Genetic diversity, infection prevalence, and possible transmission routes of Bartonella spp. in vampire bats

Bartonella spp. are globally distributed bacteria that cause endocarditis in humans and domestic animals. Recent work has suggested bats as zoonotic reservoirs of some human Bartonella infections; however, the ecological and spatiotemporal patterns of infection in bats remain largely unknown. Here we studied the genetic diversity, prevalence of infection across seasons and years, individual risk factors, and possible transmission routes of Bartonella in populations of common vampire bats (Desmodus rotundus) in Peru and Belize, for which high infection prevalence has previously been reported. Phylogenetic analysis of the gltA gene for a subset of PCR-positive blood samples revealed sequences that were related to Bartonella described from vampire bats from Mexico, other Neotropical bat species, and streblid bat flies. Sequences associated with vampire bats clustered significantly by country but commonly spanned Central and South America, implying limited spatial structure. Stable and nonzero Bartonella prevalence between years supported endemic transmission in all sites. The odds of Bartonella infection for individual bats was unrelated to the intensity of bat flies ectoparasitism, but nearly all infected bats were infested, which precluded conclusive assessment of support for vector-borne transmission. While metagenomic sequencing found no strong evidence of Bartonella DNA in pooled bat saliva and fecal samples, we detected PCR positivity in individual saliva and feces, suggesting the potential for bacterial transmission through both direct contact (i.e., biting) and environmental (i.e., fecal) exposures. Further investigating the relative contributions of direct contact, environmental, and vector-borne transmission for bat Bartonella is an important next step to predict infection dynamics within bats and the risks of human and livestock exposures

Host phylogeny, geographic overlap, and roost sharing shape parasite communities in European bats

How multitrophic relationships between wildlife communities and their ectoparasitic vectors interact to shape the diversity of vector-borne microorganisms is poorly understood. Nested levels of dependence among microbes, vectors, and vertebrate hosts may have complicated effects on both microbial community assembly and evolution. We examined Bartonella sequences from European bats and their ectoparasites with a combination of network analysis, Bayesian phylogenetics, tip-association and cophylogeny tests, and linear regression to understand the ecological and evolutionary processes that shape parasite communities. We detected seven batectoparasite-Bartonella communities that can be differentiated based on bat families and roosting patterns. Tips of the Bartonella tree were significantly clustered by host taxonomy and geography. We also found significant evidence of evolutionary congruence between bat host and Bartonella phylogenies, indicating that bacterial species have evolved to infect related bat species. Exploring these ecological and evolutionary associations further, we found that sharing of Bartonella species among bat hosts was strongly associated with host phylogenetic distance and roost sharing and less strongly with geographic range overlap. Ectoparasite sharing between hosts was strongly predicted by host phylogenetic distance, roost sharing, and geographic overlap but had no additive effect on Bartonella sharing. Finally, historical Bartonella host-switching was more frequent for closely related bats after accounting for sampling bias among bat species. This study helps to disentangle the complex ecology and evolution of Bartonella bacteria in bat species and their arthropod vectors. Our work provides insight into the important mechanisms that partition parasite communities among hosts, particularly the effect of host phylogeny and roost sharing, and could help to elucidate the evolutionary patterns of other diverse vector-borne microorganisms

Host phylogeny, geographic overlap, and roost sharing shape parasite communities in European bats

How multitrophic relationships between wildlife communities and their ectoparasitic vectors interact to shape the diversity of vector-borne microorganisms is poorly understood. Nested levels of dependence among microbes, vectors, and vertebrate hosts may have complicated effects on both microbial community assembly and evolution. We examined Bartonella sequences from European bats and their ectoparasites with a combination of network analysis, Bayesian phylogenetics, tip-association and cophylogeny tests, and linear regression to understand the ecological and evolutionary processes that shape parasite communities. We detected seven bat-ectoparasite-Bartonella communities that can be differentiated based on bat families and roosting patterns. Tips of the Bartonella tree were significantly clustered by host taxonomy and geography. We also found significant evidence of evolutionary congruence between bat host and Bartonella phylogenies, indicating that bacterial species have evolved to infect related bat species. Exploring these ecological and evolutionary associations further, we found that sharing of Bartonella species among bat hosts was strongly associated with host phylogenetic distance and roost sharing and less strongly with geographic range overlap. Ectoparasite sharing between hosts was strongly predicted by host phylogenetic distance, roost sharing, and geographic overlap but had no additive effect on Bartonella sharing. Finally, historical Bartonella host-switching was more frequent for closely related bats after accounting for sampling bias among bat species. This study helps to disentangle the complex ecology and evolution of Bartonella bacteria in bat species and their arthropod vectors. Our work provides insight into the important mechanisms that partition parasite communities among hosts, particularly the effect of host phylogeny and roost sharing, and could help to elucidate the evolutionary patterns of other diverse vector-borne microorganisms

