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1.  Genetic Structure of Chimpanzee Populations 
PLoS Genetics  2007;3(4):e66.
Little is known about the history and population structure of our closest living relatives, the chimpanzees, in part because of an extremely poor fossil record. To address this, we report the largest genetic study of the chimpanzees to date, examining 310 microsatellites in 84 common chimpanzees and bonobos. We infer three common chimpanzee populations, which correspond to the previously defined labels of “western,” “central,” and “eastern,” and find little evidence of gene flow between them. There is tentative evidence for structure within western chimpanzees, but we do not detect distinct additional populations. The data also provide historical insights, demonstrating that the western chimpanzee population diverged first, and that the eastern and central populations are more closely related in time.
Author Summary
Common chimpanzees have been traditionally classified into three populations: western, central, and eastern. While the morphological or behavioral differences are very small, genetic studies of mitochondrial DNA and the Y chromosome have supported the geography-based designations. To obtain a crisp picture of chimpanzee population structure, we gather far more data than previously available: 310 microsatellite markers genotyped in 78 common chimpanzees and six bonobos, allowing a high resolution genetic analysis of chimpanzee population structure analogous to recent studies that have elucidated human structure. We show that the traditional chimpanzee population designations—western, central, and eastern—accurately label groups of individuals that can be defined from the genetic data without any prior knowledge about where the samples were collected. The populations appear to be discontinuous, and we find little evidence for gradients of variation reflecting hybridization among chimpanzee populations. Regarding chimpanzee history, we demonstrate that central and eastern chimpanzees are more closely related to each other in time than either is to western chimpanzees.
PMCID: PMC1853122  PMID: 17447846
2.  Genetics: A New Landscape for Medical Geography 
The emergence and re-emergence of human pathogens resistant to medical treatment will present a challenge to the international public health community in the coming decades. Geography is uniquely positioned to examine the progressive evolution of pathogens across space and through time, and to link molecular change to interactions between population and environmental drivers. Landscape as an organizing principle for the integration of natural and cultural forces has a long history in geography, and, more specifically, in medical geography. Here, we explore the role of landscape in medical geography, the emergent field of landscape genetics, and the great potential that exists in the combination of these two disciplines. We argue that landscape genetics can enhance medical geographic studies of local-level disease environments with quantitative tests of how human-environment interactions influence pathogenic characteristics. In turn, such analyses can expand theories of disease diffusion to the molecular scale and distinguish the important factors in ecologies of disease that drive genetic change of pathogens.
PMCID: PMC3928082  PMID: 24558292
medical geography; disease ecology; landscape genetics; pathogenic evolution
3.  Chimpanzee population structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change 
BMC Evolutionary Biology  2015;15(1):2.
The Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) is found in the Gulf of Guinea biodiversity hotspot located in western equatorial Africa. This subspecies is threatened by habitat fragmentation due to logging and agricultural development, hunting for the bushmeat trade, and possibly climate change. Although P. t. ellioti appears to be geographically separated from the neighboring central chimpanzee (P. t. troglodytes) by the Sanaga River, recent population genetics studies of chimpanzees from across this region suggest that additional factors may also be important in their separation. The main aims of this study were: 1) to model the distribution of suitable habitat for P. t. ellioti across Cameroon and Nigeria, and P. t. troglodytes in southern Cameroon, 2) to determine which environmental factors best predict their optimal habitats, and 3) to compare modeled niches and test for their levels of divergence from one another. A final aim of this study was to examine the ways that climate change might impact suitable chimpanzee habitat across the region under various scenarios.
Ecological niche models (ENMs) were created using the software package Maxent for the three populations of chimpanzees that have been inferred to exist in Cameroon and eastern Nigeria: (i) P. t. troglodytes in southern Cameroon, (ii) P. t. ellioti in northwestern Cameroon, and (iii) P. t. ellioti in central Cameroon. ENMs for each population were compared using the niche comparison test in ENMtools, which revealed complete niche divergence with very little geographic overlap of suitable habitat between populations.
These findings suggest that a positive relationship may exist between environmental variation and the partitioning of genetic variation found in chimpanzees across this region. ENMs for each population were also projected under three different climate change scenarios for years 2020, 2050, and 2080. Suitable habitat of P. t. ellioti in northwest Cameroon / eastern Nigeria is expected to remain largely unchanged through 2080 in all considered scenarios. In contrast, P. t. ellioti in central Cameroon, which represents half of the population of this subspecies, is expected to experience drastic reductions in its ecotone habitat over the coming century.
Electronic supplementary material
The online version of this article (doi:10.1186/s12862-014-0275-z) contains supplementary material, which is available to authorized users.
PMCID: PMC4314735  PMID: 25608567
4.  Neighbouring chimpanzee communities show different preferences in social grooming behaviour 
Grooming handclasp (GHC) behaviour was originally advocated as the first evidence of social culture in chimpanzees owing to the finding that some populations engaged in the behaviour and others do not. To date, however, the validity of this claim and the extent to which this social behaviour varies between groups is unclear. Here, we measured (i) variation, (ii) durability and (iii) expansion of the GHC behaviour in four chimpanzee communities that do not systematically differ in their genetic backgrounds and live in similar ecological environments. Ninety chimpanzees were studied for a total of 1029 h; 1394 GHC bouts were observed between 2010 and 2012. Critically, GHC style (defined by points of bodily contact) could be systematically linked to the chimpanzee's group identity, showed temporal consistency both within and between groups, and could not be accounted for by the arm-length differential between partners. GHC has been part of the behavioural repertoire of the chimpanzees under study for more than 9 years (surpassing durability criterion) and spread across generations (surpassing expansion criterion). These results strongly indicate that chimpanzees' social behaviour is not only motivated by innate predispositions and individual inclinations, but may also be partly cultural in nature.
