Spatial, demographic, and phylogenetic patterns of Bartonella diversity in bats

Includes bibliographical references.2015 Summer.Much recent attention has focused on bats as potentially exceptional reservoirs of pathogens. Bats are known to carry zoonotic viruses deadly to humans with no apparent signs of pathology, however the evolutionary and physiological processes that are behind this ability remain largely unknown. Despite this uncertainty, bats’ long lifespans, deep evolutionary history, sociality, and migratory behavior make them a fascinating system in which to study patterns of diversity in viruses, bacteria, and other infectious organisms. This thesis explores ecological and evolutionary processes that structure the diversity of infectious bacteria in bats. I focus on Bartonella, a genus of vector-borne intracellular bacteria, because of its high prevalence and genetic diversity within bats. I examined the structure of Bartonella species assemblages in Eidolon spp. fruit bats across Africa and Madagascar using newly developed molecular and statistical tools. The results from this examination indicate that fruit bats from distant geographic locations host similar communities of Bartonella; I attribute this to widespread dispersal and communal roosting behavior in Eidolon spp. bats. To understand how Bartonella diversity has evolved and is structured geographically, I assembled a global dataset of Bartonella genotypes from bats and their ectoparasites. Using this dataset, I analyzed the contributions of cospeciation and sympatry among host species to the diversity of Bartonella in bats. Continued development of this research could provide a model system for the study of ecological and evolutionary processes contributing to pathogen diversification and infection dynamics in natural systems

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

Saccadic latency in amblyopia.

We measured saccadic latencies in a large sample (total n = 459) of individuals with amblyopia or risk factors for amblyopia, e.g., strabismus or anisometropia, and normal control subjects. We presented an easily visible target randomly to the left or right, 3.5° from fixation. The interocular difference in saccadic latency is highly correlated with the interocular difference in LogMAR (Snellen) acuity-as the acuity difference increases, so does the latency difference. Strabismic and strabismic-anisometropic amblyopes have, on average, a larger difference between their eyes in LogMAR acuity than anisometropic amblyopes and thus their interocular latency difference is, on average, significantly larger than anisometropic amblyopes. Despite its relation to LogMAR acuity, the longer latency in strabismic amblyopes cannot be attributed either to poor resolution or to reduced contrast sensitivity, because their interocular differences in grating acuity and in contrast sensitivity are roughly the same as for anisometropic amblyopes. The correlation between LogMAR acuity and saccadic latency arises because of the confluence of two separable effects in the strabismic amblyopic eye-poor letter recognition impairs LogMAR acuity while an intrinsic sluggishness delays reaction time. We speculate that the frequent microsaccades and the accompanying attentional shifts, made while strabismic amblyopes struggle to maintain fixation with their amblyopic eyes, result in all types of reactions being irreducibly delayed

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/

Why do some coronaviruses become pandemic threats when others do not?

Despite multiple spillover events and short chains of transmission on at least 4 continents, Middle East Respiratory Syndrome Coronavirus (MERS-CoV) has never triggered a pandemic. By contrast, its relative, Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has, despite apparently little, if any, previous circulation in humans. Resolving the unsolved mystery of the failure of MERS-CoV to trigger a pandemic could help inform how we understand the pandemic potential of pathogens, and probing it underscores a need for a more holistic understanding of the ways in which viral genetic changes scale up to population-level transmission

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

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

Author Correction: Ecology, evolution and spillover of coronaviruses from bats.

In the past two decades, three coronaviruses with ancestral origins in bats have emerged and caused widespread outbreaks in humans, including severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Since the first SARS epidemic in 2002–2003, the appreciation of bats as key hosts of zoonotic coronaviruses has advanced rapidly. More than 4,000 coronavirus sequences from 14 bat families have been identified, yet the true diversity of bat coronaviruses is probably much greater. Given that bats are the likely evolutionary source for several human coronaviruses, including strains that cause mild upper respiratory tract disease, their role in historic and future pandemics requires ongoing investigation. We review and integrate information on bat–coronavirus interactions at the molecular, tissue, host and population levels. We identify critical gaps in knowledge of bat coronaviruses, which relate to spillover and pandemic risk, including the pathways to zoonotic spillover, the infection dynamics within bat reservoir hosts, the role of prior adaptation in intermediate hosts for zoonotic transmission and the viral genotypes or traits that predict zoonotic capacity and pandemic potential. Filling these knowledge gaps may help prevent the next pandemic