Host dispersal shapes the population structure of a tick-borne bacterial pathogen

Ana Claudia Norte, Gabriele Margos, Noemie S. Becker, Jaime Albino Ramos, Maria Sofia Nuncio, Volker Fingerle, Pedro Miguel Araujo, Peter Adamik, Haralambos Alivizatos, Emilio Barba, Rafael Barrientos, Laure Cauchard, Tibor Csorgo, Anastasia Diakou, Niels J. Dingemanse, Blandine Doligez, Anna Dubiec, Tapio Eeva, Barbara Flaisz, Tomas GrimMichaela Hau, Dieter Heylen, Sandor Hornok, Savas Kazantzidis, David Kovats, Frantisek Krause, Ivan Literak, Raivo Mand, Lucia Mentesana, Jennifer Morinay, Marko Mutanen, Julio Manuel Neto, Marketa Novakova, Juan Jose Sanz, Luis Pascoal da Silva, Hein Sprong, Ina-Sabrina Tirri, Janos Torok, Tomi Trilar, Zdenek Tyller, Marcel E. Visser, Isabel Lopes de Carvalho*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

39 Citations (Scopus)

Abstract

Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick-borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B. burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies "Candidatus Borrelia aligera" was also detected. Multilocus sequence typing (MLST) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick-borne pathogens are shaped by their host associations and the movement patterns of these hosts.

Original languageEnglish
Pages (from-to)485-501
Number of pages17
JournalMolecular Ecology
Volume29
Issue number3
Early online date9 Jan 2020
DOIs
Publication statusPublished - Feb 2020

Bibliographical note

Funding Information:
We would like to thank Cecilia Hizo‐Teufel and Christine Hartberger for help with laboratory analyses, Marko Mägi, Vallo Tilgar, Oscar Frías, Alejandra Toledo Vásquez, Alexia Mouchet, Josef Heryan, Cinthya Lange, Piet de Goede, Henri Bouwmeester, Esa Lehikoinen, Franck Théron, Petra Bandelj, Tea Knapič, Irena Kodele Krašna, Pavle Štirn, Katarina Prosenc Trilar, Modest Vengušt, Hanna Holmström, Jorma Nurmi, Miia Rainio, Pablo Sánchez‐Virosta, Silvia Espín and Lucy Winder who helped with tick collection, Vítor Hugo Paiva for help with statistical analyses, the Falsterbo Ringing Station and Instituto da Conservação da Natureza e Florestas IP and the Slovenian Bird Ringing Center at Slovenian Museum of Natural History for providing conditions for fieldwork and bird ringing. We thank the two anonymous reviewers for their insightful comments on this paper. This study received financial support from Fundação para a Ciência e a Tecnologia by the strategic program of MARE (MARE ‐ UID/MAR/04292/2013) and the fellowship to Ana Cláudia Norte (SFRH/BPD/108197/2015), and the Portuguese National Institute of Health. Raivo Mänd, Tomi Trilar, Tapio Eeva, Tomas Grim and Dieter Heylen were supported by the Estonian Research Council (research grant # IUT34‐8), the Slovenian Research Agency ‐programme “Communities, relations and communications in the ecosystems” (No. P1‐0255), the Academy of Finland (project 265859), the Internal Grant Agency of Palacky University (PrF_2014_018, PrF_2015_018, PrF_2013_018) and the Marie Sklodowska‐Curie Actions (EU‐Horizon 2020, Individual Global Fellowship, project no 799609), respectively. All applicable institutional and/or national guidelines for the care and use of animals were followed in this study.

Publisher Copyright:
© 2019 John Wiley & Sons Ltd

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

Keywords

  • birds
  • Borrelia garinii
  • host-parasite interactions
  • Lyme borreliosis
  • migration
  • ticks
  • BURGDORFERI SENSU-LATO
  • IXODES-RICINUS TICKS
  • BLACKBIRDS TURDUS-MERULA
  • BORRELIA-BURGDORFERI
  • LYME-DISEASE
  • MIGRATORY BIRDS
  • WILD BIRDS
  • TRANSMISSION
  • ACARI
  • PREVALENCE

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