Cardinium symbiosis as a potential confounder of mtDNA based phylogeographic inference in Culicoides imicola (Diptera: Ceratopogonidae), a vector of veterinary viruses

Stefanos Siozios,Gert Venter,Jack Pilgrim,Matthew Baylis,Gregory D D Hurst,Claire Garros

doi:10.1186/s13071-020-04568-3

Abstract

BackgroundCulicoides imicola (Diptera: Ceratopogonidae) is an important Afrotropical and Palearctic vector of disease, transmitting viruses of animal health and economic significance including African horse sickness and bluetongue viruses. Maternally inherited symbiotic bacteria (endosymbionts) of arthropods can alter the frequency of COI (cytochrome c oxidase subunit I) mitochondrial haplotypes (mitotypes) in a population, masking the true patterns of host movement and gene flow. Thus, this study aimed to assess the mtDNA structure of C. imicola in relation to infection with Candidatus Cardinum hertigii (Bacteroides), a common endosymbiont of Culicoides spp.MethodsUsing haplotype network analysis, COI Sanger sequences from Cardinium-infected and -uninfected C. imicola individuals were first compared in a population from South Africa. The network was then extended to include mitotypes from a geographic range where Cardinium infection has previously been investigated.ResultsThe mitotype network of the South African population demonstrated the presence of two broad mitotype groups. All Cardinium-infected specimens fell into one group (Fisher’s exact test, P = 0.00071) demonstrating a linkage disequilibrium between endosymbiont and mitochondria. Furthermore, by extending this haplotype network to include other C. imicola populations from the Mediterranean basin, we revealed mitotype variation between the Eastern and Western Mediterranean basins (EMB and WMB) mirrored Cardinium-infection heterogeneity.ConclusionsThese observations suggest that the linkage disequilibrium of Cardinium and mitochondria reflects endosymbiont gene flow within the Mediterranean basin but may not assist in elucidating host gene flow. Subsequently, we urge caution on the single usage of the COI marker to determine population structure and movement in C. imicola and instead suggest the complementary utilisation of additional molecular markers.Graphical

Highlights

Culicoides imicola (Diptera: Ceratopogonidae) is an important Afrotropical and Palearctic vector of disease, transmitting viruses of animal health and economic significance including African horse sickness and bluetongue viruses
To confirm individuals in this study were not cryptic species of C. imicola missed by morphological identification, a distance estimation of Mitochondrial DNA (mtDNA) barcodes was assessed giving a minimum identity of > 98%, consistent with all individuals belonging to the same species
Extending the haplotype network to include C. imicola populations from the Western Mediterranean Basin (WMB; Corsica and Portugal) and the Eastern Mediterranean Basin (EMB; Israel) led to 12 haplotypes being observed with 0–1.77% range of divergence over a 451 bp region

Summary

Introduction

Culicoides imicola (Diptera: Ceratopogonidae) is an important Afrotropical and Palearctic vector of disease, transmitting viruses of animal health and economic significance including African horse sickness and bluetongue viruses. This study aimed to assess the mtDNA structure of C. imicola in relation to infection with Candidatus Cardinum hertigii (Bacteroides), a common endosymbiont of Culicoides spp. As endosymbionts enter a naïve population, selective sweeps of the bacteria can occur and with them the homogenisation of linked mtDNA haplotypes, leading to the apparent absence of biodiversity [4]. Variation in endosymbiont presence over space can lead to a perceived genetic population structure when none exists. Inferences from these studies can only be interpreted in the context of any history of infection with endosymbiotic bacteria

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