Transovarial transmission of Babesia ovis in Rhipicephalus bursa, confirmed by multi-generational experiments

Abstract

Babesia ovis is a tick-transmitted intraerythrocytic apicomplexan parasite that causes ovine babesiosis, a disease with high economic impact in endemic regions. Although Rhipicephalus bursa is a known biological vector of B. ovis, the dynamics of vertical (transovarial) transmission are poorly understood. In the present study, the transovarial transmission of B. ovis was investigated experimentally in four continuous generations of R. bursa under laboratory controlled conditions. A total of 11 sheep were used during the study. An initial stabilate co-infected with B. ovis and Theileria ovis was inoculated into a splenectomized sheep, followed by an infestation with Babesia-free adult R. bursa. Study of dead tick bodies and larval pools by molecular methodology confirmed the elimination of T. ovis and the vertical transmission B. ovis. Rhipicephalus bursa ticks derived vertically from F1 to F4 generations kept high levels of infection (98% in F3 adults), and consistently led to severe clinical babesiosis in both immunosuppressed and immunocompetent sheep. Although all feeding stages became infected while feeding on their hosts, only adult ticks were able to transmit the parasite to vertebrate hosts. Our findings demonstrate that B. ovis can be transmitted vertically through several tick generations, while preserving its ability to cause severe disease, even without selective pressure. The virulent, mono-infected B. ovis strain developed in this study will provide an infectious challenge model for future vaccine and pathogenesis studies under field-relevant conditions. Babesia ovis est un parasite apicomplexe intra & eacute;rythrocytaire transmis par les tiques et responsable de la bab & eacute;siose ovine, une maladie & agrave; fort impact & eacute;conomique dans les r & eacute;gions end & eacute;miques. Bien que Rhipicephalus bursa soit un vecteur biologique connu de B. ovis, la dynamique de la transmission verticale (transovarienne) est mal comprise. Dans la pr & eacute;sente & eacute;tude, la transmission transovarienne de B. ovis a & eacute;t & eacute; & eacute;tudi & eacute;e exp & eacute;rimentalement sur quatre g & eacute;n & eacute;rations continues de R. bursa dans des conditions contr & ocirc;l & eacute;es en laboratoire. Au total, 11 moutons ont & eacute;t & eacute; utilis & eacute;s au cours de l'& eacute;tude. Un stabilat initial co-infect & eacute; par B. ovis et Theileria ovis a & eacute;t & eacute; inocul & eacute; & agrave; un mouton spl & eacute;nectomis & eacute;, suivi d'une infestation par des adultes de R. bursa indemnes de Babesia. L'& eacute;tude des tiques mortes et des lots de larves par m & eacute;thodologie mol & eacute;culaire a confirm & eacute; l'& eacute;limination de T. ovis et la transmission verticale de B. ovis. Les tiques R. bursa d & eacute;riv & eacute;es verticalement des g & eacute;n & eacute;rations F1 & agrave; F4 ont conserv & eacute; des niveaux d'infection & eacute;lev & eacute;s (98 % chez les adultes F3) et ont syst & eacute;matiquement entra & icirc;n & eacute; une bab & eacute;siose clinique s & eacute;v & egrave;re chez les moutons immunod & eacute;prim & eacute;s et immunocomp & eacute;tents. Bien que tous les stades d'alimentation aient & eacute;t & eacute; infect & eacute;s en se nourrissant de leurs h & ocirc;tes, seules les tiques adultes ont pu transmettre le parasite & agrave; leurs h & ocirc;tes vert & eacute;br & eacute;s. Nos r & eacute;sultats d & eacute;montrent que B. ovis peut & ecirc;tre transmis verticalement par plusieurs g & eacute;n & eacute;rations de tiques tout en pr & eacute;servant sa capacit & eacute; & agrave; provoquer une maladie grave, m & ecirc;me en l'absence de pression s & eacute;lective. La souche virulente et mono-infect & eacute;e de B. ovis d & eacute;velopp & eacute;e dans cette & eacute;tude fournira un mod & egrave;le infectieux pour de futures & eacute;tudes de vaccin et de pathog & eacute;n & egrave;se dans des conditions de terrain.