Infanticide in Chimpanzees: Taphonomic Case Studies from Gombe

Objectives We present a study of skeletal damage to four chimpanzee (Pan troglodytes) infanticide victims from Gombe National Park, Tanzania. Skeletal analysis may provide insight into the adaptive significance of infanticide by examining whether nutritional benefits sufficiently explain infanticidal behavior. The nutritional hypothesis would be supported if bone survivorship rates and skeletal damage patterns are comparable to those of monkey prey. If not, other explanations, such as the resource competition hypothesis, should be considered. Methods Taphonomic assessment of two chimpanzee infants included description of breakage and surface modification, data on MNE, %MNE, and bone survivorship. Two additional infants were assessed qualitatively. The data were compared to published information on monkey prey. We also undertook a review of published infanticide cases. Results The cases were intercommunity infanticides (one male and three female infants) committed by males. Attackers partially consumed two of the victims. Damage to all four infants included puncture marks and compression fractures to the cranium, crenulated breaks to long bones, and incipient fractures on ribs. Compared to monkey prey, the chimpanzee infants had an abundance of vertebrae and hand/foot bones. Conclusions The cases described here suggest that chimpanzees may not always completely consume infanticide victims, while reports on chimpanzee predation indicated that complete consumption of monkey prey usually occurred. Infanticidal chimpanzees undoubtedly gain nutritional benefits when they consume dead infants, but this benefit may not sufficiently explain infanticide in this species. Continued study of infanticidal and hunting behavior, including skeletal analysis, is likely to be of interest

CHIIMP: An automated high-throughput microsatellite genotyping approach reveals greater allelic diversity in wild chimpanzees

Short tandem repeats (STRs), also known as microsatellites, are commonly used to non invasively genotype wild-living endangered species, including African apes. Until recently, capillary electrophoresis has been the method of choice to determine the length of polymorphic STR loci. However, this technique is labor intensive, difficult to compare across platforms, and notoriously imprecise. Here we developed a MiSeq-based approach and tested its performance using previously genotyped fecal samples from long-term studied chimpanzees in Gombe National Park, Tanzania. Using data from eight microsatellite loci as a reference, we designed a bioinformatics platform that converts raw MiSeq reads into locus-specific files and automatically calls alleles after filtering stutter sequences and other PCR artifacts. Applying this method to the entire Gombe population, we confirmed previously reported genotypes, but also identified 31 new alleles that had been missed due to sequence differences and size homoplasy. The new genotypes, which increased the allelic diversity and heterozygosity in Gombe by 61% and 8%, respectively, were validated by replicate amplification and pedigree analyses. This demonstrated inheritance and resolved one case of an ambiguous paternity. Using both singleplex and multiplex locus amplification, we also genotyped fecal samples from chimpanzees in the Greater Mahale Ecosystem in Tanzania, demonstrating the utility of the MiSeq-based approach for genotyping non-habituated populations and performing comparative analyses across field sites. The new automated high-throughput analysis platform (available at https://github.com/ShawHahnLab/chiimp) will allow biologists to more accurately and effectively determine wildlife population size and structure, and thus obtain information critical for conservation efforts

Prevalence and correlates of partner violence among adolescent girls and young women: Evidence from baseline data of a cluster randomised trial in Tanzania.

BACKGROUND: Little has been documented about partner violence among adolescent girls and young women (AGYW) who are out of school, a factor associated with HIV acquisition. To understand areas for prioritising HIV prevention intervention efforts, we explored the prevalence and correlates of partner violence among out of school AGYW in Shinyanga, Tanzania. METHODS: A cross-sectional analysis of data from AGYW aged 15-23 years recruited in a cluster randomised trial conducted between October and December 2017 was used to examine correlates of partner violence. Data were collected through an Audio Computer-Assisted Self-interview. Multivariate logistic regression analysis was used to evaluate the association. RESULTS: 2276 (75.5%) AGYW were sexually active. Of these, 816 (35.9%) reported having experienced violence from partners in the last six months. After adjusting for other covariates, being formerly married (AOR = 1.55, 95% CI:1.02, 2.37), having children (AOR = 1.79, 95% CI:1.47, 2.16), anxiety and depression symptoms (AOR = 3.27, 95%CI: 2.15, 4.96), having engaged in sex work in the past six months (AOR = 1.92, 95% CI: 1.45, 2.53) and economic deprivation (AOR = 1.61, 95% CI: 1.34,1.92) were significantly associated with partner violence. CONCLUSIONS: Almost one in three sexually active AGYW had experienced partner violence in the 6 months preceding the survey. The findings underscore the need for future research to focus on understanding the reasons and dynamics underlying high level of partner violence among AGYW. Furthermore, there is a need for implementing intervention programs that aim to reduce economic deprivation among AGYWs and address social norms and structures perpetuating violence against AGYW. TRIAL REGISTRATION: ClinicalTrials.gov-ID NCT03597243

Cash Transfer to Adolescent Girls and Young Women to Reduce Sexual Risk Behavior (CARE): Protocol for a Cluster Randomized Controlled Trial.

