Estimating Pan evolutionary history from nucleotide site patterns

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.

A Comparison Of Fecal Glucocorticoid Metabolite Concentration And Gut Microbiota Diversity In Bonobos (Pan paniscus)

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.

Failure to account for behavioral variability overestimates bonobo populations and compromises accuracy in population monitoring

Wildlife population monitoring depends on accurate counts of individual animals or artefacts of behavior (e.g., nests or dung), but also must account for potential biases in the likelihood to encounter these animals or artefacts. In indirect surveying, which depends largely upon artefacts of behavior, likelihood to encounter indirect signs of a species is derived from both artefact production and decay. Although environmental context as well as behavior contribute to artefact abundance, variability in behaviors relevant to artefact abundance is rarely considered in population estimation. Here we demonstrate how ignoring behavioral variability contributes to overestimation of population size of a highly endangered great ape endemic only to the Democratic Republic of the Congo, the bonobo (Pan paniscus). Variability in decay of signs of bonobo presence (i.e., nests) is well documented and linked to environmental determinants. Conversely, a single metric of sign production (i.e., nest construction) is commonly used to estimate bonobo density, assumed to be representative of bonobo nest behavior across all contexts. We estimated nest construction rates from three bonobo groups within the Kokolopori Bonobo Reserve and found that nest construction rates in bonobos to be highly variable across populations as well as seasonal within populations. Failure to account for behavioral variability in nest construction leads to potentially severe degradation in accuracy of bonobo population estimates of abundance, accounting for a likely overestimation of bonobo numbers by 34%, and in the worst cases as high as 80% overestimation. Using bonobo nesting as an example, we demonstrate that failure to account for inter- and intra-population behavioral variation compromises our ability to monitor population change or reliably compare contributors to population decline or persistence. We argue that variation in sign production is but one of several potential ways that behavioral variability can affect conservation monitoring, should be measured across contexts whenever possible, and must be considered in population estimation confidence intervals. With increasing attention to behavioral variability as a potential tool for conservation, conservationists must also account for the impact that behavioral variability across time, space, individuals, and populations can play upon precision and accuracy of wildlife population estimation.

Relationships between the hard and soft dimensions of the nose in Pan troglodytes and Homo sapiens reveal the nasal protrusions of Plio-Pleistocene hominids

By identifying similarity in bone and soft tissue covariation patterns in hominids, it is possible to produce facial approximation methods that are compatible with more than one species of primate. In this study, we conducted an interspecific comparison of the nasomaxillary region in chimpanzees and modern humans with the aim of producing a method for predicting the nasal protrusions of ancient Plio-Pleistocene hominids. We addressed this aim by first collecting and performing regression analyses of linear and angular measurements of nasal cavity length and inclination in modern humans ( Homo sapiens; n = 72) and chimpanzees ( Pan troglodytes ; n = 19), and then by performing a set of out-of-group tests. The first test was performed on two subjects that belonged to the same genus as the training sample, i.e., Homo ( n = 1) and Pan ( n = 1), and the second test, which functioned as an interspecies compatibility test, was performed on Pan paniscus ( n = 1), Gorilla gorilla ( n = 3), Pongo pygmaeus ( n = 1), Pongo abelli ( n = 1), Symphalangus syndactylus ( n = 3), and Papio hamadryas ( n = 3). We identified statistically significant correlations in both humans and chimpanzees with slopes that displayed homogeneity of covariation. Joint prediction formulae were found to be compatible with humans and chimpanzees as well as all other African great apes, i.e., bonobos and gorillas. The main conclusion that can be drawn from this study is that regression models for approximating nasal projection are homogenous among humans and African apes and can thus be reasonably extended to ancestors leading to these clades.

