Publications by authors named "Fiona A Stewart"

75 Publications

CD4 receptor diversity represents an ancient protection mechanism against primate lentiviruses.

Proc Natl Acad Sci U S A 2021 Mar;118(13)

Lukuru Wildlife Research Foundation, Tshuapa-Lomami-Lualaba Project, BP 2012, Kinshasa, Democratic Republic of the Congo.

Infection with human and simian immunodeficiency viruses (HIV/SIV) requires binding of the viral envelope glycoprotein (Env) to the host protein CD4 on the surface of immune cells. Although invariant in humans, the Env binding domain of the chimpanzee CD4 is highly polymorphic, with nine coding variants circulating in wild populations. Here, we show that within-species CD4 diversity is not unique to chimpanzees but found in many African primate species. Characterizing the outermost (D1) domain of the CD4 protein in over 500 monkeys and apes, we found polymorphic residues in 24 of 29 primate species, with as many as 11 different coding variants identified within a single species. D1 domain amino acid replacements affected SIV Env-mediated cell entry in a single-round infection assay, restricting infection in a strain- and allele-specific fashion. Several identical CD4 polymorphisms, including the addition of -linked glycosylation sites, were found in primate species from different genera, providing striking examples of parallel evolution. Moreover, seven different guenons ( spp.) shared multiple distinct D1 domain variants, pointing to long-term trans-specific polymorphism. These data indicate that the HIV/SIV Env binding region of the primate CD4 protein is highly variable, both within and between species, and suggest that this diversity has been maintained by balancing selection for millions of years, at least in part to confer protection against primate lentiviruses. Although long-term SIV-infected species have evolved specific mechanisms to avoid disease progression, primate lentiviruses are intrinsically pathogenic and have left their mark on the host genome.
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http://dx.doi.org/10.1073/pnas.2025914118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8020793PMC
March 2021

Visualization of endogenous gut bacteria in Drosophila melanogaster using fluorescence in situ hybridization.

PLoS One 2021 19;16(2):e0247376. Epub 2021 Feb 19.

Institut für Mathematische Modellierung Biologischer Systeme, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany.

All metazoans are colonized by a complex and diverse set of microorganisms. The microbes colonize all parts of the body and are especially abundant in the gastrointestinal tract, where they constitute the gut microbiome. The fruit fly Drosophila melanogaster turned out to be an exquisite model organism to functionally test the importance of an intact gut microbiome. Still, however, fundamental questions remain unanswered. For example, it is unknown whether a fine-tuned regionalization of the gut microbiome exists and how such a spatial organization could be established. In order to pave the way for answering this question, we generated an optimized and adapted fluorescence in situ hybridization (FISH) protocol. We focused on the detection of the two major Drosophila gut microbiome constituting bacteria genera: Acetobacter and Lactobacillus. FISH allows to detect the bacteria in situ and thus to investigate their spatial localization in respect to the host as well as to other microbiome members. We demonstrate the applicability of the protocol using a diverse set of sample types.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0247376PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7894962PMC
February 2021

Ecological correlates of chimpanzee (Pan troglodytes schweinfurthii) density in Mahale Mountains National Park, Tanzania.

PLoS One 2021 12;16(2):e0246628. Epub 2021 Feb 12.

Department of Anthropology, University College London, London, United Kingdom.

Understanding the ecological factors that drive animal density patterns in time and space is key to devising effective conservation strategies. In Tanzania, most chimpanzees (~75%) live outside national parks where human activities threaten their habitat's integrity and connectivity. Mahale Mountains National Park (MMNP), therefore, is a critical area for chimpanzees (Pan troglodytes schweinfurthii) in the region due to its location and protective status. Yet, despite its importance and long history of chimpanzee research (>50 years), a park-wide census of the species has never been conducted. The park is categorized as a savanna-woodland mosaic, interspersed with riparian forest, wooded grassland, and bamboo thicket. This heterogeneous landscape offers an excellent opportunity to assess the ecological characteristics associated with chimpanzee density, a topic still disputed, which could improve conservation plans that protect crucial chimpanzee habitat outside the park. We examined the influence of fine-scale vegetative characteristics and topographical features on chimpanzee nest density, modeling nest counts using hierarchical distance sampling. We counted 335 nests in forest and woodland habitats across 102 transects in 13 survey sites. Nests were disproportionately found more in or near evergreen forests, on steep slopes, and in feeding tree species. We calculated chimpanzee density in MMNP to be 0.23 ind/km2, although density varied substantially among sites (0.09-3.43 ind/km2). Density was associated with factors related to the availability of food and nesting trees, with topographic heterogeneity and the total basal area of feeding tree species identified as significant positive predictors. Species-rich habitats and floristic diversity likely play a principal role in shaping chimpanzee density within a predominately open landscape with low food abundance. Our results provide valuable baseline data for future monitoring efforts in MMNP and enhance our understanding of this endangered species' density and distribution across Tanzania.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0246628PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7880473PMC
February 2021

Red-tailed monkeys (Cercopithecus ascanius) prey upon and mob birds in the Issa Valley, western Tanzania.

Primates 2020 Jul 12;61(4):563-566. Epub 2020 Jun 12.

Greater Mahale Ecosystem Research and Conservation Project, Box 66, Kigoma, Tanzania.

