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Haemoproteus infection status of collared flycatcher males changes within a breeding season

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Abstract

In ecological studies of haemosporidian parasites, prevalence is typically considered as a stable attribute. However, little is known about the possible within-host dynamics of these parasites that may originate from environmental fluctuations, parasite life cycles and the ability of hosts to suppress or clear infection. We sampled the blood of male collared flycatchers Ficedula albicollis twice within a breeding season and investigated the determinants of initial infection status and change in infection status. We found that older males tended to be initially more infected at courtship. Change in infection status was unrelated to male traits, but a widespread disappearance of Haemoproteus pallidus infection from the blood was detected between courtship and nestling rearing. The probability of change in infection status increased with the time elapsed between sampling occasions. This suggests that the disappearance of infection from the blood was due to either an active parasite suppression mechanism or the beginning of the latent phase in the parasite life cycle. Initial infection status or disappearance of infection from the blood showed no correlation with breeding success. These results show that H. pallidus infection status and thus prevalence are dynamically changing attributes and this has widespread practical and ecological implications.

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References

  • Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347:220,436

    Article  CAS  Google Scholar 

  • Atkinson CT, van Riper C III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions. Oxford University Press, Oxford, pp 19–48

    Google Scholar 

  • Bensch S, Pérez-Tris J, Waldenström J, Hellgren O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites-multiple cases of cryptic speciation? Evolution 58:1617–1621

    Article  CAS  PubMed  Google Scholar 

  • Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Res 9:1353–1358

    Article  Google Scholar 

  • Bernotienė R, Palinauskas V, Iezhova T, Murauskaitė D, Valkiūnas G (2016) Avian haemosporidian parasites (Haemosporidia): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Exp Parasitol 163:31–37

    Article  CAS  PubMed  Google Scholar 

  • Burkett-Cadena ND, McClure CJW, Estep LK, Eubanks MD (2013) Hosts or habitats: what drives the spatial distribution of mosquitoes? Ecosphere 4:30

    Article  Google Scholar 

  • Chakarov N, Linke B, Boerner M, Goesmann A, Krüger O, Hoffman JI (2015) Apparent vector-mediated parent-to-offspring transmission in an avian malaria-like parasite. Mol Ecol 24:1355–1363.

  • Cosgrove CL, Wood MJ, Day KP, Sheldon B (2008) Sesonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77:540–548

    Article  PubMed  Google Scholar 

  • Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, Voelker G (2014) Does the niche breadth or trade-off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Mol Ecol 23:3322–3329

    Article  PubMed  Google Scholar 

  • Dybdahl MF, Storfer A (2003) Parasite local adaptation: red queen versus suicide king. Trends Ecol Evol 18:523–530

    Article  Google Scholar 

  • Ewald PW (1983) Host-parasite relations, vectors, and the evolution of disease severity. Ann Rev Ecol Syst 14:465–485

    Article  Google Scholar 

  • Figuerola J, Muñoz E, Gutiérrez R, Ferrer D (1999) Blood parasites, leucocytes and plumage brightness in the cirl bunting, Emberiza cirlus. Funct Ecol 13:594–601

    Article  Google Scholar 

  • Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78

    Article  CAS  PubMed  Google Scholar 

  • Gandon S, Michalakis Y (2000) Evolution of parasite virulence against qualitative and quantitative host resistance. P Roy Soc Lond B 267:985–990

    Article  CAS  Google Scholar 

  • Garamszegi LZ (2006) The evolution of virulence and host specialization in malaria parasites of primates. Ecol Lett 9:933–940

    Article  PubMed  Google Scholar 

  • Garamszegi LZ (2011) The evolution of virulence in primate malaria parasites based on Bayesian reconstructions of ancestral states. Int J Parasitol 41:205–212

    Article  PubMed  Google Scholar 

  • Garamszegi LZ, Møller AP, Török J, Michl G, Péczely P, Richard M (2004) Immune challange mediates vocal communication in a passerine bird: an experiment. Behav Ecol 15:148–157

    Article  Google Scholar 

  • Garamszegi LZ, Rosivall B, Hegyi G, Szöllősi E, Török J, Eens M (2006) Determinants of male territorial behavior in a Hungarian collared flycatcher population: plumage traits of residents and challengers. Behav Ecol Sociobiol 60:663–671

    Article  Google Scholar 

  • Golding N, Nunn MA, Purse BV (2015) Identifying biotic interactions which drive the spatial distribution of a mosquito community. Parasites & Vectors 8:367

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hasselquist D (2007) Comparative immunoecology in birds: hypotheses and tests. J Ornithol 148:S571–S582

    Article  Google Scholar 

  • Hegyi G, Török J, Tóth L (2002) Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher. J Evol Biol 15:710–719

    Article  Google Scholar 

  • Hegyi G, Rosivall B, Török J (2006) Paternal age and offspring growth: separating the intrinsic quality of young from rearing effects. Behav Ecol Sociobiol 60:672–682

    Article  Google Scholar 

  • Hellgren O, Pérez-Tris J, Bensch S (2009) A Jack of all trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90:2840–2849

    Article  PubMed  Google Scholar 

  • Jenkins T, Owens IPF (2011) Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance–occupancy relationship? Mol Ecol 20:3910–3920

    Article  PubMed  Google Scholar 

  • Kirchner JW, Roy BA (2002) Evolutionary implications of host-pathogen specificity: fitness consequences of pathogen virulence traits. Evol Ecol Res 4:27–48

    Google Scholar 

  • Knowles SCL, Wood MJ, Alves R, Wilkin TA, Bensch S, Sheldon BC (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Mol Ecol 20:1062–1076

    Article  PubMed  Google Scholar 

  • Könczey R, Török J, Tóth L (1992) Breeding success and breeding site fidelity in the collared flycatcher (Ficedula albicollis). Állattani Közlemények 78:69–76