PMCID: PMC3479803  PMID: 22933372
group differences; Pan troglodytes; grooming handclasp; traditions; Chimfunshi Wildlife Orphanage Trust; social culture
5.  Psychoactive substances and the political ecology of mental distress 
The goal of this paper is to both understand and depathologize clinically significant mental distress related to criminalized contact with psychoactive biotic substances by employing a framework known as critical political ecology of health and disease from the subdiscipline of medical geography. The political ecology of disease framework joins disease ecology with the power-calculus of political economy and calls for situating health-related phenomena in their broad social and economic context, demonstrating how large-scale global processes are at work at the local level, and giving due attention to historical analysis in understanding the relevant human-environment relations. Critical approaches to the political ecology of health and disease have the potential to incorporate ever-broadening social, political, economic, and cultural factors to challenge traditional causes, definitions, and sociomedical understandings of disease. Inspired by the patient-centered medical diagnosis critiques in medical geography, this paper will use a critical political ecology of disease approach to challenge certain prevailing sociomedical interpretations of disease, or more specifically, mental disorder, found in the field of substance abuse diagnostics and the related American punitive public policy regimes of substance abuse prevention and control, with regards to the use of biotic substances. It will do this by first critically interrogating the concept of "substances" and grounding them in an ecological context, reviewing the history of both the development of modern substance control laws and modern substance abuse diagnostics, and understanding the biogeographic dimensions of such approaches. It closes with proposing a non-criminalizing public health approach for regulating human close contact with psychoactive substances using the example of cannabis use.
PMCID: PMC3278374  PMID: 22257499
6.  Factors that drive variation among gut microbial communities 
Gut Microbes  2013;4(5):403-408.
Surveys of humans from around the world have revealed differences in gut microbiota composition among geographically separated populations. But because humans from the same regions often share common ancestry as well as dietary and cultural habits, most studies have not been able to differentiate among the effects of heritable factors and external factors on the composition of the gut microbiota. Here we discuss how the analysis of gut microbial communities of chimpanzees residing in Gombe Stream National Park has provided an unprecedented opportunity to measure the effects of external factors while controlling for heritable factors. The differences in gut microbiota composition between separated host populations of chimpanzees are due almost entirely to external factors, with the contribution of heritable factors to intraspecific variation in gut microbiota composition being too small to detect. The dominant influence of external factors in generating differences among the gut microbiota of our closest relatives lends promise to the possibility of manipulating the composition of the gut microbiome within human hosts. These results highlight the need for controlled studies that isolate the roles of specific external factors, such as diet, cultural practices and geography, in generating differences in the gut microbiota composition.
PMCID: PMC3839986  PMID: 23941900
microbiota; Pan troglodytes; enterotypes
7.  Effective sociodemographic population assessment of elusive species in ecology and conservation management 
Ecology and Evolution  2013;3(9):2903-2916.
Wildlife managers are urgently searching for improved sociodemographic population assessment methods to evaluate the effectiveness of implemented conservation activities. These need to be inexpensive, appropriate for a wide spectrum of species and straightforward to apply by local staff members with minimal training. Furthermore, conservation management would benefit from single approaches which cover many aspects of population assessment beyond only density estimates, to include for instance social and demographic structure, movement patterns, or species interactions. Remote camera traps have traditionally been used to measure species richness. Currently, there is a rapid move toward using remote camera trapping in density estimation, community ecology, and conservation management. Here, we demonstrate such comprehensive population assessment by linking remote video trapping, spatially explicit capture–recapture (SECR) techniques, and other methods. We apply it to three species: chimpanzees Pan troglodytes troglodytes, gorillas Gorilla gorilla gorilla, and forest elephants Loxodonta cyclotis in Loango National Park, Gabon. All three species exhibited considerable heterogeneity in capture probability at the sex or group level and density was estimated at 1.72, 1.2, and 1.37 individuals per km2 and male to female sex ratios were 1:2.1, 1:3.2, and 1:2 for chimpanzees, gorillas, and elephants, respectively. Association patterns revealed four, eight, and 18 independent social groups of chimpanzees, gorillas, and elephants, respectively: key information for both conservation management and studies on the species' ecology. Additionally, there was evidence of resident and nonresident elephants within the study area and intersexual variation in home range size among elephants but not chimpanzees. Our study highlights the potential of combining camera trapping and SECR methods in conducting detailed population assessments that go far beyond documenting species diversity patterns or estimating single species population size. Our study design is widely applicable to other species and spatial scales, and moderately trained staff members can collect and process the required data. Furthermore, assessments using the same method can be extended to include several other ecological, behavioral, and demographic aspects: fission and fusion dynamics and intergroup transfers, birth and mortality rates, species interactions, and ranging patterns.