Stress distribution in the bonobo (Pan paniscus) trapeziometacarpal joint during grasping

The primate thumb plays a central role in grasping and the basal trapeziometacarpal (TMC) joint is critical to its function. The TMC joint morphology varies across primates, yet little is known about form-function interaction within in the TMC joint. The purpose of this study was to investigate how stress distributions within the joint differ between five grasping types commonly employed by bonobos (Pan paniscus). Five cadaveric bonobo forearms were CT scanned in five standardized positions of the hand as a basis for the generation of parametric finite element models to compare grasps. We have developed a finite element analysis (FEA) approach to investigate stress distribution patterns in the TMC joint associated with each grasp type. We hypothesized that the simulated stress distributions for each position would correspond with the patterns expected from a saddle-shaped joint. However, we also expected differences in stress patterns arising from instraspecific variations in morphology. The models showed a high agreement between simulated and expected stress patterns for each of the five grasps (86% of successful simulations), while partially (52%) and fully (14%) diverging patterns were also encountered. We identified individual variations of key morphological features in the bonobo TMC joint that account for the diverging stress patterns and emphasized the effect of interindividual morphological variation on joint functioning. This study gives unprecedented insight in the form-function interactions in the TMC joint of the bonobo and provides an innovative FEA approach to modelling intra-articular stress distributions, a valuable tool for the study of the primate thumb biomechanics.

Evaluating the efficacy of a consumer-centric method for ecological sampling: Using bonobo (Pan paniscus) feeding patterns as an instrument for tropical forest characterization

1. Characteristics of food availability and distribution are a key component of a species ecology. Objective measurement of food resources, such as vegetation plot sampling, do not consider aspects of selection by the consumer and therefore may produce imprecise measures of availability. Further, in most animal ecology research, traditional ecological surveying often is time-intensive and supplementary to ongoing behavioral observation. We propose a method to integrate ecological sampling of an animal's environment into existing behavioral data collection systems by using the consumer as the surveyor. Here, we introduce the consumer-centric method (CCM) of assessing resource availability for its ability to measure food resource abundance, distribution, and dispersion. This method catalogues feeding locations observed during behavioral observation and uses aggregated data to characterize these ecological metrics. 2. We evaluated the CCM relative to traditional vegetation plot surveying using accumulated feeding locations across three years visited by a tropical frugivore, the bonobo (Pan paniscus), and compared it with data derived from over 200 vegetation plots across their 50km2+ home range. 3. We demonstrate that food species abundance estimates derived from the CCM are comparable to those derived from traditional vegetation plot sampling after approximately 600 observation days or 60 spatially explicit feeding locations. The agreement between the methods further improved when accounting for aspects of consumer selectivity in objective vegetation plot sampling (e.g., size minima). Estimates of density from CCM correlated with plot-derived estimates and were relatively insensitive to home range inclusion and other species characteristics, but were sensitive to sampling frequency (e.g., consumption frequency). Agreement between the methods in relative distribution of resources performed better across species than expected by chance, although measures of dispersion correlated poorly. 4. We demonstrate that while providing a robust measure to quantify local food availability, the CCM has an advantage over traditional sampling methods as it incorporates sampling biases relevant to the consumer. Therefore, as this method can be incorporated into existing observational data collection and does not require additional ecological surveying, it serves as a promising method for behavioral ecological data collection for animal species who re-use space and consume immobile food items.

The early bonobo gets the juice? The evolutionary roots of pre-crastination in bonobos (Pan paniscus)

This paper is to appear in Animal Behavior and Cognition. ----- Pre-crastination refers to the propensity to initiate tasks at the earliest possible moment. Research with human adults has found that some individuals consistently chose to transport a nearby object a further distance rather than delay initiation of the transport to select an object closer to the target. This phenomenon has never been tested in animals using analogous methods. Consequently, we tested bonobos – the species most closely related to humans - using two versions of a comparable transport task. Overall, we found that all five bonobos tended to select the first object they encountered to transport to the goal. Unlike humans, the bonobos sometimes transported both available objects. Two of the five bonobos consistently pre-crastinated, a similar proportion to that found in human experiments. However, if the pre-crastination choice was non-functional, the bonobos chose the motorically efficient choice. In sum, our findings provide an existence proof for pre-crastination tendencies in some bonobos, akin to the distribution of this trait in humans. We discuss the possibility that the pre-crastination choice represents an automatic response triggered by the affordances of the objects encountered.