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 Grim; Michaela 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

doi:10.1111/mec.15336

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)

NIOO - Animal Ecology (AnE)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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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 language	English
Article number	485-501
Pages (from-to)	485-501
Number of pages	17
Journal	Molecular Ecology
Volume	29
Issue number	3
Early online date	09 Jan 2020
DOIs	https://doi.org/10.1111/mec.15336
Publication status	Published - 01 Feb 2020

Keywords

international
Borrelia garinii
host-parasite interactions
Lyme borreliosis
migration
ticks
birds
Plan_S-Compliant_NO

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6925_NorteFinal published version, 1.93 MB

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Norte, A. C., Margos, G., Becker, N. S., Ramos, J. A., Nuncio, M. S., Fingerle, V., Araujo, P. M., Adamik, P., Alivizatos, H., Barba, E., Barrientos, R., Cauchard, L., Csorgo, T., Diakou, A., Dingemanse, N. J., Doligez, B., Dubiec, A., Eeva, T., Flaisz, B., ... de Carvalho, I. L. (2020). Host dispersal shapes the population structure of a tick-borne bacterial pathogen. Molecular Ecology, 29(3), 485-501. [485-501]. https://doi.org/10.1111/mec.15336

@article{790c94003285436282504e0b1e3f864c,

title = "Host dispersal shapes the population structure of a tick-borne bacterial pathogen",

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.",

keywords = "international, Borrelia garinii, host-parasite interactions, Lyme borreliosis, migration, ticks, birds, Plan_S-Compliant_NO",

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

note = "6925, AnE; Data Archiving: Data archived at Borrelia MLST database (https://pubmlst.org/borrelia/); no NIOO data",

year = "2020",

month = feb,

day = "1",

doi = "10.1111/mec.15336",

language = "English",

volume = "29",

pages = "485--501",

journal = "Molecular Ecology",

issn = "0962-1083",

publisher = "Wiley-Blackwell",

number = "3",

}

Norte, AC, Margos, G, Becker, NS, Ramos, JA, Nuncio, MS, Fingerle, V, Araujo, PM, Adamik, P, Alivizatos, H, Barba, E, Barrientos, R, Cauchard, L, Csorgo, T, Diakou, A, Dingemanse, NJ, Doligez, B, Dubiec, A, Eeva, T, Flaisz, B, Grim, T, Hau, M, Heylen, D, Hornok, S, Kazantzidis, S, Kovats, D, Krause, F, Literak, I, Mand, R, Mentesana, L, Morinay, J, Mutanen, M, Neto, JM, Novakova, M, Sanz, JJ, da Silva, LP, Sprong, H, Tirri, I-S, Torok, J, Trilar, T, Tyller, Z, Visser, ME & de Carvalho, IL 2020, 'Host dispersal shapes the population structure of a tick-borne bacterial pathogen', Molecular Ecology, vol. 29, no. 3, 485-501, pp. 485-501. https://doi.org/10.1111/mec.15336

TY - JOUR

T1 - Host dispersal shapes the population structure of a tick-borne bacterial pathogen

AU - Norte, Ana Claudia

AU - Margos, Gabriele

AU - Becker, Noemie S.

AU - Ramos, Jaime Albino

AU - Nuncio, Maria Sofia

AU - Fingerle, Volker

AU - Araujo, Pedro Miguel

AU - Adamik, Peter

AU - Alivizatos, Haralambos

AU - Barba, Emilio

AU - Barrientos, Rafael

AU - Cauchard, Laure

AU - Csorgo, Tibor

AU - Diakou, Anastasia

AU - Dingemanse, Niels J.

AU - Doligez, Blandine

AU - Dubiec, Anna

AU - Eeva, Tapio

AU - Flaisz, Barbara

AU - Grim, Tomas

AU - Hau, Michaela

AU - Heylen, Dieter

AU - Hornok, Sandor

AU - Kazantzidis, Savas

AU - Kovats, David

AU - Krause, Frantisek

AU - Literak, Ivan

AU - Mand, Raivo

AU - Mentesana, Lucia

AU - Morinay, Jennifer

AU - Mutanen, Marko

AU - Neto, Julio Manuel

AU - Novakova, Marketa

AU - Sanz, Juan Jose

AU - da Silva, Luis Pascoal

AU - Sprong, Hein

AU - Tirri, Ina-Sabrina

AU - Torok, Janos

AU - Trilar, Tomi

AU - Tyller, Zdenek

AU - Visser, Marcel E.

AU - de Carvalho, Isabel Lopes

N1 - 6925, AnE; Data Archiving: Data archived at Borrelia MLST database (https://pubmlst.org/borrelia/); no NIOO data

PY - 2020/2/1

Y1 - 2020/2/1

N2 - 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.

AB - 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.

KW - international

KW - Borrelia garinii

KW - host-parasite interactions

KW - Lyme borreliosis

KW - migration

KW - ticks

KW - birds

KW - Plan_S-Compliant_NO

UR - https://pubmlst.org/borrelia/

U2 - 10.1111/mec.15336

DO - 10.1111/mec.15336

M3 - Article

SN - 0962-1083

VL - 29

SP - 485

EP - 501

JO - Molecular Ecology

JF - Molecular Ecology

IS - 3

M1 - 485-501

ER -

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

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Keywords

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