PMCID: PMC3790539  PMID: 24101982
Camera trapping; chimpanzee; conservation management; density; elephant; gorilla; multiple species monitoring; spatially explicit capture–recapture
8.  Genomic Tools for Evolution and Conservation in the Chimpanzee: Pan troglodytes ellioti Is a Genetically Distinct Population 
PLoS Genetics  2012;8(3):e1002504.
In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10–20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions.
Author Summary
Chimpanzees are viewed with fondness as our closest animal relatives and are valued by scientists for the biological and evolutionary insights they provide. In spite of this, the relationships between different populations of common chimpanzees are still relatively poorly understood, a situation that potentially threatens conservation efforts. Here we have used information gathered in the Chimpanzee Genome Project to design comprehensive tests of genetic variability that show unambiguously the existence of four genetically distinct groups (or populations) of common chimpanzee. We demonstrate that previous methods based on mitochondrial DNA sequences alone are not always accurate and show the feasibility of cheap new genetic tests of individuals' origins that could play an important role in conservation.
PMCID: PMC3291532  PMID: 22396655
9.  Quantifying Effects of Environmental and Geographical Factors on Patterns of Genetic Differentiation 
Molecular ecology  2011;20(22):4631-4642.
Elucidating the factors influencing genetic differentiation is an important task in biology, and the relative contribution from natural selection and genetic drift has long been debated. In this study, we used a regression-based approach to simultaneously estimate the quantitative contributions of environmental adaptation and isolation by distance on genetic variation in Boechera stricta, a wild relative of Arabidopsis. Patterns of discrete and continuous genetic differentiation coexist within this species. For the discrete differentiation between two major genetic groups, environment has larger contribution than geography, and we also identified a significant environment-by-geography interaction effect. Elsewhere in the species range, we found a latitudinal cline of genetic variation reflecting only isolation by distance. To further confirm the effect of environmental selection on genetic divergence, we identified the specific environmental variables predicting local genotypes in allopatric and sympatric regions. Water availability was identified as the possible cause of differential local adaptation in both geographic regions, confirming the role of environmental adaptation in driving and maintaining genetic differentiation between the two major genetic groups. In addition, the environment-by-geography interaction is further confirmed by the finding that water availability is represented by different environmental factors in the allopatric and sympatric regions. In conclusion, this study found that geographical and environmental factors together created stronger and more discrete genetic differentiation than isolation by distance alone, which only produced a gradual, clinal pattern of genetic variation. These findings emphasize the importance of environmental selection in shaping patterns of species-wide genetic variation in the natural environment.
PMCID: PMC3204174  PMID: 21999331
Genetic variation; Environment; Geography; Niche modeling; Environmental adaptation
10.  Biogeography and ecology: towards the integration of two disciplines 
Although ecology and biogeography had common origins in the natural history of the nineteenth century, they diverged substantially during the early twentieth century as ecology became increasingly hypothesis-driven and experimental. This mechanistic focus narrowed ecology's purview to local scales of time and space, and mostly excluded large-scale phenomena and historical explanations. In parallel, biogeography became more analytical with the acceptance of plate tectonics and the development of phylogenetic systematics, and began to pay more attention to ecological factors that influence large-scale distributions. This trend towards unification exposed problems with terms such as ‘community’ and ‘niche,’ in part because ecologists began to view ecological communities as open systems within the contexts of history and geography. The papers in this issue represent biogeographic and ecological perspectives and address the general themes of (i) the niche, (ii) comparative ecology and macroecology, (iii) community assembly, and (iv) diversity. The integration of ecology and biogeography clearly is a natural undertaking that is based on evolutionary biology, has developed its own momentum, and which promises novel, synthetic approaches to investigating ecological systems and their variation over the surface of the Earth. We offer suggestions on future research directions at the intersection of biogeography and ecology.
PMCID: PMC3130436  PMID: 21768158
history; macroecology; niche; phylogeny; regional community; species sorting
11.  Unravelling the structure of species extinction risk for predictive conservation science 
Extinction risk varies across species and space owing to the combined and interactive effects of ecology/life history and geography. For predictive conservation science to be effective, large datasets and integrative models that quantify the relative importance of potential factors and separate rapidly changing from relatively static threat drivers are urgently required. Here, we integrate and map in space the relative and joint effects of key correlates of The International Union for Conservation of Nature-assessed extinction risk for 8700 living birds. Extinction risk varies significantly with species' broad-scale environmental niche, geographical range size, and life-history and ecological traits such as body size, developmental mode, primary diet and foraging height. Even at this broad scale, simple quantifications of past human encroachment across species' ranges emerge as key in predicting extinction risk, supporting the use of land-cover change projections for estimating future threat in an integrative setting. A final joint model explains much of the interspecific variation in extinction risk and provides a remarkably strong prediction of its observed global geography. Our approach unravels the species-level structure underlying geographical gradients in extinction risk and offers a means of disentangling static from changing components of current and future threat. This reconciliation of intrinsic and extrinsic, and of past and future extinction risk factors may offer a critical step towards a more continuous, forward-looking assessment of species' threat status based on geographically explicit environmental change projections, potentially advancing global predictive conservation science.
PMCID: PMC3061137  PMID: 20943690
birds; IUCN Red List; projected threat; future global change; structural equation models
12.  Functional analysis of human and chimpanzee promoters 
Genome Biology  2005;6(7):R57.