Interactions between monkeys and birds are rarely observed and, consequently, rarely described in the scientific literature. We recorded two encounters between birds (Prionops plumatus and Strix woodfordii) and red-tailed monkeys (Cercopithecus ascanius) in a woodland-mosaic habitat in western Tanzania. We observed a male red-tailed monkey consume a small bird in its entirety. Although only a few feathers remained, we provisionally identified the bird as a white-crested helmetshrike. We also observed a group of red-tailed monkeys mobbing, but not killing, an African wood owl on the forest floor. This is the first reported observation of this kind. These encounters suggest that guenons may generalize large-bodied avians as threats and small-bodied avians as potential prey. Hetero-specific encounters such as these provide insights into primate diet and anti-predatory behavior.
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http://dx.doi.org/10.1007/s10329-020-00834-1DOI Listing
July 2020

Chimpanzee ethnography reveals unexpected cultural diversity.

Nat Hum Behav 2020 09 25;4(9):910-916. Epub 2020 May 25.

School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK.

Human ethnographic knowledge covers hundreds of societies, whereas chimpanzee ethnography encompasses at most 15 communities. Using termite fishing as a window into the richness of chimpanzee cultural diversity, we address a potential sampling bias with 39 additional communities across Africa. Previously, termite fishing was known from eight locations with two distinguishable techniques observed in only two communities. Here, we add nine termite-fishing communities not studied before, revealing 38 different technical elements, as well as community-specific combinations of three to seven elements. Thirty of those were not ecologically constrained, permitting the investigation of chimpanzee termite-fishing culture. The number and combination of elements shared among individuals were more similar within communities than between them, thus supporting community-majority conformity via social imitation. The variation in community-specific combinations of elements parallels cultural diversity in human greeting norms or chopstick etiquette. We suggest that termite fishing in wild chimpanzees shows some elements of cumulative cultural diversity.
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http://dx.doi.org/10.1038/s41562-020-0890-1DOI Listing
September 2020

Strain diversity of Treponema pallidum subsp. pertenue suggests rare interspecies transmission in African nonhuman primates.

Sci Rep 2019 10 2;9(1):14243. Epub 2019 Oct 2.

Work Group Neglected Tropical Diseases, Infection Biology Unit, German Primate Center, Leibniz Institute for Primate Research, Goettingen, Germany.

In our most recent study, we found that in Tanzania infection with Treponema pallidum (TP) subsp. pertenue (TPE) is present in four different monkey species. In order to gain information on the diversity and epidemiological spread of the infection in Tanzanian nonhuman primates (NHP), we identified two suitable candidate genes for multi-locus sequence typing (MLST). We demonstrate the functionality of the MLST system in invasively and non-invasively collected samples. While we were not able to demonstrate frequent interspecies transmission of TPE in Tanzanian monkeys, our results show a clustering of TPE strains according to geography and not host species, which is suggestive for rare transmission events between different NHP species. In addition to the geographic stability, we describe the relative temporal stability of the strains infecting NHPs and identified multi-strain infection. Differences between TPE strains of NHP and human origin are highlighted. Our results show that antibiotic resistance does not occur in Tanzanian TPE strains of NHP origin.
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http://dx.doi.org/10.1038/s41598-019-50779-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6775232PMC
October 2019

Food abundance and weather influence habitat-specific ranging patterns in forest- and savanna mosaic-dwelling red-tailed monkeys (Cercopithecus ascanius).

Am J Phys Anthropol 2019 10 19;170(2):217-231. Epub 2019 Aug 19.

School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, United Kingdom.

Objectives: Primates that live in predominantly forested habitats and open, savanna mosaics should exhibit behavioral responses to differing food distributions and weather. We compared ecological constraints on red-tailed monkey ranging behavior in forest and savanna mosaic environments. Intraspecific variation in adaptations to these conditions may reflect similar pressures faced by hominins during the Plio-Pleistocene.

Methods: We followed six groups in moist evergreen forest at Ngogo (Uganda) and one group in a savanna-woodland mosaic at the Issa Valley (Tanzania). We used spatial analyses to compare home range sizes and daily travel distances (DTD) between sites. We used measures of vegetation density and phenology to interpolate spatially explicit indices of food (fruit, flower, and leaves) abundance. We modeled DTD and range use against food abundance. We modeled DTD and at Issa hourly travel distances (HTD), against temperature and rainfall.

Results: Compared to Issa, monkeys at Ngogo exhibited significantly smaller home ranges and less variation in DTD. DTD related negatively to fruit abundance, which had a stronger effect at Issa. DTD and HTD related negatively to temperature but not rainfall. This effect did not differ significantly between sites. Home range use did not relate to food abundance at either site.

Conclusions: Our results indicate food availability and thermoregulatory constraints influence red-tailed monkey ranging patterns. Intraspecific variation in home range sizes and DTD likely reflects different food distributions in closed and open habitats. We compare our results with hypotheses of evolved hominin behavior associated with the Plio-Pleistocene shift from similar closed to open environments.
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http://dx.doi.org/10.1002/ajpa.23920DOI Listing
October 2019

Control of Drosophila Growth and Survival by the Lipid Droplet-Associated Protein CG9186/Sturkopf.

