Discussion
Host selection (= choice or preference) is a trait of high relevance for
the study of infection dynamics, which has drawn much attention for
parasitoids and vectors (e.g. Henry et al., 2009; Campbell et al.,
2013), but which has been often neglected for other parasites. Parasites
differ in their ability to drive the encounter of hosts. While some
parasites rely on contact between hosts or passive encounter of a
free-living stage to reach compatible hosts, motile and vector-borne
parasites are able to find hosts in a less random manner. Discriminating
among hosts provides the opportunity of maximising fitness by selecting
the most suitable options. Little is known about how parasites select
hosts or the degree to which such choices are linked to their success,
but some empirical evidence supports the notion that host preference is
adaptive. Ectoparasitic mites (Spinturnix spp.) are more
attracted by female and subadult bats than by male bats, and they
survive longer in the former, indicating an adaptive selection of the
more beneficial type of host (Christe et al. 2007). Similar evidence of
host preference in relation with host competence was observed in
multi-host systems. Cercariae of trematodes in the family Plagiorchiidae
were put in selection chambers to choose among tadpoles of four host
species, and the choice pattern observed was negatively correlated with
the level of resistance of each host species. The preferred host species
was that with the greatest proportion of metacercariae encysted, whereas
the least chosen host was the one in which most cercariae failed (Sears
et al. 2012). In the Philornis- multihost system, larvae that feed
on the main host have higher chances of surviving than those that
parasitise alternative hosts (Manzoli et al. 2018).
Most previous work on host selection has been conducted in experimental
settings, under unnatural circumstances and providing limited
opportunities. These experiments can establish differential
attractiveness among hosts, but are unable to evaluate the degree to
which parasites can reliably differentiate among an entire assemblage of
alternative hosts in natural contexts. The Philornis- multihost
system provides the rare opportunity to evaluate host attractiveness in
the real world (for a detailed description of the advantages of this
system see Suppl. Mat. in Manzoli et al. 2018). It is noteworthy that
the longitudinal studies conducted here not only provide correlational
evidence (very strong associations between putative cause and alleged
effect), but also demonstrate robust temporal coherence, and the
analyses controlled for potential confounders that may cause spurious
associations (Höfler 2005).
Gravid Philornis females can fly relatively long distances
seeking bird broods that could be hosts of their larvae. Being the
encounter the result of such an active search, there is opportunity for
evolving capacity to discriminate among hosts and select the ones which
maximise larval fitness (Forbes et al. 2017). Our results showed that,
in this system, the parasite has an enormous ability to discriminate
between hosts of differing quality, and that host selection depends on
the structure of the host assemblage and on the size of the parasite
population (host demand). The probability and intensity of parasitism in
alternative hosts increased as better hosts were less available,
especially with growing host demand. It is worth highlighting that the
results observed were drastic: bad hosts were virtually not used at all
when better alternatives were sufficiently available, even at high host
demand levels.
Another study in a different system did not find such context-dependency
of host selection. Under experimental conditions, motile cercariae of
the trematode Ribeiroia ondatrae were attracted differentially by
five alternative hosts (Johnson et al. 2019). Unlike the experiment by
Sears et al. (2012), the attractiveness was not correlated with host
competence. The most preferred host was the bullfrog (Rana
catesbiana ), a non-native and large-bodied species in which most
cercariae failed to encyst. The attractiveness of the most competent
host in that experiment, Peudacris regila , was not altered by
variations in the assemblage composition, including presence/absence of
bullfrogs. However, bullfrog presence decreased infection for the other
3 alternative host species, which is in coincidence with the effect of
Great Kiskadees on Thornbirds observed in this work.
In response to environmental variability, parasites can evolve from
generalism to specialism or vice versa (Lievens et al. 2018). Dietary
specialisation is predicted to evolve when the fitness obtained from
feeding on different resources (i.e. hosts) is lower than that obtained
by consuming (i.e. parasitising) a limited subset, whereas generalism
should evolve when differences in energetic gains between resources are
not large (Lyimo & Ferguson, 2009). The robust dataset analysed here
shows that specificity may also be plastic within individuals, swinging
conveniently between generalism and specialism depending on the
structure of the host community. In presence of sufficient broods of
optimal hosts, ’P. torquans c. A.’ behaves as a specialist, being
found almost exclusively on Great Kiskadees. When the optimal host is
absent or very little available, however, the parasite can broaden its
host range, beginning by choosing the most suitable options, leaving bad
hosts for moments when good alternatives cannot be found. This sort of
facultative generalism is highly advantageous for the parasite, as it
may accommodate its choice so it uses suboptimal resources only at times
when it is profitable. In the study area, Great Kiskadees are present
only during a limited window of time, while Little Thornbirds (bad
alternative hosts) breed actively for much longer (Fig. 1). Hence, being
able to decide using bad hosts only when more competent ones are missing
may prove essential for the parasite to be able to persist and thrive in
this ecosystem.