Twelve promoters of genes differentially expressed between humans and chimpanzees were tested for expression activity in culture cells. Seven promoters showed a significant difference in expression level between the human and chimpanzee promoter, but only three were in the same direction as the tissues, indicating that relevant expression differences between humans and chimpanzees will be difficult to predict from cell culture experiments or DNA sequences
It has long been argued that changes in gene expression may provide an additional and crucial perspective on the evolutionary differences between humans and chimpanzees. To investigate how often expression differences seen in tissues are caused by sequence differences in the proximal promoters, we tested the expression activity in cultured cells of human and chimpanzee promoters from genes that differ in mRNA expression between human and chimpanzee tissues.
Twelve promoters for which the corresponding gene had been shown to be differentially expressed between humans and chimpanzees in liver or brain were tested. Seven showed a significant difference in activity between the human promoter and the orthologous chimpanzee promoter in at least one of the two cell lines used. However, only three of them showed a difference in the same direction as in the tissues.
Differences in proximal promoter activity are likely to be common between humans and chimpanzees, but are not linked in a simple fashion to gene-expression levels in tissues. This suggests that several genetic differences between humans and chimpanzees might be responsible for a single expression difference and thus that relevant expression differences between humans and chimpanzees will be difficult to predict from cell culture experiments or DNA sequences.
PMCID: PMC1175988  PMID: 15998446
13.  Alu Recombination-Mediated Structural Deletions in the Chimpanzee Genome 
PLoS Genetics  2007;3(10):e184.
With more than 1.2 million copies, Alu elements are one of the most important sources of structural variation in primate genomes. Here, we compare the chimpanzee and human genomes to determine the extent of Alu recombination-mediated deletion (ARMD) in the chimpanzee genome since the divergence of the chimpanzee and human lineages (∼6 million y ago). Combining computational data analysis and experimental verification, we have identified 663 chimpanzee lineage-specific deletions (involving a total of ∼771 kb of genomic sequence) attributable to this process. The ARMD events essentially counteract the genomic expansion caused by chimpanzee-specific Alu inserts. The RefSeq databases indicate that 13 exons in six genes, annotated as either demonstrably or putatively functional in the human genome, and 299 intronic regions have been deleted through ARMDs in the chimpanzee lineage. Therefore, our data suggest that this process may contribute to the genomic and phenotypic diversity between chimpanzees and humans. In addition, we found four independent ARMD events at orthologous loci in the gorilla or orangutan genomes. This suggests that human orthologs of loci at which ARMD events have already occurred in other nonhuman primate genomes may be “at-risk” motifs for future deletions, which may subsequently contribute to human lineage-specific genetic rearrangements and disorders.
Author Summary
The recent sequencing of a number of primate genomes shows that small segments of DNA known as Alu elements are found repeatedly along all chromosomes, and indeed comprise ∼10% of the human genome. Although older Alu elements that have been in the genome for a long time accumulate some random mutations, overall these elements retain high levels of sequence identity among themselves. The presence of many near-identical Alu elements located close to each other makes primate genomes prone to DNA recombination events that generate genomic deletions of varying sizes. Here, by scanning the chimpanzee genome for such deletions, we determined the role of the Alu recombination-mediated deletion process in creating structural differences between the chimpanzee and human genomes. Using a combination of computational and experimental techniques, we identified 663 deletions, involving the removal of ∼771 kb of genomic sequence. Interestingly, about half of these deletions were located within known or predicted genes, and in several cases, the deletions removed coding exons from chimpanzee genes as compared to their human counterparts. Alu recombination-mediated deletion shows signs of being a major sculptor of primate genomes and may be responsible for generating some of the genetic differences between humans and chimpanzees.
PMCID: PMC2041999  PMID: 17953488
14.  Ethnomedicinal and ecological status of plants in Garhwal Himalaya, India 
The northern part of India harbours a great diversity of medicinal plants due to its distinct geography and ecological marginal conditions. The traditional medical systems of northern India are part of a time tested culture and honored still by people today. These traditional systems have been curing complex disease for more than 3,000 years. With rapidly growing demand for these medicinal plants, most of the plant populations have been depleted, indicating a lack of ecological knowledge among communities using the plants. Thus, an attempt was made in this study to focus on the ecological status of ethnomedicinal plants, to determine their availability in the growing sites, and to inform the communities about the sustainable exploitation of medicinal plants in the wild.
The ecological information regarding ethnomedicinal plants was collected in three different climatic regions (tropical, sub-tropical and temperate) for species composition in different forest layers. The ecological information was assessed using the quadrate sampling method. A total of 25 quadrats, 10 × 10 m were laid out at random in order to sample trees and shrubs, and 40 quadrats of 1 × 1 m for herbaceous plants. In each climatic region, three vegetation sites were selected for ecological information; the mean values of density, basal cover, and the importance value index from all sites of each region were used to interpret the final data. Ethnomedicinal uses were collected from informants of adjacent villages. About 10% of inhabitants (older, experienced men and women) were interviewed about their use of medicinal plants. A consensus analysis of medicinal plant use between the different populations was conducted.