Cell Rep 2019 03;26(13):3726-3740.e7

Institute for Mathematical Modeling of Biological Systems, Heinrich Heine University Düsseldorf, 40225 Düsseldorf, Germany; Systems Biology of Lipid Metabolism, Heinrich Heine University Düsseldorf, 40225 Düsseldorf, Germany. Electronic address:

Lipid droplets (LDs) are the universal cellular storage organelles for esterified neutral lipids. The increasing number of characterized LD-associated proteins attained LDs with hitherto unexpected functions on top of their classical role as energy depot. Here, we characterize the LD-associated protein CG9186 of Drosophila by a CRISPR/Cas9-derived mutant fly line. While the mutant flies only showed a mild triacylglycerol storage phenotype, they were highly protected from desiccation stress, likely linked to a reduced locomotor activity and altered cuticular hydrocarbons. Both parameters depend on juvenile hormone (JH) signaling. Together with an observed interaction between CG9186 and JH-degrading enzymes, our results suggest that CG9186 participates in endocrine physiology regulation. In support of this hypothesis, CG9186 mutant flies show an altered expression of JH target genes and fail to adjust their developmental rate to dietary yeast-to-sugar ratio changes. Our results thus link LDs to organismic physiology regulation.
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http://dx.doi.org/10.1016/j.celrep.2019.02.110DOI Listing
March 2019

CD4 receptor diversity in chimpanzees protects against SIV infection.

Proc Natl Acad Sci U S A 2019 02 4;116(8):3229-3238. Epub 2019 Feb 4.

Sanaga-Yong Chimpanzee Rescue Center, In Defense of Animals-Africa, Portland, OR 97204.

Human and simian immunodeficiency viruses (HIV/SIVs) use CD4 as the primary receptor to enter target cells. Here, we show that the chimpanzee CD4 is highly polymorphic, with nine coding variants present in wild populations, and that this diversity interferes with SIV envelope (Env)-CD4 interactions. Testing the replication fitness of SIVcpz strains in CD4 T cells from captive chimpanzees, we found that certain viruses were unable to infect cells from certain hosts. These differences were recapitulated in CD4 transfection assays, which revealed a strong association between CD4 genotypes and SIVcpz infection phenotypes. The most striking differences were observed for three substitutions (Q25R, Q40R, and P68T), with P68T generating a second N-linked glycosylation site (N66) in addition to an invariant N32 encoded by all chimpanzee CD4 alleles. In silico modeling and site-directed mutagenesis identified charged residues at the CD4-Env interface and clashes between CD4- and Env-encoded glycans as mechanisms of inhibition. CD4 polymorphisms also reduced Env-mediated cell entry of monkey SIVs, which was dependent on at least one D1 domain glycan. CD4 allele frequencies varied among wild chimpanzees, with high diversity in all but the western subspecies, which appeared to have undergone a selective sweep. One allele was associated with lower SIVcpz prevalence rates in the wild. These results indicate that substitutions in the D1 domain of the chimpanzee CD4 can prevent SIV cell entry. Although some SIVcpz strains have adapted to utilize these variants, CD4 diversity is maintained, protecting chimpanzees against infection with SIVcpz and other SIVs to which they are exposed.
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http://dx.doi.org/10.1073/pnas.1821197116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6386711PMC
February 2019

Leopard (Panthera pardus) predation on a red-tailed monkey (Cercopithecus ascanius) in the Issa Valley, western Tanzania.

Primates 2019 Jan 17;60(1):15-19. Epub 2018 Nov 17.

School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool, L33AF, UK.

Predation is predicted to be an important selection pressure for primates. Evidence for this hypothesis is rare, however, due to the scarcity of direct observations of primate predation. We describe an observation of leopard (Panthera pardus) predation on a red-tailed monkey (Cercopithecus ascanius schmidti) at the Issa Valley, a savanna-woodland mosaic landscape in western Tanzania. We compare rates of evidence of leopard presence between Issa and other primate study sites in sub-Saharan Africa. An increase in direct observations of leopards at Issa in recent years suggests that leopards may be habituating to researcher presence.
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http://dx.doi.org/10.1007/s10329-018-0700-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6331503PMC
January 2019

PARV4 found in wild chimpanzee faeces: an alternate route of transmission?

Arch Virol 2019 Feb 20;164(2):573-578. Epub 2018 Oct 20.

CEITEC-VFU, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 612 42, Brno, Czech Republic.

Human parvovirus 4 (PARV4, family Parvoviridae, genus Tetraparvovirus) displays puzzling features, such as uncertain clinical importance/significance, unclear routes of transmission, and discontinuous geographical distribution. The origin, or the general reservoir, of human PARV4 infection is unknown. We aimed to detect and characterize PARV4 virus in faecal samples collected from two wild chimpanzee populations and 19 species of captive non-human primates. We aimed to investigate these species as a potential reservoir and alternate route of transmission on the African continent. From almost 500 samples screened, a single wild Pan troglodytes schweinfurthii sample tested positive. Full genome analysis, as well as single ORF phylogenies, confirmed species-specific PARV4 infection.
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http://dx.doi.org/10.1007/s00705-018-4073-6DOI Listing
February 2019

Food mechanical properties and isotopic signatures in forest versus savannah dwelling eastern chimpanzees.

Commun Biol 2018 10;1:109. Epub 2018 Aug 10.

Max Planck Weizmann Center for Integrative Archaeology and Anthropology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany.

