A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplification

The tick Ixodes ricinus parasitizes a wide range of vertebrates. These hosts vary in the relative contribution to the feeding of the different tick life stages, and their interplay is pivotal in the transmission dynamics of tick-borne pathogens. We aimed to know if there is a phylogenetic signal in...

Full description

Saved in:
Bibliographic Details
Main Authors: Agustin Estrada-Peña, Hein Sprong, Sara R. Wijburg
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Current Research in Parasitology and Vector-Borne Diseases
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2667114X24000293
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846148723860570112
author Agustin Estrada-Peña
Hein Sprong
Sara R. Wijburg
author_facet Agustin Estrada-Peña
Hein Sprong
Sara R. Wijburg
author_sort Agustin Estrada-Peña
collection DOAJ
description The tick Ixodes ricinus parasitizes a wide range of vertebrates. These hosts vary in the relative contribution to the feeding of the different tick life stages, and their interplay is pivotal in the transmission dynamics of tick-borne pathogens. We aimed to know if there is a phylogenetic signal in the feeding and propagation hosts of I. ricinus, independently of other traits, as well as in the amplification of Borrelia burgdorferi (s.l.) in feeding larvae. We used a compilation of 1127 published field surveys in Europe, providing data for 96,586 hosts, resulting in 265,124 larvae, 72,080 nymphs and 37,726 adults. The load of immature ticks on hosts showed a significant phylogenetic signal towards the genera Psammodromus, Podarcis, and Lacerta (nymphs only). We hypothesize that such signal is the background hallmark of the primitive hosts associations of I. ricinus, probably in the glaciation refugia. A secondary phylogenetic signal for tick immatures appeared for some genera of Rodentia and Eulipotyphla. Results suggest the notion that the tick gained these hosts after spread from glaciation refugia. Analyses support a phylogenetic signal in the tick adults, firmly linked to Cetartiodactyla, but not to Carnivora or Aves. This study provides the first demonstration of host preferences in the generalist tick I. ricinus. We further demonstrate that combinations of vertebrates contribute in different proportions supporting the tick life-cycle in biogeographical regions of the Western Palaearctic as each region has unique combinations of dominant hosts. Analysis of the amplification of B. burgdorferi (s.l.) demonstrated that each genospecies is better amplified by competent reservoirs with which a strong phylogenetic signal exists. These vertebrates are the same along the spatial range: environmental traits do not change the reservoirs along the large territory studied. The transmission of B. burgdorferi (s.l.) is amplified by a few species of vertebrates, that share biogeographical regions with the tick vector in variable proportions.
format Article
id doaj-art-2a89ad65f73047d8a6fb53b888c9f801
institution Kabale University
issn 2667-114X
language English
publishDate 2024-01-01
publisher Elsevier
record_format Article
series Current Research in Parasitology and Vector-Borne Diseases
spelling doaj-art-2a89ad65f73047d8a6fb53b888c9f8012024-11-30T07:14:27ZengElsevierCurrent Research in Parasitology and Vector-Borne Diseases2667-114X2024-01-016100198A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplificationAgustin Estrada-Peña0Hein Sprong1Sara R. Wijburg2Department of Animal Health, University of Zaragoza, Spain; Instituto Agroalimentario de Aragón, IA2, 50013-Zaragoza, Spain; Ministry of Human Health, Madrid, Spain; Corresponding author.Department of Animal Health, University of Zaragoza, SpainCentre for Infectious Diseases, National Institute for Public Health and the Environment, 3720 BA Bilthoven, the NetherlandsCentre for Infectious Diseases, National Institute for Public Health and the Environment, 3720 BA Bilthoven, the NetherlandsThe tick Ixodes ricinus parasitizes a wide range of vertebrates. These hosts vary in the relative contribution to the feeding of the different tick life stages, and their interplay is pivotal in the transmission dynamics of tick-borne pathogens. We aimed to know if there is a phylogenetic signal in the feeding and propagation hosts of I. ricinus, independently of other traits, as well as in the amplification of Borrelia burgdorferi (s.l.) in feeding larvae. We used a compilation of 1127 published field surveys in Europe, providing data for 96,586 hosts, resulting in 265,124 larvae, 72,080 nymphs and 37,726 adults. The load of immature ticks on hosts showed a significant phylogenetic signal towards the genera Psammodromus, Podarcis, and Lacerta (nymphs only). We hypothesize that such signal is the background hallmark of the primitive hosts associations of I. ricinus, probably in the glaciation refugia. A secondary phylogenetic signal for tick immatures appeared for some genera of Rodentia and Eulipotyphla. Results suggest the notion that the tick gained these hosts after spread from glaciation refugia. Analyses support a phylogenetic signal in the tick adults, firmly linked to Cetartiodactyla, but not to Carnivora or Aves. This study provides the first demonstration of host preferences in the generalist tick I. ricinus. We further demonstrate that combinations of vertebrates contribute in different proportions supporting the tick life-cycle in biogeographical regions of the Western Palaearctic as each region has unique combinations of dominant hosts. Analysis of the amplification of B. burgdorferi (s.l.) demonstrated that each genospecies is better amplified by competent reservoirs with which a strong phylogenetic signal exists. These vertebrates are the same along the spatial range: environmental traits do not change the reservoirs along the large territory studied. The transmission of B. burgdorferi (s.l.) is amplified by a few species of vertebrates, that share biogeographical regions with the tick vector in variable proportions.http://www.sciencedirect.com/science/article/pii/S2667114X24000293Ixodes ricinusPhylogenetic signalPropagation/amplification hostsAmplificationBorrelia burgdorferi (s.l.)
spellingShingle Agustin Estrada-Peña
Hein Sprong
Sara R. Wijburg
A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplification
Current Research in Parasitology and Vector-Borne Diseases
Ixodes ricinus
Phylogenetic signal
Propagation/amplification hosts
Amplification
Borrelia burgdorferi (s.l.)
title A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplification
title_full A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplification
title_fullStr A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplification
title_full_unstemmed A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplification
title_short A crucial nexus: Phylogenetic versus ecological support of the life-cycle of Ixodes ricinus (Ixodoidea: Ixodidae) and Borrelia spp. amplification
title_sort crucial nexus phylogenetic versus ecological support of the life cycle of ixodes ricinus ixodoidea ixodidae and borrelia spp amplification
topic Ixodes ricinus
Phylogenetic signal
Propagation/amplification hosts
Amplification
Borrelia burgdorferi (s.l.)
url http://www.sciencedirect.com/science/article/pii/S2667114X24000293
work_keys_str_mv AT agustinestradapena acrucialnexusphylogeneticversusecologicalsupportofthelifecycleofixodesricinusixodoideaixodidaeandborreliasppamplification
AT heinsprong acrucialnexusphylogeneticversusecologicalsupportofthelifecycleofixodesricinusixodoideaixodidaeandborreliasppamplification
AT sararwijburg acrucialnexusphylogeneticversusecologicalsupportofthelifecycleofixodesricinusixodoideaixodidaeandborreliasppamplification
AT agustinestradapena crucialnexusphylogeneticversusecologicalsupportofthelifecycleofixodesricinusixodoideaixodidaeandborreliasppamplification
AT heinsprong crucialnexusphylogeneticversusecologicalsupportofthelifecycleofixodesricinusixodoideaixodidaeandborreliasppamplification
AT sararwijburg crucialnexusphylogeneticversusecologicalsupportofthelifecycleofixodesricinusixodoideaixodidaeandborreliasppamplification