Across the different climatic regions a total of 57 species of plants were reported: 14 tree species, 10 shrub species, and 33 herb species. In the tropical and sub-tropical regions, Acacia catechu was the dominant tree while Ougeinia oojeinensis in the tropical region and Terminalia belerica in the sub-tropical region were least dominant reported. In the temperate region, Quercus leucotrichophora was the dominant tree and Pyrus pashia the least dominant tree. A total of 10 shrubs were recorded in all three regions: Adhatoda vasica was common species in the tropical and sub-tropical regions however, Rhus parviflora was common species in the sub-tropical and temperate regions. Among the 33 herbs, Sida cordifolia was dominant in the tropical and sub-tropical regions, while Barleria prionitis the least dominant in tropical and Phyllanthus amarus in the sub-tropical region. In temperate region, Vernonia anthelmintica was dominant and Imperata cylindrica least dominant. The consensus survey indicated that the inhabitants have a high level of agreement regarding the usages of single plant. The index value was high (1.0) for warts, vomiting, carminative, pain, boils and antiseptic uses, and lowest index value (0.33) was found for bronchitis.
The medicinal plants treated various ailments. These included diarrhea, dysentery, bronchitis, menstrual disorders, gonorrhea, pulmonary affections, migraines, leprosy. The ecological studies showed that the tree density and total basal cover increased from the tropical region to sub-tropical and temperate regions. The species composition changed with climatic conditions. Among the localities used for data collection in each climatic region, many had very poor vegetation cover. The herbaceous layer decreased with increasing altitude, which might be an indication that communities at higher elevations were harvesting more herbaceous medicinal plants, due to the lack of basic health care facilities. Therefore, special attention needs to be given to the conservation of medicinal plants in order to ensure their long-term availability to the local inhabitants. Data on the use of individual species of medicinal plants is needed to provide an in-depth assessment of the plants availability in order to design conservation strategies to protect individual species.
PMCID: PMC3212913  PMID: 22011477
A disease resembling human typhoid fever has been induced by feeding live cultures of Salmonella typhosa to young chimpanzees, thus confirming the classical reports of Grünbaum and of Metchnikoff and Besredka. Detailed clinical observations, results of stool and blood cultures, and serological studies have confirmed the impression that the disease produced in chimpanzees closely resembles the mild form of human typhoid fever frequently seen in childhood. Gross and histologic examination of intestines, mesenteric lymph nodes, liver, spleen, and other organs of orally infected chimpanzees has demonstrated that the pathological findings are essentially indistinguishable from those seen in mild typhoid fever in man. The clinical spectrum of disease seen in chimpanzees ranged from moderately severe illness, through transitory illness, to afebrile infection with or without bacteriemia (but invariably with an antibody response), occasionally leading to the development of persisting biliary infection and the carrier state. Thus the range of illness observed in chimpanzees resembled that seen in man, except that the severe and complicated forms of typhoid fever were not observed in the chimpanzee. A reason for this difference is proposed and discussed. In contrast to the limitations imposed upon the interpretation of human epidemiologic observations, it has been possible to demonstrate in the chimpanzee that clinical variation in disease pattern from animal to animal may occur despite the administration of the same dose of the same bacterial strain simultaneously to an entire group of animals under study; in other words, variation in clinical pattern is dependent on inherent, non-specific host factors as well as on dose, strain or preceding state of immunity. Variation in dose and in challenge strain of S. typhosa employed also appeared to have an effect upon the likelihood of producing febrile as against afebrile infection in chimpanzees. The dose required to produce clinical disease, even with the more virulent strain, was excessively large compared to what is believed to be the dose required to produce illness in man; the limitations of this assumption, and suggested explanations for the findings, are discussed. The production of the spectrum of typhoid fever in the chimpanzee has made possible the study of basic problems in this disease which are not amenable to definitive study through the use of prevailing laboratory techniques.
PMCID: PMC2137207  PMID: 13725751
16.  Ecology and geography of hemorrhagic fever with renal syndrome in Changsha, China 
BMC Infectious Diseases  2013;13:305.
Hemorrhagic fever with renal syndrome (HFRS) is an important public health problem in mainland China. HFRS is particularly endemic in Changsha, the capital city of Hunan Province, with one of the highest incidences in China. The occurrence of HFRS is influenced by environmental factors. However, few studies have examined the relationship between environmental variation (such as land use changes and climate variations), rodents and HFRS occurrence. The purpose of this study is to predict the distribution of HFRS and identify the risk factors and relationship between HFRS occurrence and rodent hosts, combining ecological modeling with the Markov chain Monte Carlo approach.
Ecological niche models (ENMs) were used to evaluate potential geographic distributions of rodent species by reconstructing details of their ecological niches in ecological dimensions, and projecting the results onto geography. The Genetic Algorithm for Rule-set Production was used to produce ENMs. Data were collected on HFRS cases in Changsha from 2005 to 2009, as well as national land survey data, surveillance data of rodents, meteorological data and normalized difference vegetation index (NDVI).
The highest occurrence of HFRS was in districts with strong temperature seasonality, where elevation is below 200 m, mean annual temperature is around 17.5°C, and annual precipitation is below 1600 mm. Cultivated and urban lands in particular are associated with HFRS occurrence. Monthly NDVI values of areas predicted present is lower than areas predicted absent, with high seasonal variation. The number of HFRS cases was correlated with rodent density, and the incidence of HFRS cases in urban and forest areas was mainly associated with the density of Rattus norvegicus and Apodemus agrarius, respectively.