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

How multitrophic relationships between wildlife communities and their ectoparasitic vectors interact to shape the diversity of vector-borne microorganisms is poorly understood. Nested levels of dependence among microbes, vectors, and vertebrate hosts may have complicated effects on both microbial community assembly and evolution. We examined Bartonella sequences from European bats and their ectoparasites with a combination of network analysis, Bayesian phylogenetics, tip-association and cophylogeny tests, and linear regression to understand the ecological and evolutionary processes that shape parasite communities. We detected seven bat–ectoparasite–Bartonella communities that can be differentiated based on bat families and roosting patterns. Tips of the Bartonella tree were significantly clustered by host taxonomy and geography. We also found significant evidence of evolutionary congruence between bat host and Bartonella phylogenies, indicating that bacterial species have evolved to infect related bat species. Exploring these ecological and evolutionary associations further, we found that sharing of Bartonella species among bat hosts was strongly associated with host phylogenetic distance and roost sharing and less strongly with geographic range overlap. Ectoparasite sharing between hosts was strongly predicted by host phylogenetic distance, roost sharing, and geographic overlap but had no additive effect on Bartonella sharing. Finally, historical Bartonella host-switching was more frequent for closely related bats after accounting for sampling bias among bat species. This study helps to disentangle the complex ecology and evolution of Bartonella bacteria in bat species and their arthropod vectors. Our work provides insight into the important mechanisms that partition parasite communities among hosts, particularly the effect of host phylogeny and roost sharing, and could help to elucidate the evolutionary patterns of other diverse vector-borne microorganisms

Novel hemotropic mycoplasmas are widespread and genetically diverse in vampire bats

Bats (Order: Chiroptera) have been widely studied as reservoir hosts for viruses of concern for human and animal health. However, whether bats are equally competent hosts of non-viral pathogens such as bacteria remains an important open question. Here, we surveyed blood and saliva samples of vampire bats from Peru and Belize for hemotropic Mycoplasma spp. (hemoplasmas), bacteria that can cause inapparent infection or anemia in hosts. 16S rRNA gene amplification of blood showed 67% (150/223) of common vampire bats (Desmodus rotundus) were infected by hemoplasmas. Sequencing of the 16S rRNA gene amplicons revealed three novel genotypes that were phylogenetically related but not identical to hemoplasmas described from other (non-vampire) bat species, rodents, humans, and non-human primates. Hemoplasma prevalence in vampire bats was highest in non-reproductive and young individuals, did not differ by country, and was relatively stable over time (i.e., endemic). Metagenomics from pooled D. rotundus saliva from Peru detected non-hemotropic Mycoplasma species and hemoplasma genotypes phylogenetically similar to those identified in blood, providing indirect evidence for potential direct transmission of hemoplasmas through biting or social contacts. This study demonstrates vampire bats host several novel hemoplasmas and sheds light on risk factors for infection and basic transmission routes. Given the high frequency of direct contacts that arise when vampire bats feed on humans, domestic animals, and wildlife, the potential of these bacteria to be transmitted between species should be investigated in future work

Livestock abundance predicts vampire bat demography, immune profiles, and bacterial infection risk

Human activities create novel food resources that can alter wildlife–pathogen interactions. If resources amplify or dampen, pathogen transmission probably depends on both host ecology and pathogen biology, but studies that measure responses to provisioning across both scales are rare. We tested these relationships with a 4-year study of 369 common vampire bats across 10 sites in Peru and Belize that differ in the abundance of livestock, an important anthropogenic food source. We quantified innate and adaptive immunity from bats and assessed infection with two common bacteria. We predicted that abundant livestock could reduce starvation and foraging effort, allowing for greater investments in immunity. Bats from high-livestock sites had higher microbicidal activity and proportions of neutrophils but lower immunoglobulin G and proportions of lymphocytes, suggesting more investment in innate relative to adaptive immunity and either greater chronic stress or pathogen exposure. This relationship was most pronounced in reproductive bats, which were also more common in high-livestock sites, suggesting feedbacks between demographic correlates of provisioning and immunity. Infection with both Bartonella and haemoplasmas were correlated with similar immune profiles, and both pathogens tended to be less prevalent in high-livestock sites, although effects were weaker for haemoplasmas. These differing responses to provisioning might therefore reflect distinct transmission processes. Predicting how provisioning alters host–pathogen interactions requires considering how both within-host processes and transmission modes respond to resource shifts