Chimpanzees are traditionally described as ripe fruit specialists with large incisors but relatively small postcanine teeth, adhering to a somewhat narrow dietary niche. Field observations and isotopic analyses suggest that environmental conditions greatly affect habitat resource utilisation by chimpanzee populations. Here we combine measures of dietary mechanics with stable isotope signatures from eastern chimpanzees living in tropical forest (Ngogo, Uganda) and savannah woodland (Issa Valley, Tanzania). We show that foods at Issa can present a considerable mechanical challenge, most saliently in the external tissues of savannah woodland plants compared to their tropical forest equivalents. This pattern is concurrent with different isotopic signatures between sites. These findings demonstrate that chimpanzee foods in some habitats are mechanically more demanding than previously thought, elucidating the broader evolutionary constraints acting on chimpanzee dental morphology. Similarly, these data can help clarify the dietary mechanical landscape of extinct hominins often overlooked by broad C3/C4 isotopic categories.
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http://dx.doi.org/10.1038/s42003-018-0115-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6123729PMC
August 2018

CHIIMP: An automated high-throughput microsatellite genotyping platform reveals greater allelic diversity in wild chimpanzees.

Ecol Evol 2018 Aug 16;8(16):7946-7963. Epub 2018 Jul 16.

Departments of Microbiology and Medicine Perelman School of Medicine University of Pennsylvania Philadelphia Pennsylvania.

Short tandem repeats (STRs), also known as microsatellites, are commonly used to noninvasively genotype wild-living endangered species, including African apes. Until recently, capillary electrophoresis has been the method of choice to determine the length of polymorphic STR loci. However, this technique is labor intensive, difficult to compare across platforms, and notoriously imprecise. Here we developed a MiSeq-based approach and tested its performance using previously genotyped fecal samples from long-term studied chimpanzees in Gombe National Park, Tanzania. Using data from eight microsatellite loci as a reference, we designed a bioinformatics platform that converts raw MiSeq reads into locus-specific files and automatically calls alleles after filtering stutter sequences and other PCR artifacts. Applying this method to the entire Gombe population, we confirmed previously reported genotypes, but also identified 31 new alleles that had been missed due to sequence differences and size homoplasy. The new genotypes, which increased the allelic diversity and heterozygosity in Gombe by 61% and 8%, respectively, were validated by replicate amplification and pedigree analyses. This demonstrated inheritance and resolved one case of an ambiguous paternity. Using both singleplex and multiplex locus amplification, we also genotyped fecal samples from chimpanzees in the Greater Mahale Ecosystem in Tanzania, demonstrating the utility of the MiSeq-based approach for genotyping nonhabituated populations and performing comparative analyses across field sites. The new automated high-throughput analysis platform (available at https://github.com/ShawHahnLab/chiimp) will allow biologists to more accurately and effectively determine wildlife population size and structure, and thus obtain information critical for conservation efforts.
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http://dx.doi.org/10.1002/ece3.4302DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6145012PMC
August 2018

Savanna chimpanzees adjust sleeping nest architecture in response to local weather conditions.

Am J Phys Anthropol 2018 07;166(3):549-562

Department of Anthropology, Iowa State University, Ames, Iowa 50011.

Objectives: Great ape nests are hypothesized to aid safe, secure sleep via providing thermoregulation or protection from predators and vectors. We aimed to describe and investigate variation in chimpanzee nest architecture across two populations in response to local weather conditions.

Materials And Methods: We experimentally tested whether nests provide insulation by measuring heat loss within and outside nests, and took detailed measurements of the number, size, and type of materials used in nest building across two dry-habitat research sites (Fongoli, Senegal, and Issa, Tanzania). We tested application of principal components analysis (PCA) to extract composite quantitative measures of the key components of shape and architecture, before testing how PCs vary across populations with overnight weather conditions that reflect hypothesized thermoregulatory function.

Results: Heat loss is greater and occurs faster outside of nests. PCA allowed meaningful comparison of nests within and between sites. Nest variation at both sites revealed chimpanzees built thicker nests in cooler conditions and used more broken branches and support in moister conditions. Chimpanzees in Fongoli used more lining and mattress material in colder conditions, whilst in Issa nest depth and support branch size were larger in windier conditions.

Discussion: Shape and architectural measures reflected insulation and stability of nest structure. Chimpanzees in Fongoli and Issa may achieve the same functional goals by adjusting nest shape and architecture in different ways. These results suggest that wild chimpanzees show flexible building techniques in response to local, overnight weather conditions in making an insulating and stable, supportive platform for sleep.
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http://dx.doi.org/10.1002/ajpa.23461DOI Listing
July 2018

Ecology of sleeping: the microbial and arthropod associates of chimpanzee beds.

R Soc Open Sci 2018 May 16;5(5):180382. Epub 2018 May 16.

Department of Applied Ecology and Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, USA.

The indoor environment created by the construction of homes and other buildings is often considered to be uniquely different from other environments. It is composed of organisms that are less diverse than those of the outdoors and strongly sourced by, or dependent upon, human bodies. Yet, no one has ever compared the composition of species found in contemporary human homes to that of other structures built by mammals, including those of non-human primates. Here we consider the microbes and arthropods found in chimpanzee beds, relative to the surrounding environment ( = 41 and 15 beds, respectively). Based on the study of human homes, we hypothesized that the microbes found in chimpanzee beds would be less diverse than those on nearby branches and leaves and that their beds would be primarily composed of body-associated organisms. However, we found that differences between wet and dry seasons and elevation above sea level explained nearly all of the observed variation in microbial diversity and community structure. While we can identify the presence of a chimpanzee based on the assemblage of bacteria, the dominant signal is that of environmental microbes. We found just four ectoparasitic arthropod specimens, none of which appears to be specialized on chimpanzees or their structures. These results suggest that the life to which chimpanzees are exposed while in their beds is predominately the same as that of the surrounding environment.
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http://dx.doi.org/10.1098/rsos.180382DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5990838PMC
May 2018

Widespread Treponema pallidum Infection in Nonhuman Primates, Tanzania.

