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Gray M.,International Gorilla Conservation Program | Roy J.,Max Planck Institute for Evolutionary Anthropology | Vigilant L.,Max Planck Institute for Evolutionary Anthropology | Fawcett K.,Dian Fossey Gorilla Fund International | And 6 more authors.
Biological Conservation | Year: 2013

Monitoring changes in the population dynamics of endangered species is crucial to effective conservation strategies. The mountain gorilla population of the Virunga Massif has been the subject of intensive conservation efforts, research and several censuses over the last 40. years, but the region has also been affected by political instability and war. Here we present results from the 2010 census, which was the first to utilize genetic analyses of fecal samples for the entire population. The genetic analyses improved the accuracy of the population estimate by identifying several instances in which gorillas otherwise would have been undercounted or double-counted. The population was estimated to be 480 individuals; including 349 individuals found in 24 groups that were habituated for research and tourism, 101 individuals found in 12 unhabituated groups, fourteen solitary males, and a correction factor of sixteen for undetected infants. The population has increased by 26% since 2003 (an annual rate of 3.7%) and it has almost doubled since 1981. Nearly all of the increase can be attributed to a relatively higher growth rate in the habituated groups from 2003 to 2010, and in all five of the previous intervals between consecutive censuses. Nonetheless, it would be imprudent to habituate additional groups due to the concomitant risks of disease transmission from humans, behavioral disturbance and potential vulnerability to poaching. The results show that it is possible for conservation efforts to succeed even under difficult conditions, while highlighting the continuing challenges of managing a wild population of both habituated and unhabituated gorillas. © 2012 Elsevier Ltd.


Hans J.B.,Max Planck Institute for Evolutionary Anthropology | Haubner A.,Max Planck Institute for Evolutionary Anthropology | Arandjelovic M.,Max Planck Institute for Evolutionary Anthropology | Bergl R.A.,North Carolina Zoological Park | And 6 more authors.
American Journal of Primatology | Year: 2015

Genes encoded by the major histocompatibility complex (MHC) are crucial for the recognition and presentation of antigens to the immune system. In contrast to their closest relatives, chimpanzees and humans, much less is known about variation in gorillas at these loci. This study explored the exon 2 variation of -DPB1, -DQB1, and -DRB genes in 46 gorillas from four populations while simultaneously evaluating the feasibility of using fecal samples for high-throughput MHC genotyping. By applying strict similarity- and frequency-based analysis, we found, despite our modest sample size, a total of 18 alleles that have not been described previously, thereby illustrating the potential for efficient and highly accurate MHC genotyping from non-invasive DNA samples. We emphasize the importance of controlling for multiple potential sources of error when applying this massively parallel short-read sequencing technology to PCR products generated from low concentration DNA extracts. We observed pronounced differences in MHC variation between species, subspecies and populations that are consistent with both the ancient and recent demographic histories experienced by gorillas. © 2015 Wiley Periodicals, Inc.


Roy J.,Max Planck Institute for Evolutionary Anthropology | Vigilant L.,Max Planck Institute for Evolutionary Anthropology | Gray M.,International Gorilla Conservation Program | Wright E.,Max Planck Institute for Evolutionary Anthropology | And 7 more authors.
Biological Conservation | Year: 2014

Monitoring the population dynamics of endangered species is a critical component of conservation management strategies, but attaining accurate and precise estimates of population sizes using cost and time effective methods can be challenging. Routine censuses of the two populations of critically endangered mountain gorillas (. Gorilla beringei beringei) have been conducted over the last decades to monitor populations and evaluate the effectiveness of conservation strategies. A census in 2006 of the mountain gorillas in Bwindi Impenetrable National Park, Uganda, showed the value of genetic analysis of fecal samples collected at nest sites by revealing discrepancies between the numbers of nests and uniquely identified gorillas. In this study, we censused the Bwindi gorilla population using a 'mark-recapture' method which involved genetic analysis of fecal samples collected in 2011 during two 'sweep' surveys of the entire park. We found that a notable proportion of gorillas were missed in either of the two sweeps (minimum 35% and 31%, respectively). Based on the number of genotyped gorillas and correction factors, we estimated the population to contain a minimum of 400 individuals. Using the mark-recapture approach, we infer possibly as many as 430 gorillas (95% confidence interval: 398-487). As the 2010 census of the Virunga Massif population found 480 gorillas, the total number of mountain gorillas worldwide is at least 880 individuals. Simulations using different mark-recapture models suggest that a future census of Bwindi mountain gorillas would benefit by increasing the number of sweeps in order to achieve accurate and precise results. Finally, based on our results, we recommend a sequential approach incorporating a pilot study and simulations for optimizing time and resources in large mammal genetic census studies. © 2014 Elsevier Ltd.


