Conservation of Transmission Phenotype of Anaplasma marginale (Rickettsiales: Anaplasmataceae) Strains Among Dermacentor and Rhipicephalus Ticks (Acari: Ixodidae)

Authors: Scoles, Glen; UETI, M - WSU; Noh, Susan; Knowles Jr, Donald; PALMER, G - WSU

Submitted to: Journal of Medical Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/30/2006
Publication Date: 5/15/2007
Citation: Scoles, G.A., Ueti, M.W., Noh, S.M., Knowles Jr, D.P., Palmer, G.H. 2007. Conservation of Transmission Phenotype of Anaplasma marginale (Rickettsiales: Anaplasmataceae) Strains Among Dermacentor and Rhipicephalus Ticks (Acari: Ixodidae). Journal of Medical Entomology. 44(3):484-491

Interpretive Summary: The cattle fever tick and the tropical cattle tick had been eradicated from the United States by 1943; prior that date, these tick species had been the primary vectors of the bacterium that causes the disease anaplasmosis in U.S. cattle. In the absence of the cattle ticks, anaplasma has continued to be transmitted by Dermacentor ticks like the Rocky Mountain wood tick and the American dog tick. However, a few strains of anaplasma have been collected from the United States that these Dermacentor ticks cannot transmit. This raises the question of how these strains evolved and how they survive without a biological vector. Our hypothesis was that the anaplasma strains that cannot be transmitted by Dermacentor ticks are cattle tick transmissible strains that have been maintained by mechanical transmission since the eradication of the cattle ticks. To test this hypothesis we tried to transmit a non-Dermacentor transmissible anaplasma strain that was collected from Florida. We used the wood tick and the two species of cattle tick that formerly occurred in the US. For comparison we used a strain of anaplasma collected from Puerto Rico that we know can be transmitted by both the wood tick and the tropical cattle tick. The Puerto Rico anaplasma was transmitted by all three species of tick, but none of the ticks were able to transmit the Florida anaplasma, even though a small number of ticks were infected at a low level with the Florida anaplasma. This shows that the ability of a strain of anaplasma to be transmitted by ticks is maintained, even in different tick species. Because the Florida strain was able to infect a small portion of the ticks at a low level we believe that the failure of this strain to be transmitted by ticks is related to a general inability of the bacterium to efficiently enter or grow in tick cells, instead of an inability to enter or grow in the cells of specific tick species.

Technical Abstract: Before the eradication of Boophilus ticks from the United States, Rhipicephalus (Boophilus) microplus (Canestrini) and Rhipicephalus (Boophilus) annulatus (Say) were important biological vectors of the cattle pathogen Anaplasma marginale Theiler. In the absence of Boophilus ticks, A. marginale continues to be transmitted by Dermacentor ticks. However, a few U.S. strains are not transmissible by Dermacentor andersoni Stiles, Dermacentor variabilis (Say), or both, raising the question of how these strains evolved and how they are maintained. We hypothesize that the U.S. non-Dermacentor-transmissible strains of A. marginale were formerly Boophilus-transmitted strains that have been maintained by a combination of persistent infection and mechanical transmission since the eradication of their biological vector from the United States. To test this hypothesis, we attempted to transmit a well-documented non-Dermacentor-transmissible A. marginale strain (Florida), by using D. andersoni and the two Boophilus species that formerly occurred in the United States. For comparison, we examined tick-borne transmission of a strain of A. marginale (Puerto Rico), which has previously been shown to be transmissible by both D. andersoni and B. microplus. All three species of tick transmitted the Puerto Rico strain, and immunohistochemical (IHC) analysis confirmed the presence of A. marginale colonies in their salivary glands. All three tick species failed to transmit the Florida strain. Although both D. andersoni and B. microplus acquired transient midgut and salivary gland infections after acquisition feeding, we were unable to detect colonies of the Florida strain in the salivary glands with IHC. This demonstrates that the transmission phenotype of A. marginale strains is conserved among tick species, and it suggests that the failure of the Florida strain to be transmitted by ticks is related to a general inability to efficiently invade or replicate in tick cells, rather than to a failure to invade or replicate in cells of a specific tick species.