From the host’s perspective, the degree of host selection observed in
this system may favour the evolution of resistance. The strategy of
tolerance of Great Kiskadees appears to be very successful (Manzoli et
al. 2018), but it implies that this host is targeted and therefore
highly exposed to the parasite. Resisting is highly costly, but it may
be beneficial not only because it would reduce the parasite burden, but
also because of its potential to dissuade host selection, as parasites
would be driven to select hosts in which their fitness is maximised.
The level of host discrimination observed for Philornis flies
rivals the cognitive decisions made by vertebrates when selecting their
food items, their refuge or their partners. Further, it is in line with
the optimal foraging theory (Pyke et al. 1977) which predicts that
foragers will be selective when a high-quality food type is abundant,
but less selective when that high-quality item is scarce (Emlen 1966,
Stephens and Krebs 1986). Underlying these selection processes there are
supply-demand dynamics. For example, avian parents should include lower
quality foods in the nestling diet only when brood demand is higher than
expected or when there is a shortage of food availability (Wright et al.
1998; Sauter et al. 2006). Similarly, in our system, Philornisflies select low quality hosts when host demand is high and better hosts
are lacking.
The remarkable capability of ’P. torquans c. A.’ of
discriminating among hosts should be enabled by a substantial amount of
time and energy dedicated for host searching, coupled by cues that allow
reliable differentiation among hosts. It is noteworthy that the parasite
can definitely distinguish between Little Thornbird (bad alternative
host) and Greater Thornbird (good alternative host), which is
outstanding considering that both Phacellodomus spp. are
phylogenetically very close to each other, and both build nests of
identical materials and similar shape. The mechanisms of host selection
by dipteran parasites have been studied mainly for haematophagous
species. The cues involved in them are thermal, visual and chemical
(Takken and Knols, 2010). Nonetheless, chemical cues seem to prevail in
highly selective species (Jossart et al., 2019). Anophelesgambiense is highly anthropophilic, and this preference is driven
by specific components found in human sweat (Braks et al., 2001; Zwiebel
& Takken, 2004) and skin microbiota (Verhulst et al., 2009).
Variability in the chemical composition of the sweat determines
differential attractiveness among humans (Smallegange et al., 2011).
Likewise, species of Glossinia (tse-tse fly) show variable
attraction to different odoriferous compounds (Torr & Solano, 2010).
Oviposition site selection by Glossina brevipalpis was found to
be independent of the salinity and pH of the substrate, and instead was
driven by presence of con-specific or hetero-specific puppae (Renda et
al., 2016), which would be mediated by odoriferous compounds (Saini et
al., 1996). Chemical cues have also been shown to drive host selection
in other arthropods, such as ticks (Ferreira et al., 2019).
Our findings have important implications for the epidemiology of
multi-host parasites, specifically for community scale patterns of
disease transmission. The concept of facultative generalism adds
pertinent elements to the notion of a ’dilution effect’ and the
relevance of biodiversity on infection dynamics (Schmidt & Ostfeld
2001). Shifts in biodiversity and community composition can influence
the likelihood of a parasite or vector encountering a highly competent
host species rather than a low-quality host. The ’dilution effect’
implies that greater biodiversity results in less encounters with highly
competent hosts and, therefore, in less parasite success and
transmission (Schmidt & Ostfeld 2001). However, if parasites or vectors
selectively infect the most competent hosts as observed in this study,
the presence of alternative ones (which increases with biodiversity) may
have little effect on transmission (Levine et al., 2017). Nevertheless,
when the alternative hosts are humans, domestic animals, or an
endangered wildlife species, the plastic host selection observed here,
influenced by biodiversity, can be of high importance for public health,
animal husbandry, and biodiversity conservation, respectively. For
example, humans might not be targeted by a given parasite as long as
more suitable hosts are available. This kind of ’deflection effect’ is
related to the ’dilution effect’ because they are both a function of
biodiversity. More biodiversity may dilute the infection of highly
competent hosts, or it can also divert it from a host of interest.
Reductions in biodiversity might therefore cause that humans (or
domestic animals, or endangered species) become increasingly chosen by
parasites. Thus, although the abundance of a given parasite is highly
dependent on the abundance of its ’reservoir’ host (e.g. mean abundance
of ’P. torquans c. A.’ is low in the community in years with few
Great Kiskadee broods; Manzoli et al. 2013), lack of main hosts would
paradoxically increase infection risk in an alternative host of
interest.