Heterogeneity between different areas shows that HFRS occurrence is affected by the intensity of human activity, climate conditions, and landscape elements. Rodent density and species composition have significant impacts on the number of HFRS cases and their distribution.
PMCID: PMC3708768  PMID: 23819824
17.  From Forest to Farm: Systematic Review of Cultivar Feeding by Chimpanzees – Management Implications for Wildlife in Anthropogenic Landscapes 
PLoS ONE  2012;7(4):e33391.
Crop-raiding is a major source of conflict between people and wildlife globally, impacting local livelihoods and impeding conservation. Conflict mitigation strategies that target problematic wildlife behaviours such as crop-raiding are notoriously difficult to develop for large-bodied, cognitively complex species. Many crop-raiders are generalist feeders. In more ecologically specialised species crop-type selection is not random and evidence-based management requires a good understanding of species' ecology and crop feeding habits. Comprehensive species-wide studies of crop consumption by endangered wildlife are lacking but are important for managing human–wildlife conflict. We conducted a comprehensive literature search of crop feeding records by wild chimpanzees (Pan troglodytes), a ripe-fruit specialist. We assessed quantitatively patterns of crop selection in relation to species-specific feeding behaviour, agricultural exposure, and crop availability. Crop consumption by chimpanzees is widespread in tropical Africa. Chimpanzees were recorded to eat a considerable range of cultivars (51 plant parts from 36 species). Crop part selection reflected a species-typical preference for fruit. Crops widely distributed in chimpanzee range countries were eaten at more sites than sparsely distributed crops. We identified ‘high’ and ‘low’ conflict crops according to their attractiveness to chimpanzees, taking account of their importance as cash crops and/or staple foods to people. Most (86%) high conflict crops were fruits, compared to 13% of low conflict crops. Some widely farmed cash or staple crops were seldom or never eaten by chimpanzees. Information about which crops are most frequently consumed and which are ignored has enormous potential for aiding on-the-ground stakeholders (i.e. farmers, wildlife managers, and conservation and agricultural extension practitioners) develop sustainable wildlife management schemes for ecologically specialised and protected species in anthropogenic habitats. However, the economic and subsistence needs of local people, and the crop-raiding behaviour of sympatric wildlife, must be considered when assessing suitability of particular crops for conflict prevention and mitigation.
PMCID: PMC3324475  PMID: 22509256
18.  Bonobos Fall within the Genomic Variation of Chimpanzees 
PLoS ONE  2011;6(6):e21605.
To gain insight into the patterns of genetic variation and evolutionary relationships within and between bonobos and chimpanzees, we sequenced 150,000 base pairs of nuclear DNA divided among 15 autosomal regions as well as the complete mitochondrial genomes from 20 bonobos and 58 chimpanzees. Except for western chimpanzees, we found poor genetic separation of chimpanzees based on sample locality. In contrast, bonobos consistently cluster together but fall as a group within the variation of chimpanzees for many of the regions. Thus, while chimpanzees retain genomic variation that predates bonobo-chimpanzee speciation, extensive lineage sorting has occurred within bonobos such that much of their genome traces its ancestry back to a single common ancestor that postdates their origin as a group separate from chimpanzees.
PMCID: PMC3126833  PMID: 21747915
19.  Gender and social geography: Impact on Lady Health Workers Mobility in Pakistan 
In Pakistan, where gendered norms restrict women's mobility, female community health workers (CHWs) provide doorstep primary health services to home-bound women. The program has not achieved optimal functioning. One reason, I argue, may be that the CHWs are unable to make home visits because they have to operate within the same gender system that necessitated their appointment in the first place. Ethnographic research shows that women’s mobility in Pakistan is determined not so much by physical geography as by social geography (the analysis of social phenomena in space). Irrespective of physical location, the presence of biradaria members (extended family) creates a socially acceptable ‘inside space’ to which women are limited. The presence of a non-biradari person, especially a man, transforms any space into an ‘outside space’, forbidden space. This study aims to understand how these cultural norms affect CHWs’ home-visit rates and the quality of services delivered.
Data will be collected in district Attock, Punjab. Twenty randomly selected CHWs will first be interviewed to explore their experiences of delivering doorstep services in the context of gendered norms that promote women's seclusion. Each CHW will be requested to draw a map of her catchment area using social mapping techniques. These maps will be used to survey women of reproductive age to assess variations in the CHW's home visitation rates and quality of family planning services provided. A sample size of 760 households (38 per CHW) is estimated to have the power to detect, with 95% confidence, households the CHWs do not visit. To explore the role of the larger community in shaping the CHWs mobility experiences, 25 community members will be interviewed and five CHWs observed as they conduct their home visits. The survey data will be merged with the maps to demonstrate if any disjunctures exist between CHWs’ social geography and physical geography. Furthermore, the impacts these geographies have on home visitation rates and quality of services delivered will be explored.
The study will provide generic and theoretical insights into how the CHW program policies and operations can improve working conditions to facilitate the work of female staff in order to ultimately provide high-quality services.
PMCID: PMC3524461  PMID: 23066890
Reproductive health services; Primary health care services; Pakistan; Family planning; Community health workers; Lady health worker; Gender; Women’s mobility; Social geography; Mixed methods
20.  Impact of Geography and Climate on the Genetic Differentiation of the Subtropical Pine Pinus yunnanensis 
PLoS ONE  2013;8(6):e67345.
