Frances J. White’s research while affiliated with University of Oregon and other places

Despite recent advances in chronometric techniques (e.g., Uranium-Lead [U-Pb], cosmogenic nuclides, electron spin resonance spectroscopy [ESR]), considerable uncertainty remains regarding the age of many Plio-Pleistocene hominin sites, including several in South Africa. Consequently, biochronology remains important in assessments of Plio-Pleistocene geochronology and provides direct age estimates of the fossils themselves. Historically, cercopithecid monkeys have been among the most useful taxa for biochronology of early hominins because they are widely present and abundant in the African Plio-Pleistocene record. The last major studies using cercopithecids were published over 30 y ago. Since then, new hominin sites have been discovered, radiometric age estimates have been refined, and many changes have occurred in cercopithecid taxonomy and systematics. Thus, a biochronological reassessment using cercopithecids is long overdue. Here, we provide just such a revision based on our recent study of every major cercopithecid collection from African Plio-Pleistocene sites. In addition to correlations based on shared faunal elements, we present an analysis based on the dentition of the abundant cercopithecid Theropithecus oswaldi , which increases in size in a manner that is strongly correlated with geological age ( r ² ∼0.83), thereby providing a highly accurate age-estimation tool not previously utilized. In combination with paleomagnetic and U-Pb data, our results provide revised age estimates and suggest that there are no hominin sites in South Africa significantly older than ∼2.8 Ma. Where conflicting age estimates exist, we suggest that additional data are needed and recall that faunal estimates have ultimately proved reliable in the past (e.g., the age of the KBS Tuff).

Sex, age, diet, stress and social environment have all been shown to influence the gut microbiota. In several mammals, including humans, increased stress is related to decreasing gut microbial diversity and may differentially impact specific taxa. Recent evidence from gorillas shows faecal glucocorticoid metabolite concentration (FGMC) did not significantly explain gut microbial diversity, but it was significantly associated with the abundance of the family Anaerolineaceae. These patterns have yet to be examined in other primates, like bonobos ( Pan paniscus ). We compared FGMC to 16S rRNA amplicons for 202 bonobo faecal samples collected across 5 months to evaluate the impact of stress, measured with FGMC, on the gut microbiota. Alpha diversity measures (Chao’s and Shannon’s indexes) were not significantly related to FGMC. FGMC explained 0.80 % of the variation in beta diversity for Jensen–Shannon and 1.2% for weighted UniFrac but was not significant for unweighted UniFrac. We found that genus SHD-231 , a member of the family Anaerolinaceae had a significant positive relationship with FGMC. These results suggest that bonobos are relatively similar to gorillas in alpha diversity and family Anaerolinaceae responses to FGMC, but different from gorillas in beta diversity. Members of the family Anaerolinaceae may be differentially affected by FGMC across great apes. FGMC appears to be context dependent and may be species-specific for alpha and beta diversity but this study provides an example of consistent change in two African apes. Thus, the relationship between physiological stress and the gut microbiome may be difficult to predict, even among closely related species.

Significance There is genomic evidence of widespread admixture in deep time between many closely related species, including humans. Our closest living relatives, bonobos and chimpanzees, may also exhibit such patterns. However, assessing the exact degree of interbreeding remains challenging because previous studies have resulted in multiple inconsistent demographic models. We use an approach that addresses these gaps by analyzing all lineages, simultaneously estimating parameters, and comparing previously models. We find evidence of considerable introgression from western into eastern chimpanzees. We also show more breeding females than males and evidence of male-biased dispersal in western chimpanzees. These findings highlight the extent of admixture in bonobo and chimpanzee evolutionary history and are consistent with substantial differences between past and present chimpanzee biogeography.