Evolutionary and ecological processes in microparasite communities of bats

2020 Spring.Includes bibliographical references.The majority of parasites infecting humans come from animals, so it is necessary to study how parasites are maintained in nature to understand which human populations are at risk of spillover. Parasites are also highly diverse in their own right, with their own fascinating ecology, so studying parasite communities will give us a full perspective of Earth's biodiversity. Research has shown that bats are significant hosts of parasites globally, including important pathogens of humans. The unique evolution of flight in bats has influenced their ability to disperse parasites, and may have modified their immune systems to be more tolerant of infections compared to other mammals. Thus, studying bat parasite communities could deepen our knowledge of the evolutionary history of mammalian parasites and the importance of flight in the maintenance of parasite community diversity in bats. In this dissertation, I focus on the evolutionary history and ecological forces affecting diversity in blood-borne microparasite communities of bats. There is a particular focus in this dissertation on Bartonella bacteria, a common parasite in mammals. To determine the importance of bats in the historical diversification of Bartonella bacteria, I performed the most comprehensive phylogenetic analysis of the genus to date, including data from 121 strains cultured from bats globally. I discovered that Bartonella bacteria began infecting mammals 62 million years ago and likely originated from bats. In a review of other bat parasites, including eukaryotic trypanosomes and haemosporidian parasites, I find that bats have had a similarly deep influence on the evolution of these taxa, and their historical spread across continents and to other mammalian hosts. To examine the importance of dispersal on parasite community diversity at smaller ecological scales, I focused on Bartonella communities in African fruit bats. I investigated differences in the Bartonella communities in fruit bat populations across a West African island chain. In addition, I examined the population genetics of bat flies, the presumed vectors of Bartonella in bats, and bat fly symbionts to compare with the genetic population structure of the bat hosts. Bartonella communities differed across islands and showed a pattern of isolation by geographic distance, indicating that dispersal of parasite species is constrained by bat movement patterns. Population structure was reduced in bat flies and symbionts compared to that of the bat hosts, suggesting that bat movements between islands are going undetected from population genetics of the hosts alone. Finally, I investigated Bartonella community dynamics in a captive colony of fruit bats in Ghana over a sampling period of three years. In this study, the population density of bat flies declined over time and was then restored via reintroduction of flies from a wild source population, causing predictable changes in Bartonella prevalence within the bat colony. These results provide the first experimental confirmation of bat flies as vectors of Bartonella in bats. In addition, changes in Bartonella diversity within the colony that occurred in the absence of bat flies might be attributed to ecological drift and selection through interspecies competition mediated by the host immune system. These projects highlight the ecological and evolutionary processes affecting microparasite communities of bats, providing useful information for understanding how parasite biodiversity is created and maintained in natural populations

Trends in Bacterial Pathogens of Bats:Global Distribution and Knowledge Gaps

Bats have received considerable recent attention for infectious disease research because of their potential to host and transmit viruses, including Ebola, Hendra, Nipah, and multiple coronaviruses. These pathogens are occasionally transmitted from bats to wildlife, livestock, and to humans, directly or through other bridging (intermediate) hosts. Due to their public health relevance, zoonotic viruses are a primary focus of research attention. In contrast, other emerging pathogens of bats, such as bacteria, are vastly understudied despite their ubiquity and diversity. Here, we describe the currently known host ranges and geographic distributional patterns of potentially zoonotic bacterial genera in bats, using published presence-absence data of pathogen occurrence. We identify apparent gaps in our understanding of the distribution of these pathogens on a global scale. The most frequently detected bacterial genera in bats are Bartonella, Leptospira, and Mycoplasma. However, a wide variety of other potentially zoonotic bacterial genera are also occasionally found in bats, such as Anaplasma, Brucella, Borrelia, Coxiella, Ehrlichia, Francisella, Neorickettsia, and Rickettsia. The bat families Phyllostomidae, Vespertilionidae, and Pteropodidae are most frequently reported as hosts of bacterial pathogens; however, the presence of at least one bacterial genus was confirmed in all 15 bat families tested. On a spatial scale, molecular diagnostics of samples from 58 countries and four overseas departments and island states (French Guiana, Mayotte, New Caledonia, and Réunion Island) reported testing for at least one bacterial pathogen in bats. We also identified geographical areas that have been mostly neglected during bacterial pathogen research in bats, such as the Afrotropical region and Southern Asia. Current knowledge on the distribution of potentially zoonotic bacterial genera in bats is strongly biased by research effort towards certain taxonomic groups and geographic regions. Identifying these biases can guide future surveillance efforts, contributing to a better understanding of the ecoepidemiology of zoonotic pathogens in bats.<br/

Bartonella DNA in heart tissues of bats in central and eastern Europe and a review of phylogenetic relations of bat-associated bartonellae

Background: Bats are among the most widely distributed mammals worldwide and can represent hosts or reservoirs for a number of different pathogens. Bartonella spp. are opportunistic bacterial pathogens, which are transmitted by a large variety of arthropods. The aim of this study was to investigate the presence and host-associations of these Gram-negative bacteria in heart tissues of bats collected in four different countries from eastern and central Europe and to analyze their phylogenetic relationship with other bat-associated bartonellae. Results: The results of this study show for the first time the presence of Bartonella spp. DNA in heart tissues of bats from central and eastern Europe. The overall prevalence of the infection was 1.38%. Phylogenetic analysis identified four new Bartonella spp. sequences, which were closely related with other Bartonella previously isolated from bats in Europe and North America. Conclusions: The gltA sequences of Bartonella spp. showed considerable heterogeneity in the phylogenetic analysis resulting in six different clades. Our study demonstrated the presence of Bartonella spp. only in heart tissues of bats from Romania, with two new bat species recorded as hosts (Myotis cf. alcathoe and Pipistrellus pipistrellus