Emerg Infect Dis 2018 06;24(6):1002-1009

We investigated Treponema pallidum infection in 8 nonhuman primate species (289 animals) in Tanzania during 2015-2017. We used a serologic treponemal test to detect antibodies against the bacterium. Infection was further confirmed from tissue samples of skin-ulcerated animals by 3 independent PCRs (polA, tp47, and TP_0619). Our findings indicate that T. pallidum infection is geographically widespread in Tanzania and occurs in several species (olive baboons, yellow baboons, vervet monkeys, and blue monkeys). We found the bacterium at 11 of 14 investigated geographic locations. Anogenital ulceration was the most common clinical manifestation; orofacial lesions also were observed. Molecular data show that nonhuman primates in Tanzania are most likely infected with T. pallidum subsp. pertenue-like strains, which could have implications for human yaws eradication.
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http://dx.doi.org/10.3201/eid2406.180037DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6004850PMC
June 2018

The impact of genome variation and diet on the metabolic phenotype and microbiome composition of Drosophila melanogaster.

Sci Rep 2018 04 18;8(1):6215. Epub 2018 Apr 18.

Institute for Mathematical Modeling of Biological Systems, Heinrich Heine University, Duesseldorf, Germany.

The metabolic phenotype of an organism depends on a complex regulatory network, which integrates the plethora of intrinsic and external information and prioritizes the flow of nutrients accordingly. Given the rise of metabolic disorders including obesity, a detailed understanding of this regulatory network is in urgent need. Yet, our level of understanding is far from completeness and complicated by the discovery of additional layers in metabolic regulation, such as the impact of the microbial community present in the gut on the hosts' energy storage levels. Here, we investigate the interplay between genome variation, diet and the gut microbiome in the shaping of a metabolic phenotype. For this purpose, we reared a set of fully sequenced wild type Drosophila melanogaster flies under basal and nutritionally challenged conditions and performed metabolic and microbiome profiling experiments. Our results introduce the fly as a model system to investigate the impact of genome variation on the metabolic response to diet alterations and reveal candidate single nucleotide polymorphisms associated with different metabolic traits, as well as metabolite-metabolite and metabolite-microbe correlations. Intriguingly, the dietary changes affected the microbiome composition less than anticipated. These results challenge the current view of a rapidly changing microbiome in response to environmental fluctuations.
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http://dx.doi.org/10.1038/s41598-018-24542-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5906449PMC
April 2018

Allometry and Ecology of the Bilaterian Gut Microbiome.

mBio 2018 03 27;9(2). Epub 2018 Mar 27.

Division of Gastroenterology, Hepatology, and Nutrition, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.

Classical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed. Here, we investigated the influence of several well-known ecological principles on animal-associated microbiota by characterizing gut microbial specimens from bilaterally symmetrical animals () ranging from flies to whales. A rigorously vetted sample set containing 265 specimens from 64 species was assembled. Bacterial lineages were characterized by 16S rRNA gene sequencing. Previously published samples were also compared, allowing analysis of over 1,098 samples in total. A restricted number of bacterial phyla was found to account for the great majority of gut colonists. Gut microbial composition was associated with host phylogeny and diet. We identified numerous gut bacterial 16S rRNA gene sequences that diverged deeply from previously studied taxa, identifying opportunities to discover new bacterial types. The number of bacterial lineages per gut sample was positively associated with animal mass, paralleling known species-area relationships from island biogeography and implicating body size as a determinant of community stability and niche complexity. Samples from larger animals harbored greater numbers of anaerobic communities, specifying a mechanism for generating more-complex microbial environments. Predictions for species/abundance relationships from models of neutral colonization did not match the data set, pointing to alternative mechanisms such as selection of specific colonists by environmental niche. Taken together, the data suggest that niche complexity increases with gut size and that niche selection forces dominate gut community construction. The intestinal microbiome of animals is essential for health, contributing to digestion of foods, proper immune development, inhibition of pathogen colonization, and catabolism of xenobiotic compounds. How these communities assemble and persist is just beginning to be investigated. Here we interrogated a set of gut samples from a wide range of animals to investigate the roles of selection and random processes in microbial community construction. We show that the numbers of bacterial species increased with the weight of host organisms, paralleling findings from studies of island biogeography. Communities in larger organisms tended to be more anaerobic, suggesting one mechanism for niche diversification. Nonselective processes enable specific predictions for community structure, but our samples did not match the predictions of the neutral model. Thus, these findings highlight the importance of niche selection in community construction and suggest mechanisms of niche diversification.
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http://dx.doi.org/10.1128/mBio.00319-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5874926PMC
March 2018

DNA recovery from wild chimpanzee tools.

PLoS One 2018 3;13(1):e0189657. Epub 2018 Jan 3.

Primate Archaeology Research Group, University of Oxford, Oxford, United Kingdom.