Objectives Geographic variation is an important feature among primates, but the mechanisms underlying it are not well understood. Macaques are geographically widespread and have been translocated to captive populations, providing a prime opportunity to evaluate changes in cranial form in response to a novel environment. Clinal variation was assessed among wild fascicularis ‐group macaques and compared to two translocated populations to explore the relative contributions of developmental plasticity and microevolutionary forces in producing geographic variation in cranial form. Materials and Methods Forty‐five 3D coordinates over the cranium were taken on 380 wild macaques and 56 captive Macaca mulatta from Cayo Santiago, PR and Beaverton, OR. Geographic shape, represented by the singular warp scores from a two‐block partial least squares analysis, and centroid size were regressed against latitude, mean annual temperature, and mean annual precipitation among wild macaques. The two captive populations were compared to wild M. mulatta to assess potential changes in cranial form. Results Size and geographic shape were highly correlated with latitude in wild macaques, but neither ecological variable was important across the entire cline. Precipitation was important for shape only outside the tropics. Translocated M. mulatta are significantly larger, but not different in shape, compared to wild M. mulatta . Discussion These results are consistent with previous studies demonstrating cranial form is latitudinally variable among fascicularis ‐group macaques, but the potential drivers remain unclear. Size is highly plastic while geographic shape has evolved differentiation at interpopulation and interspecific levels. Variation in cranial morphology likely arises first in size, followed relatively rapidly by evolved modifications to shape.

Recommendations for the successful management and maintenance of bachelor groups of western lowland gorillas (Gorilla gorilla gorilla) in zoological settings have been an increasingly prevalent focus within the zoological community. Over the past two decades, studies have examined the impact of various environmental factors on the stability of bachelor groups, proposed management strategies for bachelor groups, and compared behavioral trends between bachelor and mixed-sex groups. These studies have clearly demonstrated that bachelor groups are complex social units that require specialized management approaches. In this study, we aimed to assess the extent to which bachelor group management across North American zoos accredited by the Association of Zoos and Aquariums aligns with established recommendations. We distributed a comprehensive survey broadly encompassing habitat and housing, aggression and wounding, group demographics, feeding, and training to the 22 zoos housing bachelor groups as of 2019. We received completed surveys from 19 zoos, representing a total of 21 social units and 59 individual gorillas. We used descriptive statistics to represent the range of current management strategies across the surveyed population and ANOVAs to assess significant variation in key demographic variables. Our results demonstrate that a majority of zoos have adopted the best practices for the formation of social groups established by Stoinski et al. in 2004. However, there is much less standardization across zoos in protocols surrounding training and feeding. Additionally, important variables in the assessment of wounding, such as time of day and location, are often unknown or not observed by animal care professionals. We highlight these two areas as being of particular focus in developing and adhering to consistent protocols across institutions.

Introgression appears increasingly ubiquitous in the evolutionary history of various taxa, including humans. However, accurately estimating introgression is difficult, particularly when 1) there are many parameters, 2) multiple models fit the data well, and 3) parameters are not simultaneously estimated. Here, we use the software Legofit to investigate the evolutionary history of bonobos (Pan paniscus) and chimpanzees (P. troglodytes) using whole genome sequences. This approach 1) ignores within-population variation, reducing the number of parameters requiring estimation, 2) allows for model selection, and 3) simultaneously estimates all parameters. We tabulated site patterns from the autosomes of 71 bonobos and chimpanzees representing all five extant Pan lineages. We then compared previously proposed demographic models and estimated parameters using a deterministic approach. We further considered sex bias in Pan evolutionary history by analyzing the site patterns from the X chromosome. Introgression from bonobos into the ancestor of eastern and central chimpanzees and from western into eastern chimpanzees best explained the autosomal site patterns. This second event was substantial with an estimated 0.21 admixture proportion. Estimates of effective population size and most divergence dates are consistent with previous findings; however, we observe a deeper divergence within chimpanzees at 987 ka. Finally, we identify male-biased reproduction in Pan evolutionary history and suggest that western to eastern chimpanzee introgression was driven by western males mating with eastern females.

Host sex, age, diet, stress, and social environment have all been found to influence the gut microbiota. In non-human primates (NHP), recent evidence from gorillas found fecal glucocorticoid metabolite concentration (FGMC) had no significant role in structuring their gut microbiota, but there was a significant differential abundance between family Anaerolineaceae and gorilla FGMC. This pattern has yet to be examined in other NHP, like bonobos (Pan paniscus). We compared FGMC to 16S rRNA amplicons for 201 bonobo fecal samples collected in the wild across five months to evaluate the impact of stress, measured with FGMC, on the gut microbiota. Simpsons index was the only alpha diversity index to have a significant linear relationship with FGMC [R2 = 0.9643, F(4, 210) = 28.56, p = 0.0023]. FGMC level explained 1.63% of the variation in beta diversity for Jensen-Shannon Distance, 2.49% for Weighted UniFrac, and 3.53% for Unweighted UniFrac using PERMANOVAs. Differential abundance models showed seventeen taxa that were significantly correlated with FGMC. We found that genus SHD-231 in the family Anaerolinaceae was significant in our differential abundance model results, similar to western lowland gorilla abundance model results. These results suggest bonobos exhibit different patterns than gorillas in alpha and beta diversity measures and that members of the family Anaerolinaceae may be differentially affected by host stress across great apes. Incorporating FGMC into gut microbiota research can provide a more robust understanding of how stress impacts the gut microbiota of primates and humans and has important ties to overall host health.

