistance management is achieved if drugs can be combined that select for alternative allelic versions of the target locus. Glunt et al. (2017) further discuss the challenges of insecticide resistance in the context of malaria, with a specific focus on pyrethroids impregnated long-lasting insecticidal bed nets (LLINs) and their efficacy in preventing malaria. About 1 billion LLINs, a major vector control tool, have been distributed in Africa in the las

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