RESUMEN
Tick-borne pathogen co-infections are common in nature. Co-infecting pathogens interact with each other and the tick microbiome, which influences individual pathogen fitness, and ultimately shapes virulence, infectivity, and transmission. In this review, we discuss how tick-borne pathogens are an ideal framework to study the evolutionary dynamics of co-infections. We highlight the importance of inter-species and intra-species interactions in vector-borne pathogen ecology and evolution. We also propose experimental evolution in tick cell lines as a method to directly test the impact of co-infections on pathogen evolution. Experimental evolution can simulate in real-time the long periods of time involved in within-vector pathogen interactions in nature, a major practical obstacle to cracking the influence of co-infections on pathogen evolution and ecology.
RESUMEN
Multistrain microbial pathogens often induce strain-specific antibody responses in their vertebrate hosts. Mothers can transmit antibodies to their offspring, which can provide short-term, strain-specific protection against infection. Few experimental studies have investigated this phenomenon for multiple strains of zoonotic pathogens occurring in wildlife reservoir hosts. The tick-borne bacterium Borrelia afzelii causes Lyme disease in Europe and consists of multiple strains that cycle between the tick vector (Ixodes ricinus) and vertebrate hosts, such as the bank vole (Myodes glareolus). We used a controlled experiment to show that female bank voles infected with B. afzelii via tick bite transmit protective antibodies to their offspring. To test the specificity of protection, the offspring were challenged using a natural tick bite challenge with either the maternal strain to which the mothers had been exposed or a different strain. The maternal antibodies protected the offspring against a homologous infectious challenge but not against a heterologous infectious challenge. The offspring from the uninfected control mothers were equally susceptible to both strains. Borrelia outer surface protein C (OspC) is an antigen that is known to induce strain-specific immunity. Maternal antibodies in the offspring reacted more strongly with homologous than with heterologous recombinant OspC, but other antigens may also mediate strain-specific immunity. Our study shows that maternal antibodies provide strain-specific protection against B. afzelii in an ecologically important rodent reservoir host. The transmission of maternal antibodies may have important consequences for the epidemiology of multistrain pathogens in nature.IMPORTANCE Many microbial pathogen populations consist of multiple strains that induce strain-specific antibody responses in their vertebrate hosts. Females can transmit these antibodies to their offspring, thereby providing them with short-term strain-specific protection against microbial pathogens. We investigated this phenomenon using multiple strains of the tick-borne microbial pathogen Borrelia afzelii and its natural rodent reservoir host, the bank vole, as a model system. We found that female bank voles infected with B. afzelii transmitted to their offspring maternal antibodies that provided highly efficient but strain-specific protection against a natural tick bite challenge. The transgenerational transfer of antibodies could be a mechanism that maintains the high strain diversity of this tick-borne pathogen in nature.
Asunto(s)
Anticuerpos Antiprotozoarios/inmunología , Arvicolinae , Grupo Borrelia Burgdorferi/fisiología , Inmunidad Materno-Adquirida/inmunología , Enfermedad de Lyme/inmunología , Enfermedades de los Roedores/inmunología , Zoonosis/inmunología , Animales , Enfermedad de Lyme/parasitología , Enfermedades de los Roedores/parasitología , Zoonosis/parasitologíaRESUMEN
The study of polymorphic immune genes in host populations is critical for understanding genetic variation in susceptibility to pathogens. Controlled infection experiments are necessary to separate variation in the probability of exposure from genetic variation in susceptibility to infection, but such experiments are rare for wild vertebrate reservoir hosts and their zoonotic pathogens. The bank vole (Myodes glareolus) is an important reservoir host of Borrelia afzelii, a tick-borne spirochete that causes Lyme disease. Bank vole populations are polymorphic for Toll-like receptor 2 (TLR2), an innate immune receptor that recognizes bacterial lipoproteins. To test whether the TLR2 polymorphism influences variation in the susceptibility to infection with B. afzelii, we challenged pathogen-free, lab-born individuals of known TLR2 genotype with B. afzelii-infected ticks. We measured the spirochete load in tissues of the bank voles. The susceptibility to infection with B. afzelii following an infected tick bite was very high (95%) and did not differ between TLR2 genotypes. The TLR2 polymorphism also had no effect on the spirochete abundance in the tissues of the bank voles. Under the laboratory conditions of our study, we did not find that the TLR2 polymorphism in bank voles influenced variation in the susceptibility to B. afzelii infection.