Most of our knowledge of wild chimpanzee behaviour stems from fewer than 10 long-term field sites. This bias limits studies to a potentially unrepresentative set of communities known to show great behavioural diversity on small geographic scales. Here, we introduce a new genetic approach to bridge the gap between behavioural material evidence in unhabituated chimpanzees and genetic advances in the field of primatology. The use of DNA analyses has revolutionised archaeological and primatological fields, whereby extraction of DNA from non-invasively collected samples allows researchers to reconstruct behaviour without ever directly observing individuals. We used commercially available forensic DNA kits to show that termite-fishing by wild chimpanzees (Pan troglodytes schweinfurthii) leaves behind detectable chimpanzee DNA evidence on tools. We then quantified the recovered DNA, compared the yield to that from faecal samples, and performed an initial assessment of mitochondrial and microsatellite markers to identify individuals. From 49 termite-fishing tools from the Issa Valley research site in western Tanzania, we recovered an average of 52 pg/μl chimpanzee DNA, compared to 376.2 pg/μl in faecal DNA extracts. Mitochondrial DNA haplotypes could be assigned to 41 of 49 tools (84%). Twenty-six tool DNA extracts yielded >25 pg/μl DNA and were selected for microsatellite analyses; genotypes were determined with confidence for 18 tools. These tools were used by a minimum of 11 individuals across the study period and termite mounds. These results demonstrate the utility of bio-molecular techniques and a primate archaeology approach in non-invasive monitoring and behavioural reconstruction of unhabituated primate populations.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0189657PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5751987PMC
February 2018

Modifiers of radiation effects in the eye.

Life Sci Space Res (Amst) 2017 Nov 18;15:43-54. Epub 2017 Jul 18.

Center for Radiological Research, Columbia University, College of Physicians and Surgeons, 630 W. 168th St., New York, NY 10032, USA.

World events, including the threat of radiological terrorism and the fear of nuclear accidents, have highlighted an urgent need to develop medical countermeasures to prevent or reduce radiation injury. Similarly, plans for manned spaceflight to a near-Earth asteroid or journey to Mars raise serious concerns about long-term effects of space radiation on human health and the availability of suitable therapeutic interventions. At the same time, the need to protect normal tissue from the deleterious effects of radiotherapy has driven considerable research into the design of effective radioprotectors. For more than 70 years, animal models of radiation cataract have been utilized to test the short and long-term efficacy of various radiation countermeasures. While some compounds, most notably the Walter Reed (WR) class of radioprotectors, have reported limited effectiveness when given before exposure to low-LET radiation, the human toxicity of these molecules at effective doses limits their usefulness. Furthermore, while there has been considerable testing of eye responses to X- and gamma irradiation, there is limited information about using such models to limit the injurious effects of heavy ions and neutrons on eye tissue. A new class of radioprotector molecules, including the sulfhydryl compound PrC-210, are reported to be effective at much lower doses and with far less side effects. Their ability to modify ocular radiation damage has not yet been examined. The ability to non-invasively measure sensitive, radiation-induced ocular changes over long periods of time makes eye models an attractive option to test the radioprotective and radiation mitigating abilities of new novel compounds.
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http://dx.doi.org/10.1016/j.lssr.2017.07.005DOI Listing
November 2017

The diet of open-habitat chimpanzees (Pan troglodytes schweinfurthii) in the Issa valley, western Tanzania.

J Hum Evol 2017 11 3;112:57-69. Epub 2017 Oct 3.

School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, United Kingdom; Ugalla Primate Project, Box 108, Uvinza, Tanzania; Department of Archaeology and Anthropology, University of Cambridge, United Kingdom.

Comparative data on the diets of extant primates inform hypotheses about hominin resource use. Historically, data describing chimpanzee diets stem primarily from forest-dwelling communities, and we lack comparative data from chimpanzees that live in mosaic habitats that more closely resemble those reconstructed for Plio-Pleistocene hominins. We present data on the diet of a partially-habituated community of open habitat chimpanzees (Pan troglodytes schweinfurthii) from the Issa valley, western Tanzania, collected over a four-year period. Based mostly on macroscopic faecal analysis, Issa chimpanzees consumed a minimum of 69 plant species. There was no relationship between plant consumption and either fruit availability or feeding tree density; the most frequently consumed plant species were found in riverine forests, with woodland species consumed more frequently during the late dry season. We conclude by contextualising these findings with those of other open-habitat chimpanzee sites, and also by discussing how our results contribute towards reconstructions of early hominin exploitation of mosaic landscapes.
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http://dx.doi.org/10.1016/j.jhevol.2017.08.016DOI Listing
November 2017

Adenovirus infection in savanna chimpanzees (Pan troglodytes schweinfurthii) in the Issa Valley, Tanzania.

Arch Virol 2018 Jan 4;163(1):191-196. Epub 2017 Oct 4.

CEITEC-VFU, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 612 42, Brno, Czech Republic.

Adenoviruses are a widespread cause of diverse human infections with recently confirmed zoonotic roots in African great apes. We focused on savanna-dwelling chimpanzees in the Issa Valley (Tanzania), which differ from those from forested sites in many aspects of behavior and ecology. PCR targeting the DNA polymerase gene detected AdV in 36.7% (69/188) of fecal samples. We detected five groups of strains belonging to the species Human mastadenovirus E and two distinct groups within the species Human mastadenovirus C based on partial hexon sequence. All detected AdVs from the Issa Valley are related to those from nearby Mahale and Gombe National Parks, suggesting chimpanzee movements and pathogen transmission.
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http://dx.doi.org/10.1007/s00705-017-3576-xDOI Listing
January 2018

How radiation influences atherosclerotic plaque development: a biophysical approach in ApoE⁻/⁻ mice.

