Introduction

Understanding the ecological mechanisms influencing the origin and evolution of host-pathogen associations is fundamental and it became a vigorous area of research in human health, agriculture, and food security, during recent years (Heard and Hauser, 1995; Woolhouse et al., 2005; Brooks et al., 2014). These studies are of special interest, considering the so-called crisis of Emerging Infectious Diseases (EIDs), present and future (Brooks et al., 2019). This crisis is the fulfilling of the prediction that EIDs are ”accidents waiting to happen” (Brooks and Ferrao, 2005).
However, such studies are strongly influences by the researcher’s perspective of its accepted theoretical evolutionary framework (see a summary of this under a historical perspective in Nylin et al. 2018; Brooks and Boeger 2019; Brooks et al. 2019; Agosta and Brooks 2020), often influenced by the perspective that parasites are ultimate specialists (Agosta et al., 2010). Traditionally, the nature of host-parasite/pathogen associations is regarded as a symmetrically selective interaction built under a 1:1 relation in a context of strong selective pressures (Kaltz and Shykoff, 1998). This vision generated a paradox - the Parasite Paradox (Agosta et al., 2010). The Parasite Paradox results from the accumulation of studies on host-parasite evolution in the last 40 years that, even utilizing protocols strongly biased towards co-speciation, still detected a large amount of what has been called to this date as host-switching (Krasnov and Shenbrot 2002; Hoberg and Brooks 2008; Agosta et al. 2010; De Vienne et al. 2013). Increasing phylogenetic and historical evidence points out that expansion in host range (=host repertoire according to Braga et al. 2018) is a primary dynamic in pathogen evolution and ecology. The complex structure of host-pathogen associations strongly sustain that the widely held evolutionary paradigm, which has been conceptually dominant for a century, cannot accommodate the present knowledge on the origin and evolution of symbiotic associations (Nylin et al., 2018).
The Stockholm Paradigm (Hoberg and Brooks, 2015; Brooks et al., 2019) provides such a theoretical framework. The fundamental element of this new perspective on the evolution and ecology of associations is the recognition that the vast majority of ecological changes occur through Ecological Fitting (Janzen, 1985a; Agosta and Klemens, 2008). The other two elements of the Paradigm - the Oscillation Hypothesis (Janz and Nylin, 2008) and the Taxon Pulse (Erwin, 1985) - are thought to represent emergent properties of the complex system composed of species that interact – with other species or the environment - under the ability to change by Ecological Fitting (Janzen, 1985; Brooks et al., 2006; Agosta and Klemens, 2008; Brooks et al., 2019).
Under the framework of the Stockholm Paradigm, Araujo et al. (2015) developed a mathematical model that evaluated the colonization of new host species by an evolving population. The simulations support the postulate that host colonization by Ecological Fitting is likely ubiquitous. Among other conclusions, Araujo et al. (2015) also suggested that successful colonizations are not limited to a high degree of compatibility of the pathogen population to the new host. Support for this perspective has been recently revealed by empirical experimentation (Khokhlova et al., 2020). Araujo et al. (2015) also indicate that poorly adapted pathogens can survive in a new host despite being in a sub-optimum condition, whereas they did not explicitly explore populational parameters that might influence the pathogen’s colonization success.
The Stockholm Paradigm was recently expanded to incorporate any process of ecological change in evolution (Agosta and Brooks, 2020), including invasive species (Hoberg, 2010), phytophagous insects (Agosta, 2006; Nylin et al., 2018), ecological associations and community structuring (Wilkinson, 2004), and plant–bird pollination (Janeček et al., 2020). Colonization of new conditions, reflecting change from the ancestral selective pressure, most likely occur by ecological fitting in association to environmental and ecological disruptions (Brooks et al., 2019) and far less frequently by immediately preceding releasing mutations (see also Morse 2001).
Hence, in the present work we expand the study of Araujo et al. (2015) using simulations based on an individual-based model (IBM) considering elements of the Stockholm Paradigm to explore the significance and interaction of selected parameters that could be considered important for the success of colonization of new host species. The model is focused in host-pathogens systems, as Araujo t al. (2015). Although methodologically different, it can be applied to equivalent ecological changes, such as similar studies that developed other type of models to study, for instance, invasive species (e.g. Pȩkalski 2003). The tested parameters are the reproduction rate, the rate of novelty emergence (analogous to mutation rate), and the propagule size of the founder pathogen population, all of which are frequently considered as key population parameters in studies of biological invasion and epidemiology (Woolhouse, 2001; Dobson, 2004; Lockwood et al., 2005; Woolhouse et al., 2005; Braendle and Flatt, 2006; Hoberg, 2010; Hurford et al., 2010; Briski et al., 2012; Johnson et al., 2015; Mason, 2016; Gould and Stinchcombe, 2017).
The resulting simulations strongly support previous accounts on the process of colonization of new environmental conditions - in this case of new host-pathogens associations under an ecological perspective - and provides new insights into the process of emerging infectious diseases. The overall result of the simulations provides instrumental support to the recognized crisis of emergence of new infectious diseases (Fauci, 2001; Morens et al., 2004; Brooks and Ferrao, 2005; Brooks et al., 2014; Hoberg and Brooks, 2015; Mondragon et al., 2018; Morand and Figuié, 2018).