Mary Katherine Gonder

Great ape genetic diversity and population history

Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria–Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.

African origin of the malaria parasite Plasmodium vivax

Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.

Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas.

ABSTRACT Chimpanzees and gorillas are the only nonhuman primates known to harbor viruses closely related to HIV-1. Phylogenetic analyses showed that gorillas acquired the simian immunodeficiency virus SIVgor from chimpanzees, and viruses from the SIVcpz/SIVgor lineage have been transmitted to humans on at least four occasions, leading to HIV-1 groups M, N, O, and P. To determine the geographic distribution, prevalence, and species association of SIVgor, we conducted a comprehensive molecular epidemiological survey of wild gorillas in Central Africa. Gorilla fecal samples were collected in the range of western lowland gorillas (n = 2,367) and eastern Grauer gorillas (n = 183) and tested for SIVgor antibodies and nucleic acids. SIVgor antibody-positive samples were identified at 2 sites in Cameroon, with no evidence of infection at 19 other sites, including 3 in the range of the Eastern gorillas. In Cameroon, based on DNA and microsatellite analyses of a subset of samples, we estimated the prevalence of SIVgor to be 1.6% (range, 0% to 4.6%), which is significantly lower than the prevalence of SIVcpzPtt in chimpanzees (5.9%; range, 0% to 32%). All newly identified SIVgor strains formed a monophyletic lineage within the SIVcpz radiation, closely related to HIV-1 groups O and P, and clustered according to their field site of origin. At one site, there was evidence for intergroup transmission and a high intragroup prevalence. These isolated hot spots of SIVgor-infected gorilla communities could serve as a source for human infection. The overall low prevalence and sporadic distribution of SIVgor could suggest a decline of SIVgor in wild populations, but it cannot be excluded that SIVgor is still more prevalent in other parts of the geographical range of gorillas.

Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations

The history of the genus Pan is a topic of enduring interest. Chimpanzees (Pan troglodytes) are often divided into subspecies, but the population structure and genetic history of chimpanzees across Africa remain unclear. Some population genetics studies have led to speculation that, until recently, this species constituted a single population with ongoing gene flow across its range, which resulted in a continuous gradient of allele frequencies. Chimpanzees, designated here as P. t. ellioti, occupy the Gulf of Guinea region that spans southern Nigeria and western Cameroon at the center of the distribution of this species. Remarkably, few studies have included individuals from this region, hindering the examination of chimpanzee population structure across Africa. Here, we analyzed microsatellite genotypes of 94 chimpanzees, including 32 designated as P. t. ellioti. We find that chimpanzees fall into three major populations: (i) Upper Guinea in western Africa (P. t. verus); (ii) the Gulf of Guinea region (P. t. ellioti); and (iii) equatorial Africa (P. t. troglodytes and P. t. schweinfurthii). Importantly, the Gulf of Guinea population is significantly different genetically from the others, sharing a last common ancestor with the populations in Upper Guinea ~0.46 million years ago (mya) and equatorial Africa ~0.32 mya. Equatorial chimpanzees are subdivided into up to three populations occupying southern Cameroon, central Africa, and eastern Africa, which may have constituted a single population until ~0.10–0.11 mya. Finally, occasional hybridization may be occurring between the Gulf of Guinea and southern Cameroon populations.

New Genetic Evidence on the Evolution of Chimpanzee Populations and Implications for Taxonomy

Primatologists widely recognize chimpanzees as belonging to a single species, Pan troglodytes, which they traditionally have further divided into 3 subspecies: west African P. t. verus, central African P. t. troglodytes, and east African P. t. schweinfurthii. Previously, we suggested that the phylogeographic history of chimpanzees may be different from that implied by the widely used taxonomy of the species. We based the suggestion on only a limited sample of haplotypes from the first hypervariable region (HVRI) of mitochondrial (mt)DNA from chimpanzees in Nigeria. We have now compiled a more geographically comprehensive genetic database for chimpanzees, including samples obtained near the Niger and Sanaga Rivers. Our database is composed of 254 HVRI haplotypes from chimpanzees of known geographic origin, including 79 unique HVRI haplotypes from chimpanzees living in Nigeria and Cameroon. The genetic data provide clear evidence that a major phylogeographic break between chimpanzee lineages occurs near the Sanaga River in central Cameroon and suggest the need for a reclassification of chimpanzees.

Chimpanzee population structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change

BackgroundThe 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.ResultsEcological 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.ConclusionsThese 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.

