DISCUSSION
In this study, we proposed a theoretical model to investigate how the
intensity of host-switching, mediated by opportunity and compatibility
of interaction (using host phylogenetic distance as proxy), shapes the
phylogenetic history and ecology of the parasites. Our results indicated
that different host-switching intensities can drive distinct ecological
and evolutionary patterns of the parasite lineages. The model reproduced
the eco-evolutionary pattern of all analysed empirical cases, but the
range of predicted host-switching intensity varied among them. The
parasitism type did not explain this variation, but the extent of the
spatial scales of the empirical cases analysed present some correlation
with the predicted intensity of host-switching. Host-switching intensity
was higher for local empiric cases when compared to regional scale
cases.
Variation in host-switching intensity through history influences the
resulting eco-evolutionary patterns of the parasites involved. When the
frequency of host-switching is sufficiently high, parasites can maintain
the gene flow among infrapopulations of distinct hosts and speciation
does not occur. On the other hand, if the gene flow is reduced,
reduction in host-switching favours parasite speciation (see the
eco-evolutionary dynamics in the movie available in supplemental
information III S16 and S17). This was the general pattern observed for
all simulated communities, strongly suggesting that host-switching is an
important driver for parasite evolution. During simulations, in line
with the oscillation hypothesis, species first increase their host
repertoire (generalize) and then speciate (specialize) (Janz & Nylin
2008; Braga et al. 2018).
Our results also support that host phylogenetic relationship is a good
predictor of host-switching - i. e. host-switching is most likely to
occur between related host species. There is probably some common trait,
such as a specific physiological mechanism that has evolved and may be
being expressed through phylogeny. The dispersion of parasites followed
by colonization of a new host lineage has been increasingly investigated
in the Stockholm Paradigm (Agosta et al. 2010; Araujo et al. 2015; Nylin
et al. 2018; Brooks et al. 2019). For a parasite lineage, the closer
(phylogenetically) the species of the original and new host, the greater
the possibility that the necessary combination of elements that compose
the adequate resource is conserved or, is at least quali- and
quantitatively similar. Hence, phylogenetic proximity has been widely
recognized as a potential criterion to anticipate the emergence of new
associations (Streicker et al. 2010; Damas et al. 2020). However, this
is not a universal criterion, as compatibility appears to be also
modulated by other biological elements (e.g. morphology, genetics,
ecology) associated with the opportunity of encounters between hosts and
parasites. This theoretical framework has provided evidence on how the
host-switching mediated by compatibility and opportunity of interaction
influence the dynamics of parasitic interactions leading to species
diversification (Agosta et al. 2010; Nylin et al. 2018; Brooks et al.
2019). The possibility of encounter between potential symbionts in time
and space, emerges from geographic distributions, ecology, and inherent
biological traits of the associates. Compatibility emerges from the
ancestral capacity in which both must be physiologically compatible to
establish a long-term association. Compatibility and opportunity should
occur simultaneously to allow the establishment of new associations.
Thus, any factor that influences the compatibility and/or the
opportunity among hosts and parasites may affect the intensity of host
switching by parasites. Such factors can include biological and/or
spatial variations, which may explain the varied predicted intensities
of host-switching among analysed communities.
The parasitism type (ecto vs endoparasites) had no effect on the
predicted intensity of host-switching by parasites. Ectoparasites have
direct contact with the external environment, while endoparasites may
have free-living infective stages but spend most of their life without
direct contact with the environment (Bush et al. 2001). Because of this,
higher host-switching intensity could be expected in ecto rather than
endoparasites due to the amount of time under variable environmental
conditions that could lead to a stronger selective pressure to use a
broader array of hosts. In addition, all parasites analysed here are
monoxenic and differ by the transmission strategy: ectoparasites can
transmit between host individuals during adult stages, while the
endoparasites only during the larval stage. Hence, the strategy of
transmission of the ectoparasites allows successive host-switching by an
individual parasite, while endoparasites are restricted to less
host-switching events. This wider possibility of transmission was
assumed to favor a higher intensity of host-switching by ectoparasites
than by endoparasites (Boeger et al. 2005). Consequently, as we could
not detect significant differences between the empirical networks
analysed herein, our results do not support these hypotheses. For
instance, an alternative explanation may be linked to the generalization
that propagule size compensates for the wider possibility of
transmission. Moreover, there is great heterogeneity in the
characteristics of both ecto and endoparasites. Each parasitism type
includes a great diversity of organisms, with profound differences in
their evolutionary history and biological characteristics (for example,
by comparing species of the genus fleas, lice, feather mites, helminths,
platyhelminthes), which may be more influential to host-switching
intensity than the general site of parasitism type itself. Expanding the
analyses to a broader sample of empirical networks, including variations
in the reproductive strategies may provide important insights on this
question.
Unlike parasitism type, our results indicate that host-switching
intensity is higher on local than regional spatial scale. The
opportunity for interaction is increased in host communities at a local
scale, as this reduces the likelihood that geographic barriers exist,
hampering the possibility of encounter. This is evident when comparing
rodent and flea cases at regional (ID. 4) and local spatial scales (ID.
5). Similarly, since the cases of Rhabdias spp. and frogs (ID. 8)
are defined geographically (and not by host taxa) it was assumed that
host-switching and ecological fitting were evolutionarily more important
than association with particular host taxa (Kuzmin et al. 2014; Müller
et al. 2018). However, the majority of the empirical cases analysed
herein and elsewhere suggest that switches are responsible for parasite
diversification and distribution (see Krasnov et al. 2016; Dona et al.
2017; Patella et al. 2017).
Although the model can reconstruct eco-evolutionary patterns of
empirical cases, it has some limitations. First, there is no variation
of the carrying capacity imposed by each host species; second, variation
in abundance and spatial distribution are not explicitly considered;
third, the parasites compete for the same resource (in contrast, each
parasite species would have a carrying capacity); and finally, selective
pressure is not explicitly modelled. The solutions to these limitations
would make the model more realistic but also demand more computational
time and increase the number of parameters to be evaluated. Thus,
quantitative comparisons of predicted host-switching intensities should
not be done, but the qualitative implications, as already discussed.
Furthermore, we emphasize the need for empirical phylogenetic studies,
since the availability of phylogenetic data on parasites is still
scarce. Phylogenetic data on parasites are extremely important to
clarify the role of host-switching in the ecological and evolutionary
patterns of parasite lineages.
Our results indicate that the intensity of host-switching, mediated by
opportunity and compatibility of interaction, influence the phylogenetic
history and ecology of the parasites. As suggested by the Stockholm
Paradigm, parasites may already carry the ancestral capabilities to
switch to new hosts, and here we showed that the host evolutionary
history, when associated with opportunity for contact and interaction
compatibility (opportunity + compatibility are represented by the
parameter r ), creates the possibility for the colonization of a
new host species. Our study represents a first attempt to model and
evaluate the empirical evolutionary history of hosts as a proxy for
parasite resources and offers a new approach to understanding the
eco-evolutionary patterns of parasite species. This model has important
implications for predicting changes in host lineages in situations of
environmental or climatic changes or yet in cases of emerging diseases
where the parasitic host switches can cause disease outbreaks.