Roy J.,Max Planck Institute for Evolutionary Anthropology | Gray M.,International Gorilla Conservation Program | Stoinski T.,The Dian Fossey Gorilla Fund International and Zoo Atlanta | Robbins M.M.,Max Planck Institute for Evolutionary Anthropology | Vigilant L.,Max Planck Institute for Evolutionary Anthropology
BMC Ecology | Year: 2014

Molecular studies in social mammals rarely compare the inferences gained from genetic analyses with field information, especially in the context of dispersal. In this study, we used genetic data to elucidate sex-specific dispersal dynamics in the Virunga Massif mountain gorilla population (Gorilla beringei beringei), a primate species characterized by routine male and female dispersal from stable mixed-sex social groups. Specifically, we conducted spatial genetic structure analyses for each sex and linked our genetically-based observations with some key demographic and behavioural data from this population.Results: To investigate the spatial genetic structure of mountain gorillas, we analysed the genotypes of 193 mature individuals at 11 microsatellite loci by means of isolation-by-distance and spatial autocorrelation analyses. Although not all males and females disperse, female gorillas displayed an isolation-by-distance pattern among groups and a signal of dispersal at short distances from their natal group based on spatial autocorrelation analyses. In contrast, male genotypes were not correlated with spatial distance, thus suggesting a larger mean dispersal distance for males as compared to females. Both within sex and mixed-sex pairs were on average genetically more related within groups than among groups.Conclusions: Our study provides evidence for an intersexual difference in dispersal distance in the mountain gorilla. Overall, it stresses the importance of investigating spatial genetic structure patterns on a sex-specific basis to better understand the dispersal dynamics of the species under investigation. It is currently poorly understood why some male and female gorillas disperse while others remain in the natal group. Our results on average relatedness within and across groups confirm that groups often contain close relatives. While inbreeding avoidance may play a role in driving female dispersal, we note that more detailed dyadic genetic analyses are needed to shed light on the role of inbreeding avoidance as an ultimate cause of female dispersal in mountain gorillas. © 2014 Roy et al.; licensee BioMed Central Ltd.


Robbins A.M.,Max Planck Institute for Evolutionary Anthropology | Gray M.,International Gorilla Conservation Program | Uwingeli P.,Rwanda Development Board | Mburanumwe I.,Institute Congolais Pour La Conservation Of La Nature | And 2 more authors.
Primates | Year: 2014

Using 30 years of demographic data from 15 groups, this study estimates how harem size, female fertility, and offspring survival may contribute to variance in the siring rates of dominant male mountain gorillas throughout the Virunga Volcano Region. As predicted for polygynous species, differences in harem size were the greatest source of variance in the siring rate, whereas differences in female fertility and offspring survival were relatively minor. Harem size was positively correlated with offspring survival, even after removing all known and suspected cases of infanticide, so the correlation does not seem to reflect differences in the ability of males to protect their offspring. Harem size was not significantly correlated with female fertility, which is consistent with the hypothesis that mountain gorillas have minimal feeding competition. Harem size, offspring survival, and siring rates were not significantly correlated with the proportion of dominant tenures that occurred in multimale groups versus one-male groups; even though infanticide is less likely when those tenures end in multimale groups than one-male groups. In contrast with the relatively small contribution of offspring survival to variance in the siring rates of this study, offspring survival is a major source of variance in the male reproductive success of western gorillas, which have greater predation risks and significantly higher rates of infanticide. If differences in offspring protection are less important among male mountain gorillas than western gorillas, then the relative importance of other factors may be greater for mountain gorillas. Thus, our study illustrates how variance in male reproductive success and its components can differ between closely related species. © 2014, Japan Monkey Centre and Springer Japan.


