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Background  Ticks are obligate haematophagous ectoparasites of vertebrates and frequently parasitize avian species that can carry them across continents during their long-distance migrations. Ticks may have detrimental effects on the health state of their avian hosts, which can be either directly caused by blood-draining or mediated by microbial pathogens transmitted during the blood meal. Indeed, ticks host complex microbial communities, including bacterial pathogens and symbionts.  Midichloria  bacteria ( Rickettsiales ) are widespread tick endosymbionts that can be transmitted to vertebrate hosts during the tick bite, inducing an antibody response. Their actual role as infectious/pathogenic agents is, however, unclear.    Methods  We screened for  Midichloria  DNA African ticks and blood samples collected from trans-Saharan migratory songbirds at their arrival in Europe during spring migration.    Results  Tick infestation rate was 5.7%, with most ticks belonging to the  Hyalomma marginatum  species complex. Over 90% of  Hyalomma  ticks harboured DNA of  Midichloria  bacteria belonging to the monophylum associated with ticks.  Midichloria  DNA was detected in 43% of blood samples of avian hosts. Tick-infested adult birds were significantly more likely to test positive to the presence of  Midichloria  DNA than non-infested adults and second-year individuals, suggesting a long-term persistence of these bacteria within avian hosts. Tick parasitism was associated with a significantly delayed timing of spring migration of avian hosts but had no significant effects on body condition, whereas blood  Midichloria  DNA presence negatively affected fat deposits of tick-infested avian hosts.    Conclusions  Our results show that ticks effectively transfer  Midichloria  bacteria to avian hosts, supporting the hypothesis that they are infectious to vertebrates. Bird infection likely enhances the horizontal spread of these bacteria across haematophagous ectoparasite populations. Moreover, we showed that  Midichloria  and tick parasitism have detrimental non-independent effects on avian host health during migration, highlighting the complexity of interactions involving ticks, their vertebrate hosts, and tick-borne bacteria.    Electronic supplementary material  The online version of this article (10.1186/s13071-018-2669-z) contains supplementary material, which is available to authorized users.

Patterns of Midichloria infection in avian-borne African ticks and their trans-Saharan migratory hosts