Jim Moore

The conserved transcriptome in human and rodent male gametogenesis

We report a cross-species expression profiling analysis of the human, mouse, and rat male meiotic transcriptional program, using enriched germ cell populations, whole gonads, and high-density oligonucleotide microarrays (GeneChips). Among 35% of the protein-coding genes present in rodent and human genomes that were found to be differentially expressed between germ cells and somatic controls, a key group of 357 conserved core loci was identified that displays highly similar meiotic and postmeiotic patterns of transcriptional induction across all three species. Genes known to be important for sexual reproduction are significantly enriched among differentially expressed core loci and a smaller group of conserved genes not detected in 17 nontesticular somatic tissues, correlating transcriptional activation and essential function in the male germ line. Some genes implicated in the etiology of cancer are found to be strongly transcribed in testis, suggesting that these genes may play unexpected roles in sexual reproduction. Expression profiling data further identified numerous conserved genes of biological and clinical interest previously unassociated with the mammalian male germ line.

Female transfer in primates

Intergroup transfer by males is nearly universal among social primates. Furthermore, among the most frequently studied monkeys-savanna baboons and Japanese and rhesus macaques—females typically remain in their natal groups, so troops are composed of related matrilines. These facts strongly support two major theories: (l) that kin selection is a powerful force in patterning sociality (if one is to live in a group, one should prefer a group of one’s relatives); and (2) that the ultimate explanation for intergroup transfer is the avoidance of inbreeding depression (though both sexes would prefer to live with kin, one sex has to disperse to avoid inbreeding and for a variety of reasons the losing sex is generally male). Substantial rates of transfer by females in social species with routine male transfer would cast doubt on both ideas. In fact, evidence reviewed here indicates that female transfer is not unusual and among folivorous primates (e.g., Alouatta,the Colobinae) it seems to be routine. In addition to casting doubt on the demographic significance of inbreeding avoidance and favoring mutualistic and/or game theory interpretations of behavior over nepotistic ones, this finding supports the hypothesis that predator detection is the primary selective pressure favoring sociality for many primates. Finally, while female bonding [sensuWrangham, R. W. (1980), Behaviour75:262–299] among primates appears to be less common than generally believed, the observed correlation between female transfer and morphological adaptations to folivory provides empirical support for Wrangham’s model for the evolution of female-bonded groups.

Dispersal, nepotism, and primate social behavior

High degrees of relatedness within primate social groups are thought to promote the evolution of altruistic behavior via kin selection. Dispersal, for whatever reason, should limit opportunities for nepotistic behaviors. Conversely, emigration is usually attributed to the avoidance of inbreeding depression. Actual dispersal patterns may result from a balance of these forces. Systematic behavioral differences are expected between taxa that differ in such patterns. In fact, comparisons of (a) colobines vs. cercopithecines, (b) bonnet, stumptailed, and Barbary macaques vs. Japanese and rhesus macaques, and (c) red vs. mantled howler monkeys yield a perplexing blend of unexplained differences and unmet theoretical expectations. Kin selection may be less important than generally believed, and/or methodological standardization more so.

Subsistence strategies of two "savanna" chimpanzee populations: the stable isotope evidence.

Twenty‐two chimpanzee hair samples collected from night nests at two different “savanna” sites were analyzed for carbon and nitrogen stable isotope ratios represented as δ13C and δ15N values. The first at Ugalla, Tanzania is a miombo woodland with grass groundcover and small patches of forest. The second at Ishasha, Democratic Republic of the Congo is a habitat composed of riverine gallery forest, semideciduous thicket forest, wooded grassland, and grassland. Based on comparative data from other primates, Ugalla hair δ13C values suggest that the chimpanzees are feeding primarily in the woodland rather than in forest patches or on grassland foods (grasses or grammivorous fauna). Similar comparisons indicate that the Ishasha chimpanzees are feeding within the forests and not in more open areas. In addition, the Ugalla chimpanzees had δ15N values that indicate extensive ingestion of leguminous flowers, seeds, and/or leaves. The Ishasha samples show a range encompassing three trophic levels. Two samples with the most positive values may indicate a nursing signal or vertebrate‐feeding. Three individuals with intermediate values are similar to those in omnivorous nonhuman primate species. The four individuals with the lowest values are very similar to those in herbivorous monkeys. Stable isotope ratios permit time‐averaged and habitat‐specific dietary comparisons among sites, even without habituation or detailed foraging observations. Am. J. Primatol. 49:297–314, 1999.

Paternity exclusion in a community of wild chimpanzees using hypervariable simple sequence repeats

We report the use of hypervariable simple sequence repeat (SSR) nuclear loci to study paternity in a community of wild chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. All 43 living members of a habituated community were sampled and 35 were genotyped at 8 SSR loci using DNA amplified from hair. Paternity exclusions were performed for 25 chimpanzees including 10 for whom the mother was also genotyped. In each case 12–20 males were potential fathers based on their age and/ or direct observation of sexual behaviour. 179 tests involving potential father/offspring combinations were performed. In four cases the data permit the probable identification of the previously undetermined father; these are the first such determinations for free‐ranging chimpanzees, and the first based on non‐invasive sampling. In another four cases we were able to exclude all but two to five potential fathers, and in the remaining cases we were able to exclude all living males. For molecular ecologists SSR genotype databases offer important advantages over currently popular minisatellite DNA fingerprinting: they can be analysed unequivocally using traditional population genetics techniques and they can be expanded through time and space by other researchers.

Savanna chimpanzees use tools to harvest the underground storage organs of plants.

