A generalist vector-transmitted parasite exhibits population genetic structure among host genera

Generalist parasites experience selective pressures from the various host species they infect. However, it is unclear if parasite transmission among host species precludes the establishment of host-specific adaptations and population genetic structure. We assessed the population genetic structure of...

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Main Authors: Vincenzo A. Ellis, Mélanie Duc, Arif Ciloglu, Olof Hellgren, Staffan Bensch
Format: Article
Language:English
Published: Cambridge University Press
Series:Parasitology
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Online Access:https://www.cambridge.org/core/product/identifier/S0031182024001641/type/journal_article
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author Vincenzo A. Ellis
Mélanie Duc
Arif Ciloglu
Olof Hellgren
Staffan Bensch
author_facet Vincenzo A. Ellis
Mélanie Duc
Arif Ciloglu
Olof Hellgren
Staffan Bensch
author_sort Vincenzo A. Ellis
collection DOAJ
description Generalist parasites experience selective pressures from the various host species they infect. However, it is unclear if parasite transmission among host species precludes the establishment of host-specific adaptations and population genetic structure. We assessed the population genetic structure of the vector-transmitted avian haemosporidian parasite Haemoproteus majoris (lineage WW2; n = 34 infections) in a single site in southern Sweden among 10 of its host species. The 2 best-sampled host genera were Phylloscopus (2 species, n = 15 infections) and Sylvia (4 species, n = 15). We designed a sequence capture protocol to isolate 1.13 Mbp (ca. 5%) of the parasite genome and identified 1399 variable sites among the sequenced infections. In a principal components analysis, infections of Phylloscopus and Sylvia species mostly separated along the first 2 principal components. Sites with the highest FST values between the genera were found in genes that have mostly not been implicated in infection pathways, but several sites code for amino acid changes. An analysis of molecular variance confirmed significant variation among host genera, but not among host species within genera. The distribution of Tajima’s D among sequenced loci was negatively skewed, plausibly reflecting a history of bottleneck followed by population expansion. Tajima’s D was lower in infections of Phylloscopus than Sylvia, plausibly because WW2 began infecting Phylloscopus hosts after it was already a parasite of Sylvia hosts. Our results provide evidence of vector-transmitted parasite population differentiation among host species in a single location. Future work should focus on identifying the mechanisms underlying this genetic population structure.
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spelling doaj-art-ff54647de9224dec8c2d3954dbab5a102025-01-30T15:22:27ZengCambridge University PressParasitology0031-18201469-816111010.1017/S0031182024001641A generalist vector-transmitted parasite exhibits population genetic structure among host generaVincenzo A. Ellis0https://orcid.org/0000-0002-7193-9408Mélanie Duc1https://orcid.org/0000-0001-5468-2594Arif Ciloglu2https://orcid.org/0000-0003-2695-7102Olof Hellgren3https://orcid.org/0000-0002-4062-7276Staffan Bensch4https://orcid.org/0000-0002-0082-0899Department of Entomology and Wildlife Ecology, University of Delaware, Newark, DE, USAP. B. Šivickis Laboratory of Parasitology, Nature Research Centre, Vilnius, LithuaniaDepartment of Parasitology, Faculty of Veterinary Medicine, Erciyes University, Kayseri, Türkiye Vectors and Vector-Borne Diseases Implementation and Research Center, Erciyes University, Kayseri, TürkiyeDepartment of Biology, Lund University, Lund, SwedenDepartment of Biology, Lund University, Lund, SwedenGeneralist parasites experience selective pressures from the various host species they infect. However, it is unclear if parasite transmission among host species precludes the establishment of host-specific adaptations and population genetic structure. We assessed the population genetic structure of the vector-transmitted avian haemosporidian parasite Haemoproteus majoris (lineage WW2; n = 34 infections) in a single site in southern Sweden among 10 of its host species. The 2 best-sampled host genera were Phylloscopus (2 species, n = 15 infections) and Sylvia (4 species, n = 15). We designed a sequence capture protocol to isolate 1.13 Mbp (ca. 5%) of the parasite genome and identified 1399 variable sites among the sequenced infections. In a principal components analysis, infections of Phylloscopus and Sylvia species mostly separated along the first 2 principal components. Sites with the highest FST values between the genera were found in genes that have mostly not been implicated in infection pathways, but several sites code for amino acid changes. An analysis of molecular variance confirmed significant variation among host genera, but not among host species within genera. The distribution of Tajima’s D among sequenced loci was negatively skewed, plausibly reflecting a history of bottleneck followed by population expansion. Tajima’s D was lower in infections of Phylloscopus than Sylvia, plausibly because WW2 began infecting Phylloscopus hosts after it was already a parasite of Sylvia hosts. Our results provide evidence of vector-transmitted parasite population differentiation among host species in a single location. Future work should focus on identifying the mechanisms underlying this genetic population structure.https://www.cambridge.org/core/product/identifier/S0031182024001641/type/journal_articleavian haemosporidianshost specificityparasite evolutionpathogenpopulation genomics
spellingShingle Vincenzo A. Ellis
Mélanie Duc
Arif Ciloglu
Olof Hellgren
Staffan Bensch
A generalist vector-transmitted parasite exhibits population genetic structure among host genera
Parasitology
avian haemosporidians
host specificity
parasite evolution
pathogen
population genomics
title A generalist vector-transmitted parasite exhibits population genetic structure among host genera
title_full A generalist vector-transmitted parasite exhibits population genetic structure among host genera
title_fullStr A generalist vector-transmitted parasite exhibits population genetic structure among host genera
title_full_unstemmed A generalist vector-transmitted parasite exhibits population genetic structure among host genera
title_short A generalist vector-transmitted parasite exhibits population genetic structure among host genera
title_sort generalist vector transmitted parasite exhibits population genetic structure among host genera
topic avian haemosporidians
host specificity
parasite evolution
pathogen
population genomics
url https://www.cambridge.org/core/product/identifier/S0031182024001641/type/journal_article
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