Hoppe E.,Robert Koch Institute | Pauly M.,Robert Koch Institute | Gillespie T.R.,Emory University | Akoua-Koffi C.,Alassane Ouattara University | And 18 more authors.
Molecular biology and evolution | Year: 2015

Human adenoviruses (HAdV; species HAdV-A to -G) are highly prevalent in the human population, and represent an important cause of morbidity and, to a lesser extent, mortality. Recent studies have identified close relatives of these viruses in African great apes, suggesting that some HAdV may be of zoonotic origin. We analyzed more than 800 fecal samples from wild African great apes and humans to further investigate the evolutionary history and zoonotic potential of hominine HAdV. HAdV-B and -E were frequently detected in wild gorillas (55%) and chimpanzees (25%), respectively. Bayesian ancestral host reconstruction under discrete diffusion models supported a gorilla and chimpanzee origin for these viral species. Host switches were relatively rare along HAdV evolution, with about ten events recorded in 4.5 My. Despite presumably rare direct contact between sympatric populations of the two species, transmission events from gorillas to chimpanzees were observed, suggesting that habitat and dietary overlap may lead to fecal-oral cross-hominine transmission of HAdV. Finally, we determined that two independent HAdV-B transmission events to humans occurred more than 100,000 years ago. We conclude that HAdV-B circulating in humans are of zoonotic origin and have probably affected global human health for most of our species lifetime. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.


PubMed | University of Missouri, Max Planck Institute for Evolutionary Anthropology, International Gorilla Conservation Program, University of Illinois at Chicago and North Carolina Zoological Park
Type: Journal Article | Journal: American journal of primatology | Year: 2015

Genes encoded by the major histocompatibility complex (MHC) are crucial for the recognition and presentation of antigens to the immune system. In contrast to their closest relatives, chimpanzees and humans, much less is known about variation in gorillas at these loci. This study explored the exon 2 variation of -DPB1, -DQB1, and -DRB genes in 46 gorillas from four populations while simultaneously evaluating the feasibility of using fecal samples for high-throughput MHC genotyping. By applying strict similarity- and frequency-based analysis, we found, despite our modest sample size, a total of 18 alleles that have not been described previously, thereby illustrating the potential for efficient and highly accurate MHC genotyping from non-invasive DNA samples. We emphasize the importance of controlling for multiple potential sources of error when applying this massively parallel short-read sequencing technology to PCR products generated from low concentration DNA extracts. We observed pronounced differences in MHC variation between species, subspecies and populations that are consistent with both the ancient and recent demographic histories experienced by gorillas.


PubMed | Max Planck Institute for Evolutionary Anthropology, International Gorilla Conservation Program, World Wildlife Foundation WWF, Institute National Of Recherche Biomedicale and 8 more.
Type: Journal Article | Journal: Molecular biology and evolution | Year: 2015

Human adenoviruses (HAdV; species HAdV-A to -G) are highly prevalent in the human population, and represent an important cause of morbidity and, to a lesser extent, mortality. Recent studies have identified close relatives of these viruses in African great apes, suggesting that some HAdV may be of zoonotic origin. We analyzed more than 800 fecal samples from wild African great apes and humans to further investigate the evolutionary history and zoonotic potential of hominine HAdV. HAdV-B and -E were frequently detected in wild gorillas (55%) and chimpanzees (25%), respectively. Bayesian ancestral host reconstruction under discrete diffusion models supported a gorilla and chimpanzee origin for these viral species. Host switches were relatively rare along HAdV evolution, with about ten events recorded in 4.5 My. Despite presumably rare direct contact between sympatric populations of the two species, transmission events from gorillas to chimpanzees were observed, suggesting that habitat and dietary overlap may lead to fecal-oral cross-hominine transmission of HAdV. Finally, we determined that two independent HAdV-B transmission events to humans occurred more than 100,000 years ago. We conclude that HAdV-B circulating in humans are of zoonotic origin and have probably affected global human health for most of our species lifetime.

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