It has been hypothesized that plant underground storage organs (USOs) played key roles in the initial hominin colonization of savanna habitats, the development of the distinctive skull and tooth morphology of the genus Australopithecus, and the evolution of the genus Homo by serving as “fallback foods” exploited during periods of food shortage. These hypotheses have been tested mostly by morphological, isotopic, and microwear analyses of hominin bones and teeth. Archaeological evidence of USO digging technology is equivocal. Until now relevant data from studies of chimpanzees, useful in behavioral models of early hominins because of their phylogenetic proximity and anatomical similarities, have been lacking. Here we report on the first evidence of chimpanzees using tools to dig for USOs, suggesting that exploitation of such resources was within the cognitive and technological reach of the earliest hominins. Consistent with scenarios of hominin adaptation to savannas, these data come from Ugalla (Tanzania), one of the driest, most open and seasonal chimpanzee habitats. USOs are, however, exploited during the rainy season, well after the period of most likely food shortage, contradicting the specific prediction of fallback food hypotheses. The discovery that savanna chimpanzees use tools to obtain USOs contradicts yet another claim of human uniqueness and provides a model for the study of variables influencing USO use among early hominins.

Non-invasive sampling and DNA amplification for paternity exclusion, community structure, and phylogeography in wild chimpanzees

Genetic studies of free-ranging primates have been seriously impeded by difficulties of sampling tissues, including the undesirability of bleeding habituated animals, of transporting frozen samples to the laboratory, and of the inherent inadequacies of accessible variation including allozymes, mtDNA RFLP patterns and DNA fingerprints. We have developed methods of non-invasive DNA sampling and DNA-level genotyping which, when combined with a hierarchical analysis of mtDNA sequences and hypervariable nDNA simple sequence repeat (microsatellite) loci size length polymorphisms, facilitate the resolution of most questions at the individual, social group (community), population, and species (phylogenetic) levels. This approach, based on DNA amplified from shed hair, represents an important new tool for the acquisition of genetic information and will facilitate the study and management of both captive and free-ranging chimpanzees (Pan troglodytes). Our hierarchical analysis of population genetics of chimpanzees has revealed high historical levels of gene flow and large effective population sizes, as well as substantial divergence between the West African subspecies and chimpanzees from central and East Africa. At the community level, closer relatedness among philopatric males than among females supports the view that kin selection has been an evolutionary force shaping male-male cooperation in this species. Results from our study of the now relatively isolated Gombe community suggest that habitat fragmentation affects population genetic structure and possibly population viability.

High Prevalence of Simian Immunodeficiency Virus Infection in a Community of Savanna Chimpanzees

ABSTRACT Simian immunodeficiency virus of chimpanzees (SIVcpz) has a significant negative impact on the health, reproduction, and life span of chimpanzees, yet the prevalence and distribution of this virus in wild-living populations are still only poorly understood. Here, we show that savanna chimpanzees, who live in ecologically marginal habitats at 10- to 50-fold lower population densities than forest chimpanzees, can be infected with SIVcpz at high prevalence rates. Fecal samples were collected from nonhabituated eastern chimpanzees (Pan troglodytes schweinfurthii) in the Issa Valley (n = 375) and Shangwa River (n = 6) areas of the Masito-Ugalla region in western Tanzania, genotyped to determine the number of sampled individuals, and tested for SIVcpz-specific antibodies and nucleic acids. None of 5 Shangwa River apes tested positive for SIVcpz; however, 21 of 67 Issa Valley chimpanzees were SIVcpz infected, indicating a prevalence rate of 31% (95% confidence interval, 21% to 44%). Two individuals became infected during the 14-month observation period, documenting continuing virus spread in this community. To characterize the newly identified SIVcpz strains, partial and full-length viral sequences were amplified from fecal RNA of 10 infected chimpanzees. Phylogenetic analyses showed that the Ugalla viruses formed a monophyletic lineage most closely related to viruses endemic in Gombe National Park, also located in Tanzania, indicating a connection between these now separated communities at some time in the past. These findings document that SIVcpz is more widespread in Tanzania than previously thought and that even very low-density chimpanzee populations can be infected with SIVcpz at high prevalence rates. Determining whether savanna chimpanzees, who face much more extreme environmental conditions than forest chimpanzees, are more susceptible to SIVcpz-associated morbidity and mortality will have important scientific and conservation implications.

Identification of Chimpanzee Subspecies with DNA from Hair and Allele-Specific Probes

We describe a non-invasive method of determining the subspecies identity of common chimpanzees (Pan troglodytes), based on subspecies-specific sequence differences in the mitochondrial genome. This procedure involves the extraction of DNA from hair, the amplification of a short (410 base pair b. p. )) segment of the non-coding displacement loop (D-loop) by the polymerase chain reaction (PCR), and subspecies identification based on rapid allele-specific oligonucleotide (ASO) probe dot-blot typing. This approach will contribute to : (i) the colony-level management of captive chimpanzees by enabling managers to recognize hybrids between subspecies and minimize outbreeding depression; (ii) the recognition of inappropriately matched individuals in comparative behavioural and experimental studies; and (iii) forensic questions surrounding the origin of illegally traded animals.

Gorillas (Gorilla gorilla gorilla) in the Likouala swamp forests of north central Congo: Preliminary data on populations and ecology

Until recently it was generally believed that gorillas avoid water. In two recent, independent faunal surveys in the Likouala swamp of north central Congo, we have found that gorillas occur at high densities, extending the known range of Gorilla gorilla gorillavery close to the Oubangui River. The gorillas in this area fed on the abundant ground vegetation of herbaceous monocotyledons in the swamp forest. In adjacent islands of terra firmathere was little evidence of gorilla nesting or feeding, indicating that they spend at least part of the year almost exclusively in the swamp forests. Recent reports from several sites in West Africa indicate that swamp forests may generally provide abundant food resources that are used regularly by gorillas.