Optimal diet and functional response models are used to understand the evolution of primate foraging strategies. The predictions of these models can be tested by examining the geographic and seasonal variation in dietary diversity. Dietary diversity is a useful tool that allows dietary comparisons across differing sampling locations and time periods. Bonobos ( Pan paniscus ) are considered primarily frugivorous and consume fruits, leaves, insects, vertebrates, terrestrial herbaceous vegetation, and flowers. Frugivores, like bonobos, are valuable for examining dietary diversity and testing foraging models because they eat a variety of species and are subject to seasonal shifts in fruit availability. Frugivorous primate species thus allow for tests of how variation in dietary diversity is correlated with variation in ecological factors. We investigated measures of dietary diversity in bonobos at two research camps across field seasons within the same protected area (N’dele and Iyema) in Lomako Forest, Democratic Republic of the Congo. We compared the results of behavioral observation (1984/1985, 1991, 1995, 2014, and 2017) and fecal washing analysis (2007 and 2009) between seasons and study period using three diversity indices (Shannon’s, Simpson’s, and SW evenness). The average yearly dietary diversity indices at N’dele were Shannon’s Hʹ = 2.04, Simpson’s D = 0.82, and SW evenness = 0.88 while at Iyema, the indices were Shannon’s Hʹ = 2.02, Simpson’s D = 0.82, and SW evenness = 0.88. Behavioral observation data sets yielded significantly higher dietary diversity indices than fecal washing data sets. We found that food item (fruit, leaf, and flower) consumption was not associated with seasonal food availability for the 2017 behavioral observation data set. Shannon’s index was lower during periods when fewer bonobo dietary items were available to consume and higher when fruit was abundant. Finally, we found that optimal diet models best-explained patterns of seasonal food availability and dietary diversity. Dietary diversity is an essential factor to consider when understanding primate diets and can be a tool in understanding variation in primate diets, particularly among frugivores. Dietary diversity varies across populations of the same species and across time, and it is critical in establishing a complete understanding of how primate diets change over time.

Despite no significant difference in wounding between bachelor and mixed-sex groups of western lowland gorillas (Gorilla gorilla gorilla) in zoological settings, anecdotal concerns around the frequency and severity of wounding in bachelor groups have perpetuated opinions of all-male units as inherently less stable. Bachelor groups are prevalent within zoological organizations and necessitate specialized care and protocols separate from those for mixed-sex groups. We collected survey data on 59 gorillas in 21 bachelor groups across 19 zoos. This survey broadly encompassed group social and demographic history, exhibit design, management practices, and wounding over the past year. Previous experience suggested that overnight housing conditions could be an important influencing factor on wounding rates. We ran Pearson’s Correlations and ANOVAs to examine wounding within the context of overnight housing conditions as well as other management and demographic factors. We found a significant negative correlation between group duration and wounding rate such that wounding rate was lower in groups that were together longer if and only if groups were separated overnight (r=-0.62, N = 11, p = 0.04). This was further supported by ANOVAs which demonstrated that groups that have been together for longer had significantly higher rates of wounding when housed together overnight than when housed separately overnight (F = 3.51, df = 3, 17, p = 0.04). Finally, we found that mature silverbacks housed socially overnight sustain significantly more wounds than mature silverbacks housed separately overnight (F = 4.11; df = 1,31; p = 0.05). Based on our analyses, overnight housing conditions have a significant impact on wounding particularly when paired with long-term (> 7 years) group social history. We recommend that groups with long social histories or primarily mature members be separated overnight should housing facilities allow.