Radiat Environ Biophys 2017 11 2;56(4):423-431. Epub 2017 Sep 2.

Centre for Environmental Safety and Security, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Atherosclerosis is the development of lipid-laden plaques in arteries and is nowadays considered as an inflammatory disease. It has been shown that high doses of ionizing radiation, as used in radiotherapy, can increase the risk of development or progression of atherosclerosis. To elucidate the effects of radiation on atherosclerosis, we propose a mathematical model to describe radiation-promoted plaque development. This model distinguishes itself from other models by combining plaque initiation and plaque growth, and by incorporating information from biological experiments. It is based on two consecutive processes: a probabilistic dose-dependent plaque initiation process, followed by deterministic plaque growth. As a proof of principle, experimental plaque size data from carotid arteries from irradiated ApoE[Formula: see text] mice was used to illustrate how this model can provide insight into the underlying biological processes. This analysis supports the promoting role for radiation in plaque initiation, but the model can easily be extended to include dose-related effects on plaque growth if available experimental data would point in that direction. Moreover, the model could assist in designing future biological experiments on this research topic. Additional biological data such as plaque size data from chronically-irradiated mice or experimental data sets with a larger variety in biological parameters can help to further unravel the influence of radiation on plaque development. To the authors' knowledge, this is the first biophysical model that combines probabilistic and mechanistic modeling which uses experimental data to investigate the influence of radiation on plaque development.
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http://dx.doi.org/10.1007/s00411-017-0709-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5655690PMC
November 2017

Role of TGF Beta and PPAR Alpha Signaling Pathways in Radiation Response of Locally Exposed Heart: Integrated Global Transcriptomics and Proteomics Analysis.

J Proteome Res 2017 01 18;16(1):307-318. Epub 2016 Nov 18.

Helmholtz Zentrum München - German Research Center for Environmental Health GmbH , Institute of Radiation Biology, 85764 Neuherberg, Germany.

Epidemiological data from patients undergoing radiotherapy for thoracic tumors clearly show the damaging effect of ionizing radiation on cardiovascular system. The long-term impairment of heart function and structure after local high-dose irradiation is associated with systemic inflammatory response, contraction impairment, microvascular damage, and cardiac fibrosis. The goal of the present study was to investigate molecular mechanisms involved in this process. C57BL/6J mice received a single X-ray dose of 16 Gy given locally to the heart at the age of 8 weeks. Radiation-induced changes in the heart transcriptome and proteome were investigated 40 weeks after the exposure. The omics data were analyzed by bioinformatics tools and validated by immunoblotting. Integrated network analysis of transcriptomics and proteomics data elucidated the signaling pathways that were similarly affected at gene and protein level. Analysis showed induction of transforming growth factor (TGF) beta signaling but inactivation of peroxisome proliferator-activated receptor (PPAR) alpha signaling in irradiated heart. The putative mediator role of mitogen-activated protein kinase cascade linking PPAR alpha and TGF beta signaling was supported by data from immunoblotting and ELISA. This study indicates that both signaling pathways are involved in radiation-induced heart fibrosis, metabolic disordering, and impaired contractility, a pathophysiological condition that is often observed in patients that received high radiation doses in thorax.
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http://dx.doi.org/10.1021/acs.jproteome.6b00795DOI Listing
January 2017

A comparative molecular survey of malaria prevalence among Eastern chimpanzee populations in Issa Valley (Tanzania) and Kalinzu (Uganda).

Malar J 2016 08 19;15(1):423. Epub 2016 Aug 19.

Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences Brno, 612 42, Brno, Czech Republic.

Background: Habitat types can affect vector and pathogen distribution and transmission dynamics. The prevalence and genetic diversity of Plasmodium spp. in two eastern chimpanzee populations-Kalinzu Forest Reserve, Uganda and Issa Valley, Tanzania-inhabiting different habitat types was investigated. As a follow up study the effect of host sex and age on infections patterns in Kalinzu Forest Reserve chimpanzees was determined.

Methods: Molecular methods were employed to detect Plasmodium DNA from faecal samples collected from savanna-woodland (Issa Valley) and forest (Kalinzu Forest Reserve) chimpanzee populations.

Results: Based on a Cytochrome-b PCR assay, 32 out of 160 Kalinzu chimpanzee faecal samples were positive for Plasmodium DNA, whilst no positive sample was detected in 171 Issa Valley chimpanzee faecal samples. Sequence analysis revealed that previously known Laverania species (Plasmodium reichenowi, Plasmodium billbrayi and Plasmodium billcollinsi) are circulating in the Kalinzu chimpanzees. A significantly higher proportion of young individuals were tested positive for infections, and switching of Plasmodium spp. was reported in one individual. Amongst the positive individuals sampled more than once, the success of amplification of Plasmodium DNA from faeces varied over sampling time.

