INTRODUCTION:
Host-parasite interactions are inter-specific relationships in which the
parasite is engaged in exploiting the host, while the host tries to
counter the infection by minimising parasite burden (resistance) and its
damage (tolerance) (Raberg et al. 2009). The outcome of this battle will
determine consequences for host and parasite: the fitness cost paid by
the host (virulence) and the success of an infection (transmission)
(Leggett et al. 2013). The majority of parasites use more than one host
species (Woolhouse et al., 2001; Schmid-Hempel, 2011). Using different
host species implies exposure to different host competences and defence
strategies, resulting in differential parasite transmission (Gervasi et
al. 2015). From a parasite’s perspective, an optimal host is one that
survives the infection, so that the cycle of the parasite can be
completed; and one that makes little effort to reduce the development,
reproduction or replication of the parasite. Hence, to maximise parasite
transmission, an ideal host should be little resistant and highly
tolerant (Martin et al. 2016).
In nature, parasites encounter potential hosts that may differ in their
quality (host competence) or quantity (abundance) (Fenton et al. 2015;
Gervasi et al. 2015). Some parasites are considered generalists because
they use a wide range of hosts, while others specialise in one or a few
host species. Under these opposing strategies, generalist parasites
benefit from broad host availability (quantity) whereas specialists
prioritise host quality. Favouring quantity over quality may result in
suboptimal exploitation of the host, maladaptive virulence and poor
transmission (Rigaud et al. 2010; Lievens et al. 2018). On the other
hand, specialists are less resilient during environmental disruptions
that may affect the structure of the host community (Auld et al. 2017).
For an infection to occur a parasite has to encounter a compatible host.
In this exposure process, the parasite may exhibit clear host
preferences (Combes, 1991). Although encounter rates are often assumed
to be a function of host density or frequency, some parasites and
vectors can also display non-random or even targeted host selection
(Johnson et al. 2019). In those cases, host preference should reflect
host competence, as selection pressures would favour choosing hosts with
high tolerance and low resistance. Motile parasites, therefore, would
not seek and infect hosts in a random manner, but rather their
preference would be driven by host quality. Theoretical approaches
explored this notion (Best el al. 2014; Forbes et al. 2017), but the
existing empirical evidence is still very limited. One of the few
studies that assessed the hypothesis that host quality drives parasite
preference found that cercariae of an amphibian trematode discriminated
among host species and preferred those that least limited the infection
(Sears et al. 2012). Another study found that cercariae showed a
consistent preference, but in this case host attractiveness was
decoupled with host competence (Johnson et al. 2019). In other system, a
parasitoid appears to contact its dinoflagellate hosts at random (Alacid
et al. 2016).
Studying the complex dynamics of multihost-multiparasite communities in
nature is a major outstanding challenge (Auld et al. 2017). This is
because in natural systems causal relationships are embedded in a wider
web of complex interactions, making extremely difficult dissecting
cause-effect patterns from background noise. A singular system,
comprising a parasitic fly and its multiple bird hosts, possesses
characteristics that make it very amenable to detailed study of the
ecology of host-parasite interactions in nature. The genusPhilornis Meinert 1890 (Diptera: Muscidae) consists of a group of
Neotropical flies that depend on bird broods (Arendt 1985; Couri 1999).
While adults are free living, larval trophic behaviour is associated
with bird nestlings. Most parasitic Philornis spp. have
subcutaneous burrowing larvae that feed on blood, tissue and fluids at
all instars (Dudaniec et al. 2006). The majority of subcutaneousPhilornis parasitise exclusively bird nestlings. Because
nestlings can be monitored daily from egg to fledging (i.e. the whole
period they are susceptible to infection by Philornis spp.),
collection of sequential infection data from the whole bird community is
feasible (Manzoli et al. 2013). Moreover, subcutaneous larvae are
relatively large and stay at the site where they penetrated the skin, so
they can also be individually followed throughout this parasitic stage,
enabling assessment of parasite success (Manzoli et al. 2018).
The parasitic fly identified in central Argentina was designated
‘Philornis torquans complex genotype central Argentina’
(hereafter, ‘P. torquans c. A.’) (Monje et al. 2013; Quiroga et
al. 2016). Philornis torquans is considered a generalist
(Löwenberg-Neto 2008), and in central Argentina it has been found to
parasitise around half of the passerine birds that breed there
(Antoniazzi et al. 2011; Manzoli et al. 2013). However, it is closely
associated with Great Kiskadees, Pitangus sulphuratus Linnaeus,
1766 (Passeriformes: Tyrannidae) (de la Peña et al. 2004; Antoniazzi et
al. 2011; Manzoli et al. 2013). Given that prevalences and burdens are
highest in Great Kiskadees, and that the abundance of their broods
determines the occurrence of P. torquans in the whole bird
community (Antoniazzi et al. 2011; Manzoli et al. 2013), Great Kiskadees
are arguably the main host of P. torquans c. A. Many other bird
species can be alternative hosts, of which Thornbirds (The Little
Thornbird - Phacellodomus sibilatrix Sclater, 1879; and
the Greater Thornbird - Ph. ruber Vieillot, 1817) are among the
ones most frequently used (Antoniazzi et al. 2011; Manzoli et al. 2013;
de la Peña et al. 2004). A recent study tested the hypothesis that, in
this system, the outcome of host-parasite interactions is different when
comparing main (Kiskadees) and alternative hosts (Thornbirds), and that
this is related to contrasts in host defence strategies (Manzoli et al.
2018). It was found that main hosts have a strategy of high tolerance
and negligible resistance, ensuring great larval success
(>90%). In Thornbirds, an inflammatory response to
infection is mounted, indicating a strategy of resistance. This response
is efficient in Little Thornbirds (parasite success is reduced in
>80%), but much less so in Greater Thornbirds
(~20% reduction). These results highlighted the
importance of defence strategies and its efficacies in determining
virulence and infection dynamics, and also provided support to the
hypothesis posited above which claimed that host selection is driven by
host quality. It is noteworthy that despite the large difference in host
competence between both Thornbird species, the parasite does not appear
to prefer the better quality alternative host over the other: 38% of
Little Thornbird broods parasitised compared to 26% Greater Thornbird
broods (Manzoli et al. 2013).
The above prompted some questions, such as, why would a gravid female
fly select a bad host instead of the optimal host or good alternative
ones? A preliminary analysis suggested that ‘P. torquans c. A.’
selects Thornbirds when the availability of Kiskadee nestlings has been
low (Manzoli et al. 2013). Here we offer data from a thorough
longitudinal study conducted along 8 breeding seasons under natural
conditions to test the hypothesis that Philornis chooses
suboptimal hosts when better alternatives are not sufficiently
available.