The population genetics of wild chimpanzees in Cameroon and Nigeria suggests a positive role for selection in the evolution of chimpanzee subspecies

BackgroundChimpanzees (Pan troglodytes) can be divided into four subspecies. Substantial phylogenetic evidence suggests that these subspecies can be grouped into two distinct lineages: a western African group that includes P. t. verus and P. t. ellioti and a central/eastern African group that includes P. t. troglodytes and P. t. schweinfurthii. The geographic division of these two lineages occurs in Cameroon, where the rages of P. t. ellioti and P. t. troglodytes appear to converge at the Sanaga River. Remarkably, few population genetic studies have included wild chimpanzees from this region.ResultsWe analyzed microsatellite genotypes of 187 wild, unrelated chimpanzees, and mitochondrial control region sequencing data from 604 chimpanzees. We found that chimpanzees in Cameroon and eastern Nigeria comprise at least two, and likely three populations. Both the mtDNA and microsatellite data suggest that there is a primary separation of P. t. troglodytes in southern Cameroon from P. t. ellioti north and west of the Sanaga River. These two populations split ~200-250 thousand years ago (kya), but have exchanged one migrant per generation since separating. In addition, P. t. ellioti consists of two populations that split from one another ~4 kya. One population is located in the rainforests of western Cameroon and eastern Nigeria, whereas the second population appears to be confined to a savannah-woodland mosaic in central Cameroon.ConclusionsOur findings suggest that there are as many as three genetically distinct populations of chimpanzees in Cameroon and eastern Nigeria. P. t. troglodytes in southern Cameroon comprises one population that is separated from two populations of P. t. ellioti in western and central Cameroon, respectively. P. t. ellioti and P. t. troglodytes appear to be characterized by a pattern of isolation-with-migration, and thus, we propose that neutral processes alone can not explain the differentiation of P. t. ellioti and P. t. troglodytes.

Ebola in great apes – current knowledge, possibilities for vaccination, and implications for conservation and human health

Ebola virus disease (EVD) is a threat to human health and to the survival of African great apes. The disease has led to major population declines in chimpanzees Pan troglodytes and gorillas Gorilla gorilla, and infected great apes play an important role as sources of human EVD outbreaks. The threat posed by EVD raises the question whether vaccination of wild apes is an effective strategy to reduce the occurrence and impact of this disease. We review the current knowledge about EVD in great apes and document the link between outbreaks in apes and in humans, mainly via bushmeat consumption. We discuss the need for control strategies, such as vaccination, and describe aspects of primate behaviour, virus biology, vaccine composition, and vaccination principles that need to be considered when making management decisions about great ape vaccination. Finally, we identify gaps in the understanding of Ebola ecology and highlight surveillance and research that can aid the survival of great apes and reduce human exposure to Ebola virus. The severe impact of EVD indicates the need for efficient monitoring and, ultimately, control of Ebola. However, the unknown reservoir and unpredictable emergence of Ebola, the elusive nature of great apes, and the lack of licensed and suitable vaccines represent major hurdles for such control. Public education about zoonotic diseases and monitoring of great ape health are both important strategies. Experts should also discuss the feasibility of developing safe vaccines that can be delivered efficiently to large populations of elusive wild apes in their natural remote habitats. This review provides a platform for further interdisciplinary discussions, so that management plans can be discussed and adjusted according to possible future changes in the development, availability and cost of vaccines, the status of EVD, knowledge about Ebola ecology, and opinion on wildlife vaccination.

Long-term urban market dynamics reveal increased bushmeat carcass volume despite economic growth and proactive environmental legislation on Bioko Island, Equatorial Guinea

Bushmeat hunting is extensive in west and central Africa as both a means for subsistence and for commercial gain. Commercial hunting represents one of the primary threats to wildlife in the region, and confounding factors have made it challenging to examine how external factors influence the commercial bushmeat trade. Bioko Island, Equatorial Guinea is a small island with large tracts of intact forest that support sizeable populations of commercially valuable vertebrates, especially endemic primates. The island also has a low human population and has experienced dramatic economic growth and rapid development since the mid-1990’s. From October 1997 – September 2010, we monitored the largest bushmeat market on Bioko in Malabo, recording over 197,000 carcasses for sale. We used these data to analyze the dynamics of the market in relation to political events, environmental legislation, and rapid economic growth. Our findings suggest that bushmeat hunting and availability increased in parallel with the growth of Equatorial Guinea’s GDP and disposable income of its citizens. During this 13-year study, the predominant mode of capture shifted from trapping to shotguns. Consequently, carcass volume and rates of taxa typically captured with shotguns increased significantly, most notably including intensified hunting of Biokos unique and endangered monkey fauna. Attempts to limit bushmeat sales, including a 2007 ban on primate hunting and trade, were only transiently effective. The hunting ban was not enforced, and was quickly followed by a marked increase in bushmeat hunting compared to hunting rates prior to the ban. Our results emphasize the negative impact that rapid development and unenforced legislation have had on Bioko’s wildlife, and demonstrate the need for strong governmental support if conservation strategies are to be successful at preventing extinctions of tropical wildlife.

Origin of the human malaria parasite Plasmodium falciparum in gorillas

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.