Asunto(s)
Arvicolinae/genética , Arvicolinae/microbiología , Enfermedad de Lyme/veterinaria , Polimorfismo Genético , Receptor Toll-Like 2/genética , Animales , Grupo Borrelia Burgdorferi/genética , Grupo Borrelia Burgdorferi/patogenicidad , Reservorios de Enfermedades , Femenino , Predisposición Genética a la Enfermedad , Enfermedad de Lyme/genética , Masculino , Ninfa/microbiología , Garrapatas/microbiologíaRESUMEN
Multiple-strain pathogens often establish mixed infections inside the host that result in competition between strains. In vector-borne pathogens, the competitive ability of strains must be measured in both the vertebrate host and the arthropod vector to understand the outcome of competition. Such studies could reveal the existence of trade-offs in competitive ability between different host types. We used the tick-borne bacterium Borrelia afzelii to test for competition between strains in the rodent host and the tick vector, and to test for a trade-off in competitive ability between these two host types. Mice were infected via tick bite with either one or two strains, and these mice were subsequently used to create ticks with single or mixed infections. Competition in the rodent host reduced strain-specific host-to-tick transmission and competition in the tick vector reduced the abundance of both strains. The strain that was competitively superior in host-to-tick transmission was competitively inferior with respect to bacterial abundance in the tick. This study suggests that in multiple-strain vector-borne pathogens there are trade-offs in competitive ability between the vertebrate host and the arthropod vector. Such trade-offs could play an important role in the coexistence of pathogen strains.
Asunto(s)
Grupo Borrelia Burgdorferi/fisiología , Ixodes/microbiología , Enfermedad de Lyme/transmisión , Animales , Vectores Arácnidos/microbiología , Grupo Borrelia Burgdorferi/clasificación , Grupo Borrelia Burgdorferi/genética , Femenino , Ixodes/crecimiento & desarrollo , Estadios del Ciclo de Vida , Enfermedad de Lyme/microbiología , Ratones Endogámicos BALB CRESUMEN
The impact of a pathogen on the fitness and behaviour of its natural host depends upon the host-parasite relationship in a given set of environmental conditions. Here, we experimentally investigated the effects of Borrelia afzelii, one of the aetiological agents of Lyme disease in humans, on the fitness of its natural rodent host, the bank vole (Myodes glareolus), in semi-natural conditions with two contrasting host population densities. Our results show that B. afzelii can modify the reproductive success and spacing behaviour of its rodent host, whereas host survival was not affected. Infection impaired the breeding probability of large bank voles. Reproduction was hastened in infected females without alteration of the offspring size at birth. At low density, infected males produced fewer offspring, fertilized fewer females and had lower mobility than uninfected individuals. Meanwhile, the infection did not affect the proportion of offspring produced or the proportion of mating partner in female bank voles. Our study is the first to show that B. afzelii infection alters the reproductive success of the natural host. The effects observed could reflect the sickness behaviour due to the infection or they could be a consequence of a manipulation of the host behaviour by the bacteria.
Asunto(s)
Arvicolinae/microbiología , Grupo Borrelia Burgdorferi/fisiología , Reproducción/fisiología , Enfermedades de los Roedores/microbiología , Animales , Arvicolinae/fisiología , Grupo Borrelia Burgdorferi/patogenicidad , Femenino , Interacciones Huésped-Patógeno/fisiología , Enfermedad de Lyme/microbiología , Masculino , Densidad de Población , Conducta Sexual Animal/fisiologíaRESUMEN
The spirochete bacterium Borrelia afzelii is the most common cause of Lyme borreliosis in Europe. This tick-borne pathogen can establish systemic infections in rodents but not in birds. However, several field studies have recovered larval Ixodes ricinus ticks infected with B. afzelii from songbirds suggesting successful transmission of B. afzelii. We reviewed the literature to determine which songbird species were the most frequent carriers of B. afzelii-infected I. ricinus larvae and nymphs. We tested experimentally whether B. afzelii is capable of co-feeding transmission on two common European bird species, the blackbird (Turdus merula) and the great tit (Parus major). For each bird species, four naïve individuals were infested with B. afzelii-infected I. ricinus nymphal ticks and pathogen-free larval ticks. None of the co-feeding larvae tested positive for B. afzelii in blackbirds, but a low percentage of infected larvae (3.33%) was observed in great tits. Transstadial transmission of B. afzelii DNA from the engorged nymphs to the adult ticks was observed in both bird species. However, BSK culture found that these spirochetes were not viable. Our study suggests that co-feeding transmission of B. afzelii is not efficient in these two songbird species.