BACKGROUND: The HIV epidemic in Eastern and Southern Africa is characterized by a high incidence and prevalence of HIV infection among adolescent girls and young women (AGYW) aged 15-24 years. For instance, in some countries, HIV prevalence in AGYW aged 20-24 years exceeds that in AGYW aged 15-19 years by 2:1. Sauti (meaning voices), a project supported by the United States Agency for International Development, is providing HIV combination prevention interventions to AGYW in the Shinyanga region, Tanzania. OBJECTIVE: The aim of this study is to determine the impact of cash transfer on risky sexual behavior among AGYW receiving cash transfer and HIV combination prevention interventions. This paper describes the research methods and general protocol of the study. Risky sexual behavior will be assessed by herpes simplex virus type 2 (HSV-2) incidence, compensated sex (defined as sexual encounters motivated by exchange for money, material support, or other benefits), and intergenerational sex (defined as a sexual partnership between AGYW and a man 10 or more years older). Through a qualitative study, the study seeks to understand how the intervention affects the structural and behavioral drivers of the HIV epidemic. METHODS: The trial employs audio computer-assisted self-interviewing, participatory group discussions (PGDs), and case studies to collect data. A total of 30 matched villages (15 intervention and 15 control clusters) were randomized to either receive cash transfer delivered over 18 months in addition to other HIV interventions (intervention arm) or to receive other HIV interventions without cash transfer (control arm). Study participants are interviewed at baseline and 6, 12, and 18 months to collect data on demographics, factors related to HIV vulnerabilities, family planning, sexual risk behavior, gender-based violence, and HSV-2 and HIV infections. A total of 6 PGDs (3 intervention, 3 control) were conducted at baseline to describe perceptions and preferences of different intervention packages, whereas 20 case studies are used to monitor and unearth the dynamics involved in delivery and uptake of cash transfer. RESULTS: The study was funded in June 2017; enrollment took place in December 2017. A total of two rounds of the follow-up survey are complete, and one round has yet to be conducted. The results are expected in December 2019 and will be disseminated through conferences and peer-reviewed publications. CONCLUSIONS: This study will document the synergetic impact of cash transfer in the presence of HIV combination prevention interventions on risky sexual behavior among out-of-school AGYW. The results will strengthen the evidence of cash transfer in the reduction of risky sexual behavior and provide feasible HIV prevention strategies for AGYW. TRIAL REGISTRATION: Clinicaltrials.gov NCT03597243; https://clinicaltrials.gov/ct2/show/NCT03597243. INTERNATIONAL REGISTERED REPORT IDENTIFIER (IRRID): DERR1-10.2196/14696

Allometry and Ecology of the Bilaterian Gut Microbiome.

Classical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed. Here, we investigated the influence of several well-known ecological principles on animal-associated microbiota by characterizing gut microbial specimens from bilaterally symmetrical animals (Bilateria) ranging from flies to whales. A rigorously vetted sample set containing 265 specimens from 64 species was assembled. Bacterial lineages were characterized by 16S rRNA gene sequencing. Previously published samples were also compared, allowing analysis of over 1,098 samples in total. A restricted number of bacterial phyla was found to account for the great majority of gut colonists. Gut microbial composition was associated with host phylogeny and diet. We identified numerous gut bacterial 16S rRNA gene sequences that diverged deeply from previously studied taxa, identifying opportunities to discover new bacterial types. The number of bacterial lineages per gut sample was positively associated with animal mass, paralleling known species-area relationships from island biogeography and implicating body size as a determinant of community stability and niche complexity. Samples from larger animals harbored greater numbers of anaerobic communities, specifying a mechanism for generating more-complex microbial environments. Predictions for species/abundance relationships from models of neutral colonization did not match the data set, pointing to alternative mechanisms such as selection of specific colonists by environmental niche. Taken together, the data suggest that niche complexity increases with gut size and that niche selection forces dominate gut community construction.IMPORTANCEThe intestinal microbiome of animals is essential for health, contributing to digestion of foods, proper immune development, inhibition of pathogen colonization, and catabolism of xenobiotic compounds. How these communities assemble and persist is just beginning to be investigated. Here we interrogated a set of gut samples from a wide range of animals to investigate the roles of selection and random processes in microbial community construction. We show that the numbers of bacterial species increased with the weight of host organisms, paralleling findings from studies of island biogeography. Communities in larger organisms tended to be more anaerobic, suggesting one mechanism for niche diversification. Nonselective processes enable specific predictions for community structure, but our samples did not match the predictions of the neutral model. Thus, these findings highlight the importance of niche selection in community construction and suggest mechanisms of niche diversification

Barriers to chimpanzee gene flow at the south-east edge of their distribution.

