INTRODUCTION
The dispersion of parasite individuals followed by colonization of a new host lineage, known as host-switching, is a common event observed during the evolutionary trajectory of many lineages of parasites (De Vienne et al. 2013). Initially, host-switching results in the increase of the host repertoire of a parasite (Braga et al. 2021) which, subsequently, when new hosts can impose reproductive isolation it may result in speciation of parasite lineages. This is the dynamic of the oscillation hypothesis (Nylin & Soren 2018). Empirical examples showing high levels of host-switching include symbiotic interactions ranging from host-parasite and plant-insect systems to microbial pathogens, brood parasitism, plant-feeding insects, and even parasitic plants (Nylin et al. 2014; Fecchio et al. 2019; Hayward et al. 2021). Consequently, understanding the factors influencing the success of host-switching and subsequent speciation events is critical for understanding the parasite diversification.
A recently proposed theoretical framework that accommodates the evolutionary dynamics of host-parasite associations, the Stockholm Paradigm (Brooks et al. 2014; Brooks et al. 2019), suggests that parasites perform host-switching by ecological fitting (Agosta & Klemmens 2008; Agosta & Brooks 2020). Ecological fitting is the process whereby organisms colonize and persist in novel environments, use novel resources or form novel associations with other species through a set of traits they already possess (Agosta & Klemmens 2008). The expression of these unexplored capabilities is mediated by the opportunity of interaction (temporal, spatial, ecological), which determines the possibility of encounters between hosts and unfamiliar parasites. After the encounter, and if the interaction is compatible, it is followed by the resolution of subsequent conflicts that emerge from the basic dynamics of “living together”, which should result in co-accommodation (Brooks & McLennan 2012; Araujo et al. 2015).
The chances of parasites dispersing from one host species to another are influenced also by ecological and life-history traits. These include characteristics of all organisms within the interaction system, such as niche similarity among host species, modes of transmission of parasites, dietary preferences of the vector (if there is one), and also ecosystemic characteristics as the host community composition and shared phylogenetic history are relevant factors that define the chances of host-switching (Bush et al. 2006; Jaramillo & Rivera-Parra 2018). Niche similarity among host species is one fundamental element constraining the incorporation of new host species by ecological fitting. This is because the capacity of a parasite species to use new resources is related to the phylogenetic conservatism of the resource provided by the host species. Phylogenetic distance between the original and new host species represents an adequate proxy for the nature of the resource which is tracked by the parasite lineage (Charleston & Robertson 2002; Agosta & Klemmens 2008; Engelstädter & Fortuna 2019). Consequently, the host phylogenetic conservatism can define the arena of possibilities for host-switching.
Several studies have indicated the ubiquity and relevance of host-switching in nature (Engelstädter & Hurst 2006; De Vienne et al. 2007; Cuthill & Charleston 2013; De Vienne et al. 2013; Engelstädter & Fortuna 2019). Although, few have explored the relationship between the switches and the evolutionary histories of host species (see Cuthill & Charleston 2013; Engelstädter & Fortuna 2019). Moreover, the effect of compatibility and interaction opportunity for parasite propagation between host species, as well as the influence of such factors in the patterns of parasite communities remain unexplored. Here, we aim to fill these unexplored gaps by proposing a novel approach to investigate how the intensity of host-switching, mediated by opportunity and compatibility of interaction, affects the phylogenetic history and ecology of the parasites. We proposed a theoretical model based on parasite individuals that can switch among host species during their evolution according to phylogenetic conservatism; that is, the probability of parasites switching hosts decreases with increasing divergence in the evolutionary time of the host. We compared the eco-evolutionary pattern that emerged from the model to nine empirical communities of parasites to predict their intensity of host-switching. These communities were classified by the parasitism type (ecto or endoparasites) and their spatial scale (local or regional). We analysed how the predicted host-switching varied over these classifications and discussed how they are mediated by opportunity and compatibility of interaction.