Conclusion: The study showed marked differences in the prevalence of malaria parasites among free ranging chimpanzee populations living in different habitats. In addition, a clear pattern of Plasmodium infections with respect to host age was found. The results presented in this study contribute to understanding the ecological aspects underlying the malaria infections in the wild. Nevertheless, integrative long-term studies on vector abundance, Plasmodium diversity during different seasons between sites would provide more insight on the occurrence, distribution and ecology of these pathogens.
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http://dx.doi.org/10.1186/s12936-016-1476-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992209PMC
August 2016

Blood and lymphatic microvessel damage in irradiated human skin: The role of TGF-β, endoglin and macrophages.

Radiother Oncol 2015 Sep 4;116(3):455-61. Epub 2015 Sep 4.

Division of Cellular Stress Response, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.

Background And Purpose: Microvascular damage is an important component of late radiation-induced morbidity. In our pre-clinical models, we demonstrated that repair of vessel injury is dependent on proper endoglin-mediated transforming growth factor-beta (TGF-β) signalling and that it can be affected by infiltrating macrophages. We now wanted to extend these findings in irradiated patients, using skin as a model system, and assess whether bisphosphonates could modulate the response.

Materials And Methods: Paired skin biopsies from irradiated and non-irradiated sites were obtained from 48 breast cancer patients. In 8 patients, biopsies were repeated after 4months of bisphosphonate treatment. Immunohistochemistry was used to assess vascular alterations and leucocyte infiltration. Western Blot and qPCR were used to assess expression of growth factors and their receptors.

Results: Decreased blood vessel numbers at early time points were followed by increased endoglin expression and restoration of vessel number. Loss of small lymphatic vessels was associated with increased TGF-β levels, whereas dilation of lymphatic vessels correlated with increased macrophage infiltration. Bisphosphonate treatment reduced leucocyte infiltration, but also prevented restoration of blood vessel numbers after irradiation.

Conclusion: Radiation injury of the microvasculature is mediated through TGF-β, whereas repair is modulated by the co-receptor endoglin and promoted by macrophages.
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http://dx.doi.org/10.1016/j.radonc.2015.08.024DOI Listing
September 2015

The ecological determinants of baboon troop movements at local and continental scales.

Mov Ecol 2015 1;3(1):14. Epub 2015 Jul 1.

Department of Biosciences, College of Science, Swansea University, Swansea, UK.

Background: How an animal moves through its environment directly impacts its survival, reproduction, and thus biological fitness. A basic measure describing how an individual (or group) travels through its environment is Day Path Length (DPL), i.e., the distance travelled in a 24-hour period. Here, we investigate the ecological determinants of baboon (Papio spp.) troop DPL and movements at local and continental scales.

Results: At the continental scale we explore the ecological determinants of annual mean DPL for 47 baboon troops across 23 different populations, updating a classic study by Dunbar (Behav Ecol Sociobiol 31: 35-49, 1992). We find that variation in baboon DPLs is predicted by ecological dissimilarity across the genus range. Troops that experience higher average monthly rainfall and anthropogenic influences have significantly shorter DPL, whilst troops that live in areas with higher average annual temperatures have significantly longer DPL. We then explore DPLs and movement characteristics (the speed and distribution of turning angles) for yellow baboons (Papio cynocephalus) at a local scale, in the Issa Valley of western Tanzania. We show that our continental-scale model is a good predictor of DPL in Issa baboons, and that troops move significantly slower, and over shorter distances, on warmer days. We do not find any effect of season or the abundance of fruit resources on the movement characteristics or DPL of Issa baboons, but find that baboons moved less during periods of high fruit availability.

Conclusion: Overall, this study emphasises the ability of baboons to adapt their ranging behaviour to a range of ecological conditions and highlights how investigations of movement patterns at different spatial scales can provide a more thorough understanding of the ecological determinants of movement.
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http://dx.doi.org/10.1186/s40462-015-0040-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4487562PMC
July 2015

Population status of chimpanzees in the Masito-Ugalla Ecosystem, Tanzania.

Am J Primatol 2015 Oct 26;77(10):1027-35. Epub 2015 Jun 26.

Department of Archaeology and Anthropology, University of Cambridge, Cambridge CB2 3QG, United Kingdom.

More than 75 percent of Tanzania's chimpanzees live at low densities on land outside national parks. Chimpanzees are one of the key conservation targets in the region and long-term monitoring of these populations is essential for assessing the overall status of ecosystem health and the success of implemented conservation strategies. We aimed to assess change in chimpanzee density within the Masito-Ugalla Ecosystem (MUE) by comparing results of re-walking the same line transects in 2007 and 2014. We further used published remote sensing data derived from Landsat satellites to assess forest cover change within a 5 km buffer of these transects over that same period. We detected no statistically significant decline in chimpanzee density across the surveyed areas of MUE between 2007 and 2014, although the overall mean density of chimpanzees declined from 0.09 individuals/km(2) in 2007 to 0.05 individuals/km(2) in 2014. Whether this change is biologically meaningful cannot be determined due to small sample sizes and large, entirely overlapping error margins. It is therefore possible that the MUE chimpanzee population has been stable over this period and indeed in some areas (Issa Valley, Mkanga, Kamkulu) even showed an increase in chimpanzee density. Variation in chimpanzee habitat preference for ranging or nesting could explain variation in density at some of the survey sites between 2007 and 2014. We also found a relationship between increasing habitat loss and lower mean chimpanzee density. Future surveys will need to ensure a larger sample size, broader geographic effort, and random survey design, to more precisely determine trends in MUE chimpanzee density and population size over time.
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http://dx.doi.org/10.1002/ajp.22438DOI Listing
October 2015