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Host Specificity Patterns Among Generalist Louse Flies

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Host Specificity Patterns Among Generalist Louse Flies bioRxiv preprint doi: https://doi.org/10.1101/2021.02.12.430912; this version posted February 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Promiscuous specialists: Host specificity 2 patterns among generalist louse flies 3 4 Aleksi Lehikoinen1*, Pekka Pohjola2*, Jari Valkama1*, Marko 5 Mutanen3 and Jaakko L.O. Pohjoismäki2§ 6 7 1 The Helsinki Lab of Ornithology, Finnish Museum of Natural 8 History, P.O. Box 17, 00014 Helsinki University, Finland. 9 2Department of Environmental and Biological Sciences, 10 University of Eastern Finland, Joensuu, Finland. 11 3 Ecology and Genetics Research Unit, P.O.Box 3000, FI- 12 90014 University of Oulu, Oulu, Finland. 13 *Equal contribution 14 §Corresponding author: [email protected], +358- 15 50 574 4745 16 17 Abstract 18 19 Ectoparasites such as louse flies (Diptera: Hippoboscidae) 20 have tendency for host specialization, which is driven by 21 adaptation to host biology as well as competition avoidance 22 between parasites of the same host. However, some louse fly 23 species, especially in genera attacking birds, show wide 24 range of suitable hosts. In the presented study, we have 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.12.430912; this version posted February 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 25 surveyed the current status of bird attacking louse flies 26 in Finland to provide comprehensive host association data 27 to analyse the ecological requirements of the generalist 28 species. A thorough sampling of 9342 birds, representing 29 134 species, recovered 576 specimens of louse flies, 30 belonging to six species: Crataerina hirundinis, C. 31 pallida, Ornithomya avicularia, O. chloropus, O. 32 fringillina and Ornithophila metallica. Despite some 33 overlapping hosts, the three Ornithomya species showed a 34 notable pattern in their host preference, which was 35 influenced not only by the host size but also by the habitat 36 and host breeding strategy. We also provide DNA barcodes 37 for most Finnish species of Hippoboscidae, which can be 38 used as a resource for species identification as well as 39 metabarcoding studies in the future. 40 41 Introduction 42 43 Parasites depend on their hosts as their principal 44 ecological niche as well as source of the essential 45 resources (1). Due to this intimate relationship, parasites 46 commonly tend to specialize on the host, adapting to the 47 host defences and ecology. Due to the selection pressures 48 and short generation time, parasites are also prone to 49 evolve rapidly, helping them to circumvent potential 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.12.430912; this version posted February 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 50 evolutionary advantages that the host has gained (2) and 51 facilitating the specialization process. Parasitic 52 lineages, especially endoparasites, are characterized by 53 long branches in molecular phylogenies (e.g. (3-5)), for 54 which reason they often constitute the “rogue” taxa in 55 them. While several non-mutually exclusive explanations for 56 this pattern have been suggested, for mitochondrial COI 57 gene, this is likely at least partly explained as being an 58 adaptation to anoxic environment (5). Additional pressure 59 for host specialization is driven by direct or interference 60 competition between different parasite species occupying 61 the same host (6). For example, spatial segregation, which 62 can allow the parasites to coexist on the same host can 63 ultimately lead to intrahost speciation, as seen in 64 Dactylogyrus gill parasites(7) and human lice (8). Host 65 niches can also be partitioned temporally, as is the case 66 with a number flea (Siphonaptera) species on small mammals, 67 such as Peromyscopsylla spp. living on e.g. bank voles 68 (Myodes glareolus (Schreber)) during winter months and 69 Ctenopththalmus spp. during spring/summer months (9). 70 Parasites can also avoid competition by specializing on 71 different aspects of the host biology. For example, the 72 parasites can attack different developmental stages of the 73 host, or in different biotopes or context, such as the ant 74 decapitating scuttle flies (Pseudacteon, Diptera: 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.12.430912; this version posted February 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 75 Phoridae), where some species attack while foraging ants 76 and some ants at the nest (10). 77 78 Louse flies (Diptera: Hippoboscidae) are obligate 79 ectoparasites of birds and mammals, belonging to the same 80 superfamily (Hippoboscoidea) with tsetse flies 81 (Glossinidae). Both families are hematophagous and 82 viviparous. As of note, bat flies (Nycteribiinae, 83 Streblinae) have been treated as independent families, but 84 are in fact embedded within the other Hippoboscidae taxa 85 (11). Adults of Hippoboscoidea species are long lived, 86 giving birth to a full-grown or pupariated larva, one at 87 the time but few to dozen during the female’s lifetime. Of 88 the 45 European species of Hippoboscidae, only 12 have been 89 recorded in Finland (12) and of these, seven attack birds: 90 Crataerina hirundinis (Linnaeus), C. pallida (Olivier), 91 Olfersia fumipennis (Sahlberg), Ornithomya avicularia 92 (Linnaeus), O. chloropus Bergroth, O. fringillina Curtis 93 and Ornithophila metallica (Schiner). Three of the species 94 are highly specialized, C. hirundinis on barn swallow 95 (Hirundo rustica Linnaeus), C. pallida on common swift 96 (Apus apus (Linnaeus)) and O. fumipennis on osprey (Pandion 97 haliaetus (Linnaeus)), while the remaining four have 98 relatively wide host range, each attacking dozens of bird 99 species (13, 14). 100 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.12.430912; this version posted February 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 101 In the presented study, we sought to survey the current 102 status of bird attacking louse flies in Finland and provide 103 comprehensive host association data to analyse the 104 ecological requirements of the generalist species as well 105 as DNA barcodes for the Finnish Hippoboscidae to facilitate 106 their identification in the future. This required the 107 concentrated effort from 36 bird ringers, who recorded the 108 abundance of bird louse flies from 9342 birds, representing 109 134 species. A total of 576 specimens, belonging to six 110 species of bird flies were sampled. From these Crataerina 111 hirundinis and C. pallida, were found only on their known 112 specific hosts, whereas Ornithomya avicularia, O. chloropus 113 and O. fringillina were found on 68 different bird species. 114 The sixth species, Ornithophila metallica was represented 115 only by one specimen. Despite some overlapping hosts, the 116 three Ornithomya species showed a notable pattern in their 117 host preference. To explain this pattern, we were 118 interested (i) what species’ traits of hosts, could 119 explain the variation in abundance of bird flies and (ii) 120 do species’ traits of hosts differ between different 121 generalist bird fly species. We predict that body size of 122 host, habitat preference, migration strategy, nest location 123 and diet could explain the variation in species and 124 abundance of bird flies in different host species of birds. 125 The obtained DNA barcodes work well for separating the 126 species and can be used as a resource for species 5 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.12.430912; this version posted February 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 127 identification as well as metabarcoding studies in the 128 future. 129 130 Materials and Methods 131 132 Data collection and filtering 133 134 The data consisted two types of information: i) information 135 if a bird has had bird fly or not and ii) information what 136 bird fly species certain bird species had been carrying. 137 138 Voluntary bird ringers were collecting information on do 139 the ringed birds have bird flies when handling the bird. 140 The ringers also identified the age of the bird if possible 141 (young born during the same year or older). That data was 142 collected during years 2008-2019, but most of the data 143 origin from 2013 onwards when new data base system was 144 launched allowing an easy data entry. Altogether 36 ringers 145 participated the data collection during these years and 146 marked information from 9342 birds (134 species 72 of which 147 had bird flies; Table S1, S2, S3). However, only some of 148 the ringers have also entered data from birds which did not 149 show signs of bird flies and thus this data could not be 150 used to study the prevalence among hosts.
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