New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences

Background: Amblyomma is the third most diversified genus of Ixodidae that is distributed across the Indomalayan, Afrotropical, Australasian (IAA), Nearctic and Neotropical biogeographic ecoregions, reaching in the Neotropic its highest diversity. There have been hints in previously published phylog...

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Authors: Uribe, Juan E., Kelava, Samuel, Nava, Santiago, Cotes-Perdomo, Andrea P., Castro, Lyda R., Rivera-Paéz, Fredy A., Perea, Silvia, Mans, Ben J., Gofton, Alexander, Teo, Ernest J. M., Zardoya, Rafael, Barker, Stephen C.
Format: article
Status:Published version
Publication Date:2024
Country:España
Institution:Consejo Superior de Investigaciones Científicas (CSIC)
Repository:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/389485
Online Access:http://hdl.handle.net/10261/389485
Access Level:Open access
Keyword:Ixodidae
Metastriata
Hard ticks
Pathogen vectors
Mitogenomics
Time-tree
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spelling New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequencesUribe, Juan E.Kelava, SamuelNava, SantiagoCotes-Perdomo, Andrea P.Castro, Lyda R.Rivera-Paéz, Fredy A.Perea, SilviaMans, Ben J.Gofton, AlexanderTeo, Ernest J. M.Zardoya, RafaelBarker, Stephen C.IxodidaeMetastriataHard ticksPathogen vectorsMitogenomicsTime-treeBackground: Amblyomma is the third most diversified genus of Ixodidae that is distributed across the Indomalayan, Afrotropical, Australasian (IAA), Nearctic and Neotropical biogeographic ecoregions, reaching in the Neotropic its highest diversity. There have been hints in previously published phylogenetic trees from mitochondrial genome, nuclear rRNA, from combinations of both and morphology that the Australasian Amblyomma or the Australasian Amblyomma plus the Amblyomma species from the southern cone of South America, might be sister-group to the Amblyomma of the rest of the world. However, a stable phylogenetic framework of Amblyomma for a better understanding of the biogeographic patterns underpinning its diversification is lacking. Methods: We used genomic techniques to sequence complete and nearly complete mitochondrial genomes –ca. 15 kbp– as well as the nuclear ribosomal cluster –ca. 8 kbp– for 17 Amblyomma ticks in order to study the phylogeny and biogeographic pattern of the genus Amblyomma, with particular emphasis on the Neotropical region. The new genomic information generated here together with genomic information available on 43 ticks (22 other Amblyomma species and 21 other hard ticks–as outgroup–) were used to perform probabilistic methods of phylogenetic and biogeographic inferences and time-tree estimation using biogeographic dates. Results: In the present paper, we present the strongest evidence yet that Australasian Amblyomma may indeed be the sister-group to the Amblyomma of the rest of the world (species that occur mainly in the Neotropical and Afrotropical zoogeographic regions). Our results showed that all Amblyomma subgenera (Cernyomma, Anastosiella, Xiphiastor, Adenopleura, Aponomma and Dermiomma) are not monophyletic, except for Walkeriana and Amblyomma. Likewise, our best biogeographic scenario supports the origin of Amblyomma and its posterior diversification in the southern hemisphere at 47.8 and 36.8 Mya, respectively. This diversification could be associated with the end of the connection of Australasia and Neotropical ecoregions by the Antarctic land bridge. Also, the biogeographic analyses let us see the colonization patterns of some neotropical Amblyomma species to the Nearctic. Conclusions: We found strong evidence that the main theater of diversification of Amblyomma was the southern hemisphere, potentially driven by the Antarctic Bridge's intermittent connection in the late Eocene. In addition, the subgeneric classification of Amblyomma lacks evolutionary support. Future studies using denser taxonomic sampling may lead to new findings on the phylogenetic relationships and biogeographic history of Amblyomma genus.This study was supported by Atracción Talento de la Comunidad de Madrid Fellowship Program (REFF 2019- T2/ AMB-13166)Peer reviewedBioMed CentralComunidad de MadridUribe, Juan E. [0000-0002-9215-9689]Perea, Silvia [0000-0003-0436-8577]Zardoya, Rafael [0000-0001-6212-9502]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/389485reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/Comunidad de Madrid/Atracción Talento/2019-T2https://doi.org/10.1186/s13071-024-06131-wSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3894852026-05-22T06:33:51Z
dc.title.none.fl_str_mv New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
title New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
spellingShingle New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
Uribe, Juan E.
