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.