Southwest China is a biodiversity hotspot characterized by complex topography, heterogeneous regional climates and rich flora. The processes and driving factors underlying this hotspot remain to be explicitly tested across taxa to gain a general understanding of the evolution of biodiversity and speciation in the region. In this study, we examined the role played by historically neutral processes, geography and environment in producing the current genetic diversity of the subtropical pine Pinus yunnanensis. We used genetic and ecological methods to investigate the patterns of genetic differentiation and ecological niche divergence across the distribution range of this species. We found both continuous genetic differentiation over the majority of its range, and discrete isolated local clusters. The discrete differentiation between two genetic groups in the west and east peripheries is consistent with niche divergence and geographical isolation of these groups. In the central area of the species’ range, population structure was shaped mainly by neutral processes and geography rather than by ecological selection. These results show that geographical and environmental factors together created stronger and more discrete genetic differentiation than isolation by distance alone, and illustrate the importance of ecological factors in forming or maintaining genetic divergence across a complex landscape. Our findings differ from other phylogenetic studies that identified the historical drainage system in the region as the primary factor shaping population structure, and highlight the heterogeneous contributions that geography and environment have made to genetic diversity among taxa in southwest China.
PMCID: PMC3693954  PMID: 23840668
21.  The geography of recreational physical activity in England 
Health & place  2010;17(1):157-165.
Levels of physical activity have declined considerably over recent decades in England, and there is evidence that activity patterns vary across areas. Previous studies of the geography of physical activity have frequently relied on model based synthetic estimates. Using data from a large population survey this study develops a direct measure of recreational physical activity and investigates variations in activity patterns across English Local Authorities. For both sexes the results show a distinct geography of recreational physical activity associated with north/south variations and urban/rural status. The environmental and behavioural factors driving those patterns are still poorly understood. We conclude that the variations observed might reflect recreational opportunities and the socio-cultural context of areas.
PMCID: PMC3722549  PMID: 20934899
recreational physical activity; geographical variation; socio-demographics; urban-rural status; England
22.  Single nucleotide polymorphisms unravel hierarchical divergence and signatures of selection among Alaskan sockeye salmon (Oncorhynchus nerka) populations 
Disentangling the roles of geography and ecology driving population divergence and distinguishing adaptive from neutral evolution at the molecular level have been common goals among evolutionary and conservation biologists. Using single nucleotide polymorphism (SNP) multilocus genotypes for 31 sockeye salmon (Oncorhynchus nerka) populations from the Kvichak River, Alaska, we assessed the relative roles of geography (discrete boundaries or continuous distance) and ecology (spawning habitat and timing) driving genetic divergence in this species at varying spatial scales within the drainage. We also evaluated two outlier detection methods to characterize candidate SNPs responding to environmental selection, emphasizing which mechanism(s) may maintain the genetic variation of outlier loci.
For the entire drainage, Mantel tests suggested a greater role of geographic distance on population divergence than differences in spawn timing when each variable was correlated with pairwise genetic distances. Clustering and hierarchical analyses of molecular variance indicated that the largest genetic differentiation occurred between populations from distinct lakes or subdrainages. Within one population-rich lake, however, Mantel tests suggested a greater role of spawn timing than geographic distance on population divergence when each variable was correlated with pairwise genetic distances. Variable spawn timing among populations was linked to specific spawning habitats as revealed by principal coordinate analyses. We additionally identified two outlier SNPs located in the major histocompatibility complex (MHC) class II that appeared robust to violations of demographic assumptions from an initial pool of eight candidates for selection.
First, our results suggest that geography and ecology have influenced genetic divergence between Alaskan sockeye salmon populations in a hierarchical manner depending on the spatial scale. Second, we found consistent evidence for diversifying selection in two loci located in the MHC class II by means of outlier detection methods; yet, alternative scenarios for the evolution of these loci were also evaluated. Both conclusions argue that historical contingency and contemporary adaptation have likely driven differentiation between Kvichak River sockeye salmon populations, as revealed by a suite of SNPs. Our findings highlight the need for conservation of complex population structure, because it provides resilience in the face of environmental change, both natural and anthropogenic.
PMCID: PMC3049142  PMID: 21332997
23.  The Number of Cultural Traits Is Correlated with Female Group Size but Not with Male Group Size in Chimpanzee Communities 
PLoS ONE  2010;5(3):e9241.
What determines the number of cultural traits present in chimpanzee (Pan troglodytes) communities is poorly understood. In humans, theoretical models suggest that the frequency of cultural traits can be predicted by population size. In chimpanzees, however, females seem to have a particularly important role as cultural carriers. Female chimpanzees use tools more frequently than males. They also spend more time with their young, skewing the infants' potential for social learning towards their mothers. In Gombe, termite fishing has been shown to be transmitted from mother to offspring. Lastly, it is female chimpanzees that transfer between communities and thus have the possibility of bringing in novel cultural traits from other communities. From these observations we predicted that females are more important cultural carriers than males. Here we show that the reported number of cultural traits in chimpanzee communities correlates with the number of females in chimpanzee communities, but not with the number of males. Hence, our results suggest that females are the carriers of chimpanzee culture.