    Google Scholar 

  • Kulma K, Low M, Bensch S, Qvarnström A (2013) Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone. Mol Ecol 22:4591–4601

    Article  CAS  PubMed  Google Scholar 

  • Krasnov BR, Poulin R, Shenbrot GJ, Mouillot D, Khokhlova JS (2004) Ectoparasitic “jack-of-all-trades”: relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. Am Nat 164:506–516

    Article  PubMed  Google Scholar 

  • Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC (2011) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. J Anim Ecol 80:1196–1206

    Article  PubMed  Google Scholar 

  • Levin BR, Bull JJ (1994) Short-sighted evolution and the virulence of pathogenic micro-organisms. Trends Microbiol 2:76–81

    Article  CAS  PubMed  Google Scholar 

  • Marzal A, Albayrak T (2012) Geographical variation of haemosporidian parasites in Turkish populations of Krüper’s Nuthatch Sitta krueperi. J Ornithol 153:1225–1231

    Article  Google Scholar 

  • Marzal A, de Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine. Oecologia 142:541–545

    Article  PubMed  Google Scholar 

  • Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc Roy Soc Lond B 267:2507–2510

    Article  CAS  Google Scholar 

  • Nicholls JA, Double MC, Rowell DM, Magrath RD (2000) The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J Avian Biol 31:165–176

    Article  Google Scholar 

  • Podmokla E, Dubiec A, Drobniak SM, Arct A, Gustaffson L, Cichon M (2014) Determinants of prevalence and intensity of infection with malaria parasites in the blue tit. J Ornithol 155:721–727

    Article  Google Scholar 

  • Poulin R, Mouillot D (2004) The relationship between specialization and local abundance: the case of helminth parasites of birds. Oecologia 140:372–378

    Article  PubMed  Google Scholar 

  • Rosivall B, Török J, Hasselquist D, Bensch S (2004) Brood sex ratio adjustment in collared flycatchers (Ficedula albicollis): results differ between populations. Behav Ecol Sociobiol 56:346–351

    Article  Google Scholar 

  • Sanz JJ, Arriero E, Moreno J, Merino S (2001) Interactions between hemoparasite status and female age in the primary reproductive output of pied flycatchers. Oecologia 126:339–344

    Article  Google Scholar 

  • Spencer KA, Buchanan KL, Leitner S, Goldsmith AR, Catchpole CK (2005) Parasites affect song complexity and neural development in a songbird. Proc Roy Soc Lond B 272:2037–2043

    Article  Google Scholar 

  • Swanson BL, Lyons AC, Bouzat JL (2014) Distribution, prevalence and host specificity of avian malaria parasites across the breeding range of the migratory lark sparrow (Chondestes grammacus). Genetica 142:235–249

    Article  PubMed  Google Scholar 

  • Szöllősi E, Cichoń M, Eens M, Hasselquist D, Kempenaers B, Merino S, Nilsson JÅ, Rosivall B, Rytkönen S, Török J, Wood MJ, Garamszegi LZ (2011) Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. J Evol Biol 24:2014–2024

    Article  PubMed  Google Scholar 

  • Szöllősi E, Rosivall B, Hasselquist D, Török J (2009) The effect of parental quality and malaria infection on nestling performance in the collared flycatcher Ficedula albicollis. J Ornithol 150:519–527

    Article  Google Scholar 

  • Svensson L (1992) Identification guide to European passerines. Stockholm

  • Török J, Hegyi G, Garamszegi LZ (2003) Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. Behav Ecol 14:382–388

    Article  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton

    Google Scholar 

  • Verheyen GR, Kempenaers B, Adriaensen F, van den Broeck M, Matthysen E, van Broeckhoven C, Dhondt AA (1995) The genetic structure of Parus caeruleus (blue tit) populations as revealed by minisatellite single locus probes. Heredity 75:571–577

    Article  Google Scholar 

  • Waldenström J, Bensch S, Hasselquist D, Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90:191–194

    Article  PubMed  Google Scholar 

  • Wood MJ, Cosgrove CL, Wilkin TA, Knowles SC, Day KP, Sheldon BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol 16:3263–3273

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank R. Főző, M. Herényi, D. Kiss, G. Nagy, B. Siklódi for their help in the field. The comments of the anonymous referees considerably improved the manuscript. The study was supported by the Hungarian Scientific Research Fund (OTKA T049650, T049678, F68295, K101611) to B R., J.T. and G.H., by the National Research, Development and Innovation Office (K-115970), a postdoctoral grant from the Hungarian Academy of Sciences to E.S., the Erdők a Közjóért Alapítvány, the Pilis Park Forestry. L.Z.G. was supported by a fund from the Spanish government within the frame of the “Plan Nacional” program (CGL2012-40026-C02-01, CGL2015-70639-P).

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Authors and Affiliations

  1. Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eötvös Loránd University, Budapest, Hungary

    Eszter Szöllősi, Gergely Hegyi, Miklós Laczi, Balázs Rosivall & János Török

  2. MTA-ELTE-MTM Ecology Research Group, Biological Institute, Eötvös Loránd University, Budapest, Hungary

    Eszter Szöllősi

  3. Department of Evolutionary Ecology, Estación Biológica de Doñana-CSIC, Seville, Spain

    László Zsolt Garamszegi

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  1. Eszter Szöllősi
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  2. László Zsolt Garamszegi
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Correspondence to Eszter Szöllősi.

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Szöllősi, E., Garamszegi, L.Z., Hegyi, G. et al. Haemoproteus infection status of collared flycatcher males changes within a breeding season. Parasitol Res 115, 4663–4672 (2016). https://doi.org/10.1007/s00436-016-5258-0

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