Ixodidae
Metastriata
Hard ticks
Pathogen vectors
Mitogenomics
Time-tree
title_short New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
title_full New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
title_fullStr New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
title_full_unstemmed New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
title_sort New insights into the molecular phylogeny, biogeographical history, and diversification of Amblyomma ticks (Acari: Ixodidae) based on mitogenomes and nuclear sequences
dc.creator.none.fl_str_mv Uribe, Juan E.
Kelava, Samuel
Nava, Santiago
Cotes-Perdomo, Andrea P.
Castro, Lyda R.
Rivera-Paéz, Fredy A.
Perea, Silvia
Mans, Ben J.
Gofton, Alexander
Teo, Ernest J. M.
Zardoya, Rafael
Barker, Stephen C.
author Uribe, Juan E.
author_facet Uribe, Juan E.
Kelava, Samuel
Nava, Santiago
Cotes-Perdomo, Andrea P.
Castro, Lyda R.
Rivera-Paéz, Fredy A.
Perea, Silvia
Mans, Ben J.
Gofton, Alexander
Teo, Ernest J. M.
Zardoya, Rafael
Barker, Stephen C.
author_role author
author2 Kelava, Samuel
Nava, Santiago
Cotes-Perdomo, Andrea P.
Castro, Lyda R.
Rivera-Paéz, Fredy A.
Perea, Silvia
Mans, Ben J.
Gofton, Alexander
Teo, Ernest J. M.
Zardoya, Rafael
Barker, Stephen C.
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Comunidad de Madrid
Uribe, Juan E. [0000-0002-9215-9689]
Perea, Silvia [0000-0003-0436-8577]
Zardoya, Rafael [0000-0001-6212-9502]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Ixodidae
Metastriata
Hard ticks
Pathogen vectors
Mitogenomics
Time-tree
topic Ixodidae
Metastriata
Hard ticks
Pathogen vectors
Mitogenomics
Time-tree
description Background: Amblyomma is the third most diversified genus of Ixodidae that is distributed across the Indomalayan, Afrotropical, Australasian (IAA), Nearctic and Neotropical biogeographic ecoregions, reaching in the Neotropic its highest diversity. There have been hints in previously published phylogenetic trees from mitochondrial genome, nuclear rRNA, from combinations of both and morphology that the Australasian Amblyomma or the Australasian Amblyomma plus the Amblyomma species from the southern cone of South America, might be sister-group to the Amblyomma of the rest of the world. However, a stable phylogenetic framework of Amblyomma for a better understanding of the biogeographic patterns underpinning its diversification is lacking. Methods: We used genomic techniques to sequence complete and nearly complete mitochondrial genomes –ca. 15 kbp– as well as the nuclear ribosomal cluster –ca. 8 kbp– for 17 Amblyomma ticks in order to study the phylogeny and biogeographic pattern of the genus Amblyomma, with particular emphasis on the Neotropical region. The new genomic information generated here together with genomic information available on 43 ticks (22 other Amblyomma species and 21 other hard ticks–as outgroup–) were used to perform probabilistic methods of phylogenetic and biogeographic inferences and time-tree estimation using biogeographic dates. Results: In the present paper, we present the strongest evidence yet that Australasian Amblyomma may indeed be the sister-group to the Amblyomma of the rest of the world (species that occur mainly in the Neotropical and Afrotropical zoogeographic regions). Our results showed that all Amblyomma subgenera (Cernyomma, Anastosiella, Xiphiastor, Adenopleura, Aponomma and Dermiomma) are not monophyletic, except for Walkeriana and Amblyomma. Likewise, our best biogeographic scenario supports the origin of Amblyomma and its posterior diversification in the southern hemisphere at 47.8 and 36.8 Mya, respectively. This diversification could be associated with the end of the connection of Australasia and Neotropical ecoregions by the Antarctic land bridge. Also, the biogeographic analyses let us see the colonization patterns of some neotropical Amblyomma species to the Nearctic. Conclusions: We found strong evidence that the main theater of diversification of Amblyomma was the southern hemisphere, potentially driven by the Antarctic Bridge's intermittent connection in the late Eocene. In addition, the subgeneric classification of Amblyomma lacks evolutionary support. Future studies using denser taxonomic sampling may lead to new findings on the phylogenetic relationships and biogeographic history of Amblyomma genus.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/389485
url http://hdl.handle.net/10261/389485
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/Comunidad de Madrid/Atracción Talento/2019-T2
https://doi.org/10.1186/s13071-024-06131-w
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
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