Multihost Bartonella parasites display covert host specificity even when transmitted by generalist vectors

Abstract

Summary Many parasites infect multiple sympatric host species, and there is a general assumption that parasite transmission between co‐occurring host species is commonplace. Such between‐species transmission could be key to parasite persistence within a disease reservoir and is consequently an emerging focus for disease control.However, while a growing body of theory indicates the potential importance of between‐species transmission for parasite persistence, conclusive empirical evidence from natural communities is lacking, and the assumption that between‐species transmission is inevitable may therefore be wrong.We investigated the occurrence of between‐species transmission in a well‐studied multihost parasite system. We identified the flea‐borne Bartonella parasites infecting sympatric populations of Apodemus sylvaticus (wood mice) and Myodes glareolus (bank voles) in the UK and confirmed that several Bartonella species infect both rodent species. However, counter to previous knowledge, genetic characterization of these parasites revealed covert host specificity, where each host species is associated with a distinct assemblage of genetic variants, indicating that between‐species transmission is rare.Limited between‐species transmission could result from rare encounters between one host species and the parasites infecting another and/or host–parasite incompatibility. We investigated the occurrence of such encounter and compatibility barriers by identifying the flea species associated with each rodent host, and the Bartonella variants carried by individual fleas. We found that the majority of fleas were host‐generalists but the assemblage of Bartonella variants in fleas tended to reflect the assemblage of Bartonella variants in the host species they were collected from, thus providing evidence of encounter barriers mediated by limited between‐species flea transfer. However, we also found several fleas that were carrying variants never found in the host species from which they were collected, indicating some degree of host–pathogen incompatibility when barriers to encounter are overcome.Overall, these findings challenge our default perceptions of multihost parasite persistence, as they show that despite considerable overlaps in host species ecology, separate populations of the same parasite species may circulate and persist independently in different sympatric host species. This questions our fundamental understanding of endemic transmission dynamics and the control of infection within natural reservoir communities.

Host Phylogeny, Geographic Overlap, and Roost Sharing Shape Parasite Communities in European Bats

“…Myotis oxygnathus was considered a synonym for My. blythii (Agnarsson et al, 2011;Balvín and Bartonička, 2014;Wilson and Reeder, 2015).…”

“…As long as noise does not totally obscure the predominant host-microbe associations, then it will be possible to measure the host-specific signal, either statistically or through genetic data. For example, Withenshaw et al (2016) were able to show that distinct genetic variants of Bartonella species separately infect two sympatric rodent species despite the presence of generalist flea vectors. Since the two host species have differences in microhabitat usage and activity patterns, they would rarely have opportunity to exchange fleas.…”

Linking community assembly and structure across scales in a wild mouse parasite community

“…The MSMs used the three most prevalent parasite species from all years of data collection: gastrointestinal parasites H. polygyrus (33% infection 2009–2011, 22.4% 2012) and E. hungaryensis (28.4% infected 2009–2011, 18% 2012), which have been found to interact within coinfected mice (Knowles et al, ), and the flea‐transmitted, blood‐borne bacterium B. taylorii (23.3% infected, 31.7% 2012; Withenshaw et al, ). Hence, the predictions for individual‐level community assembly based on the population‐level nestedness analysis using 2009–2011 data were: Uninfected → E. hungaryensis → E. hungaryensis + H. polygyrus → E. hungaryensis + H. polygyrus + B. taylorii (Figure d); predictions from the 2012 data were: Uninfected → B. taylorii → B. taylorii + H. polygyrus → B. taylorii + H. polygyrus + E. hungaryensis (Figure e).…”

“…There were five 70 × 70m grids among the sites, where each grid had 64 trap stations (10 m apart), with 2 Sherman live traps (2 × 2.5 × 6.5‐inch folding trap, H.B. Sherman) at each trapping station, 128 traps per grid (Knowles, Fenton, & Pedersen, ; Withenshaw, Devevey, Pedersen, & Fenton, ). The traps were baited at dusk with crimped oats and carrot; bedding was also placed in the trap as nesting material.…”

“…Gastrointestinal (gut) parasite infections (helminth worms and coccidial protozoans) were identified to species, and burdens were measured (either fecal egg or oocyst counts (FEC/FOC), respectively) using salt flotation and microscopy. Infection with blood parasites (e.g., Bartonella spp., a flea‐transmitted bacterium, and Trypanosoma grosi , a flea‐transmitted protozoan) was identified using targeted, nested PCR assays on DNA extracted from blood (for more details on these methods see Knowles et al, ; Withenshaw et al, ). Our previous research on these wild rodent and parasite communities has shown that most parasites are host‐specific (Knowles et al, ; Withenshaw et al, ), therefore, we focused our analysis on the parasite communities in wood mice only.…”