Abstract
BackgroundThe behaviour of blood-sucking arthropods is a crucial determinant of blood protozoan distribution and hence of host-parasite coevolution, but it is very challenging to study in the wild. The molecular identification of parasite lineages in vectors can be a useful key to understand the behaviour and transmission patterns realised by these vectors.MethodsIn this study, we collected blackflies around nests of three raptor species in the upper forest canopy in central Europe and examined the presence of vertebrate DNA and haemosporidian parasites in them. We molecularly analysed 156 blackfly individuals, their vertebrate blood meals, and the haemosporidian parasite lineages they carried.ResultsWe identified nine species of Simulium blackflies, largely belonging to the subgenera Nevermannia and Eusimulium. Only 1% of the collected specimens was visibly engorged, and only 4% contained remains of host DNA. However, in 29% of the blackflies Leucocytozoon lineages were identified, which is evidence of a previous blood meal on an avian host. Based on the known vertebrate hosts of the recorded Leucocytozoon lineages, we can infer that large and/or abundant birds, such as thrushes, crows, pigeons, birds of prey, owls and tits are the main targets of ornithophilic blackflies in the canopy. Blackfly species contained similar proportions of host group-specific parasite lineages and thus do not appear to be associated with particular host groups.ConclusionsThe Leucocytozoon clade infecting thrushes, crows, and pigeons present in most represented blackfly species suggests a lack of association between hosts and blackflies, which can increase the probability of host switches of blood parasites. However, the composition of the simuliid species differed between nests of common buzzards, goshawks and red kites. This segregation can be explained by coinciding habitat preferences between host and vector, and may lead to the fast speciation of Leucocytozoon parasites. Thus, subtle ecological preferences and lack of host preference of vectors in the canopy may enable both parasite diversification and host switches, and enforce a habitat-dependent evolution of avian malaria parasites and related haemosporidia.
Highlights
Vector-transmitted parasites are extremely common but insufficiently understood [1]
The sequencing of the cox1 fragment of blackflies revealed 9 species: 86 individuals belonged to the Simulium (Nevermannia) vernum-group, including the species S. (N.) vernum, S. (N.) naturale, and S. (N.) cryophilum, which are indistinguishable based on the sequenced cox1 fragment and will be further referred to as S. (N.) vernum*
All but two out of the 154 identified individuals belonged to the subgenera Nevermannia and Eusimulium, and nearly 30% of the individuals of both subgenera had fed on birds, as revealed by their Leucocytozoon load
Summary
Vector-transmitted parasites are extremely common but insufficiently understood [1]. In theory vectors can both catalyse and hamper the coevolution of hosts andBlood-feeding arthropods belong to the major ectoparasitic threats for wild vertebrates, not least because they transmit many potentially life-threatening disease agents [3]. Blackflies (Simuliidae), in particular, can be a major nuisance both due to mass outbreaks and the transmission of pathogens such as trypanosomes, Chakarov et al Parasites Vectors (2020) 13:309 haemosporidians and filarial nematodes [4]. Despite their key role in different environments, research on blackflies has for a long time focused on the accessible aquatic stages [5]. This has resulted in a knowledge gap on the feeding preferences of most species, only slowly improving in recent decades ([6], but see [7]). The molecular identification of parasite lineages in vectors can be a useful key to understand the behaviour and transmission patterns realised by these vectors
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