PMCID: PMC2844409  PMID: 20352086
24.  A Genome-Wide Association Study Identifies Variants Underlying the Arabidopsis thaliana Shade Avoidance Response 
PLoS Genetics  2012;8(3):e1002589.
Shade avoidance is an ecologically and molecularly well-understood set of plant developmental responses that occur when the ratio of red to far-red light (R∶FR) is reduced as a result of foliar shade. Here, a genome-wide association study (GWAS) in Arabidopsis thaliana was used to identify variants underlying one of these responses: increased hypocotyl elongation. Four hypocotyl phenotypes were included in the study, including height in high R∶FR conditions (simulated sun), height in low R∶FR conditions (simulated shade), and two different indices of the response of height to low R∶FR. GWAS results showed that variation in these traits is controlled by many loci of small to moderate effect. A known PHYC variant contributing to hypocotyl height variation was identified and lists of significantly associated genes were enriched in a priori candidates, suggesting that this GWAS was capable of generating meaningful results. Using metadata such as expression data, GO terms, and other annotation, we were also able to identify variants in candidate de novo genes. Patterns of significance among our four phenotypes allowed us to categorize associations into three groups: those that affected hypocotyl height without influencing shade avoidance, those that affected shade avoidance in a height-dependent fashion, and those that exerted specific control over shade avoidance. This grouping allowed for the development of explicit hypotheses about the genetics underlying shade avoidance variation. Additionally, the response to shade did not exhibit any marked geographic distribution, suggesting that variation in low R∶FR–induced hypocotyl elongation may represent a response to local conditions.
Author Summary
The goal of this work was to identify genetic variants underlying a well-characterized environmental response, the elongation of Arabidopsis thaliana hypocotyls (seedling stems) in response to shade, otherwise known as shade avoidance. We performed a genome-wide association study with four phenotypes: absolute hypocotyl height of plants grown in both simulated sun and shade and two measures of how height responded to shade. With this study, we confirmed previous findings that variants in two photoreceptors were associated with hypocotyl height variation. We also found associations with genetic variants in previously-identified shade avoidance genes, as well as with variants in genes not typically considered part of the shade avoidance pathway. By examining patterns of which of the four phenotypes were associated with each gene, we were then able to discriminate between genetic variants that have a general role in hypocotyl height variation and variants that are specifically involved in the shade avoidance response. We also found that shade avoidance was not broadly associated with geography, suggesting that variation in this trait may be due to local differences in light quality.
PMCID: PMC3305432  PMID: 22438834
25.  Continent-Wide Decoupling of Y-Chromosomal Genetic Variation from Language and Geography in Native South Americans 
PLoS Genetics  2013;9(4):e1003460.
Numerous studies of human populations in Europe and Asia have revealed a concordance between their extant genetic structure and the prevailing regional pattern of geography and language. For native South Americans, however, such evidence has been lacking so far. Therefore, we examined the relationship between Y-chromosomal genotype on the one hand, and male geographic origin and linguistic affiliation on the other, in the largest study of South American natives to date in terms of sampled individuals and populations. A total of 1,011 individuals, representing 50 tribal populations from 81 settlements, were genotyped for up to 17 short tandem repeat (STR) markers and 16 single nucleotide polymorphisms (Y-SNPs), the latter resolving phylogenetic lineages Q and C. Virtually no structure became apparent for the extant Y-chromosomal genetic variation of South American males that could sensibly be related to their inter-tribal geographic and linguistic relationships. This continent-wide decoupling is consistent with a rapid peopling of the continent followed by long periods of isolation in small groups. Furthermore, for the first time, we identified a distinct geographical cluster of Y-SNP lineages C-M217 (C3*) in South America. Such haplotypes are virtually absent from North and Central America, but occur at high frequency in Asia. Together with the locally confined Y-STR autocorrelation observed in our study as a whole, the available data therefore suggest a late introduction of C3* into South America no more than 6,000 years ago, perhaps via coastal or trans-Pacific routes. Extensive simulations revealed that the observed lack of haplogroup C3* among extant North and Central American natives is only compatible with low levels of migration between the ancestor populations of C3* carriers and non-carriers. In summary, our data highlight the fact that a pronounced correlation between genetic and geographic/cultural structure can only be expected under very specific conditions, most of which are likely not to have been met by the ancestors of native South Americans.
Author Summary
In the largest population genetic study of South Americans to date, we analyzed the Y-chromosomal makeup of more than 1,000 male natives. We found that the male-specific genetic variation of Native Americans lacks any clear structure that could sensibly be related to their geographic and/or linguistic relationships. This finding is consistent with a rapid initial peopling of South America, followed by long periods of isolation in small tribal groups. The observed continent-wide decoupling of geography, spoken language, and genetics contrasts strikingly with previous reports of such correlation from many parts of Europe and Asia. Moreover, we identified a cluster of Native American founding lineages of Y chromosomes, called C-M217 (C3*), within a restricted area of Ecuador in North-Western South America. The same haplogroup occurs at high frequency in Central, East, and North East Asia, but is virtually absent from North (except Alaska) and Central America. Possible scenarios for the introduction of C-M217 (C3*) into Ecuador may thus include a coastal or trans-Pacific route, an idea also supported by occasional archeological evidence and the recent coalescence of the C3* haplotypes, estimated from our data to have occurred some 6,000 years ago.
PMCID: PMC3623769  PMID: 23593040

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