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.