Populations on the edge of a species' distribution may represent an important source of adaptive diversity, yet these populations tend to be more fragmented and are more likely to be geographically isolated. Lack of genetic exchanges between such populations, due to barriers to animal movement, can not only compromise adaptive potential but also lead to the fixation of deleterious alleles. The south-eastern edge of chimpanzee distribution is particularly fragmented, and conflicting hypotheses have been proposed about population connectivity and viability. To address this uncertainty, we generated both mitochondrial and MiSeq-based microsatellite genotypes for 290 individuals ranging across western Tanzania. While shared mitochondrial haplotypes confirmed historical gene flow, our microsatellite analyses revealed two distinct clusters, suggesting two populations currently isolated from one another. However, we found evidence of high levels of gene flow maintained within each of these clusters, one of which covers an 18,000 km2 ecosystem. Landscape genetic analyses confirmed the presence of barriers to gene flow with rivers and bare habitats highly restricting chimpanzee movement. Our study demonstrates how advances in sequencing technologies, combined with the development of landscape genetics approaches, can resolve ambiguities in the genetic history of critical populations and better inform conservation efforts of endangered species

Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics

Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. Habituated (Mitumba and Kasekela) and non-habituated (Kalande) chimpanzees were studied in Gombe National Park, Tanzania. Ape population sizes were determined from demographic records (Mitumba and Kasekela) or individual sightings and genotyping (Kalande), while SIVcpz prevalence rates were monitored using non-invasive methods. Between 2002–2009, the Mitumba and Kasekela communities experienced mean annual growth rates of 1.9% and 2.4%, respectively, while Kalande chimpanzees suffered a significant decline, with a mean growth rate of −6.5% to −7.4%, depending on population estimates. A rapid decline in Kalande was first noted in the 1990s and originally attributed to poaching and reduced food sources. However, between 2002–2009, we found a mean SIVcpz prevalence in Kalande of 46.1%, which was almost four times higher than the prevalence in Mitumba (12.7%) and Kasekela (12.1%). To explore whether SIVcpz contributed to the Kalande decline, we used empirically determined SIVcpz transmission probabilities as well as chimpanzee mortality, mating and migration data to model the effect of viral pathogenicity on chimpanzee population growth. Deterministic calculations indicated that a prevalence of greater than 3.4% would result in negative growth and eventual population extinction, even using conservative mortality estimates. However, stochastic models revealed that in representative populations, SIVcpz, and not its host species, frequently went extinct. High SIVcpz transmission probability and excess mortality reduced population persistence, while intercommunity migration often rescued infected communities, even when immigrating females had a chance of being SIVcpz infected. Together, these results suggest that the decline of the Kalande community was caused, at least in part, by high levels of SIVcpz infection. However, population extinction is not an inevitable consequence of SIVcpz infection, but depends on additional variables, such as migration, that promote survival. These findings are consistent with the uneven distribution of SIVcpz throughout central Africa and explain how chimpanzees in Gombe and elsewhere can be at equipoise with this pathogen

Allometry and Ecology of the Bilaterian Gut Microbiome

Classical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed. Here, we investigated the influence of several well-known ecological principles on animal-associated microbiota by characterizing gut microbial specimens from bilaterally symmetrical animals (Bilateria) ranging from flies to whales. A rigorously vetted sample set containing 265 specimens from 64 species was assembled. Bacterial lineages were characterized by 16S rRNA gene sequencing. Previously published samples were also compared, allowing analysis of over 1,098 samples in total. A restricted number of bacterial phyla was found to account for the great majority of gut colonists. Gut microbial composition was associated with host phylogeny and diet. We identified numerous gut bacterial 16S rRNA gene sequences that diverged deeply from previously studied taxa, identifying opportunities to discover new bacterial types. The number of bacterial lineages per gut sample was positively associated with animal mass, paralleling known species-area relationships from island biogeography and implicating body size as a determinant of community stability and niche complexity. Samples from larger animals harbored greater numbers of anaerobic communities, specifying a mechanism for generating more-complex microbial environments. Predictions for species/abundance relationships from models of neutral colonization did not match the data set, pointing to alternative mechanisms such as selection of specific colonists by environmental niche. Taken together, the data suggest that niche complexity increases with gut size and that niche selection forces dominate gut community construction