The evolution and changing ecology of the African hominid oral microbiome.

The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

Archaeological mitogenomes illuminate the historical ecology of sea otters (Enhydra lutris) and the viability of reintroduction.

Genetic analyses are an important contribution to wildlife reintroductions, particularly in the modern context of extirpations and ecological destruction. To address the complex historical ecology of the sea otter (Enhydra lutris) and its failed 1970s reintroduction to coastal Oregon, we compared mitochondrial genomes of pre-extirpation Oregon sea otters to extant and historical populations across the range. We sequenced, to our knowledge, the first complete ancient mitogenomes from archaeological Oregon sea otter dentine and historical sea otter dental calculus. Archaeological Oregon sea otters (n = 20) represent 10 haplotypes, which cluster with haplotypes from Alaska, Washington and British Columbia, and exhibit a clear division from California haplotypes. Our results suggest that extant northern populations are appropriate for future reintroduction efforts. This project demonstrates the feasibility of mitogenome capture and sequencing from non-human dental calculus and the diverse applications of ancient DNA analyses to pressing ecological and conservation topics and the management of at-risk/extirpated species.

A chomped chimp: New evidence of tooth marks on an adult chimpanzee (Pan troglodytes verus).

OBJECTIVES: To describe and interpret previously unreported marks on the dry cranium of an adult chimpanzee (Pan troglodytes verus) from Côte d'Ivoire at the Smithsonian's National Museum of Natural History (USNM 450071). MATERIALS AND METHODS: All marks on the cranium were documented and assessed through physical examination of the specimen, photography, micro-computed tomography (micro-CT), and 3D laser scanning. Pits and punctures were measured with digital calipers for comparison with published carnivore tooth mark measurements. RESULTS: The cranium shows perimortem or postmortem damage to the temporal, occipital, and maxillary regions that is not recent. Size and color variation in the marks suggest two damage events, possibly involving chewing by different animals, at least one of which was a large-bodied mammal. The 22 tooth pits and punctures (0.89-8.75 mm in maximum length and 0.88-6.63 mm in breadth) overlap in size with those inflicted by wild leopards, the most significant predators of common chimpanzees due to their largely overlapping ecological distributions. CONCLUSIONS: Based on qualitative and quantitative evidence, we conclude that leopards are the most likely cause of the most prominent marks on the cranium. However, we cannot rule out the additional possibility of other chimpanzees, although there are no published studies of chimpanzee tooth marks for direct comparison. This study is the most extensive documentation to date of a modern adult chimpanzee skull exhibiting tooth marks by a large mammal, thus providing new evidence to help identify and interpret other events of predation and scavenging of large-bodied apes in the modern and fossil records.

Exercises in ethically engaged work in biological anthropology.

An ethical paradigm shift currently taking place within biological anthropology is pushing scholars to envisage and develop paths toward more ethical futures. Drawing from case studies in our own teaching, research, and fieldwork experience, we reflect on the complex, diverse, and dynamic nature of ethical considerations in our field. We discuss the acquisition and institutional narrative of a human osteological teaching collection at the University of Louisville as an embodiment of structural apathy turned structural violence, and the need for professional guidance in the potential retirement of deceased individuals from our classrooms. In documented collections (i.e., the Robert J. Terry Collection), we share our process and scholarly reemphasis of the humanity of a deceased individual through contextualized analysis (i.e., osteobiography and archival history) and postmortem agentive acts. Lastly, we present an archeological site in the U.S. Virgin Islands, which poses ethical concerns as biocultural bioarcheologists and archeologists attempt to negotiate the possible wishes of the deceased with the cultural value of reconstructing the community's otherwise undocumented past, all amidst the immediate threat of anthropogenic climate change. We offer these exercises and discussion in ethically engaged projects transparently and with an overarching admission that none are models for replication. Rather, at various stages in our careers and engagement with ethics, we acknowledge that progress is worthwhile, albeit challenging, and that proceeding forward collectively as biological anthropologists should be deliberate, reflexive, and compassionate for deceased individuals and their descendant communities, as well as among and between colleagues.

Metagenomic and paleopathological analyses of a historic documented collection explore ancient dental calculus as a diagnostic tool.

Dental calculus is a microbial biofilm that contains biomolecules from oral commensals and pathogens, including those potentially related to cause of death (CoD). To assess the utility of calculus as a diagnostically informative substrate, in conjunction with paleopathological analysis, calculus samples from 39 individuals in the Smithsonian Institution's Robert J. Terry Collection with CoDs of either syphilis or tuberculosis were assessed via shotgun metagenomic sequencing for the presence of Treponema pallidum subsp. pallidum and Mycobacterium tuberculosis complex (MTBC) DNA. Paleopathological analysis revealed that frequencies of skeletal lesions associated with these diseases were partially inconsistent with diagnostic criteria. Although recovery of T. p. pallidum DNA from individuals with a syphilis CoD was elusive, MTBC DNA was identified in at least one individual with a tuberculosis CoD. The authenticity of MTBC DNA was confirmed using targeted quantitative PCR assays, MTBC genome enrichment, and in silico bioinformatic analyses; however, the lineage of the MTBC strain present could not be determined. Overall, our study highlights the utility of dental calculus for molecular detection of tuberculosis in the archaeological record and underscores the effect of museum preparation techniques and extensive handling on pathogen DNA preservation in skeletal collections.

Complete mitochondrial genome of the Galápagos sea lion, Zalophuswollebaeki (Carnivora, Otariidae): paratype specimen confirms separate species status.

The endangered Galápagos sea lion (Zalophuswollebaeki) inhabits the Galápagos Islands off the coast of Ecuador. We present a complete mitochondrial genome (16 465 bp) of a female paratype from the collections of the Natural History Museum Oslo, Norway, assembled from next-generation sequencing reads. It contains all canonical protein-coding, rRNA, tRNA genes, and the D-loop region. Sequence similarity is 99.93% to a previously published conspecific mitogenome sequence and 99.37% to the mitogenome sequence of the sister species Z.californianus. Sequence similarity of the D-loop region of the Z.wollebaeki paratype mitogenome is >99%, while the sequence difference to the Z.californianus sequences exceeds 2.5%. The paratype mitogenome sequence supports the taxonomic status of Z.wollebaeki as a separate species.

Oral metagenomes from Native American Ancestors reveal distinct microbial lineages in the pre-contact era.

OBJECTIVES: Limited studies have focused on how European contact and colonialism impacted Native American oral microbiomes, specifically, the diversity of commensal or opportunistically pathogenic oral microbes, which may be associated with oral diseases. Here, we studied the oral microbiomes of pre-contact Wichita Ancestors, in partnership with the Descendant community, The Wichita and Affiliated Tribes, Oklahoma, USA. MATERIALS AND METHODS: Skeletal remains of 28 Wichita Ancestors from 20 archeological sites (dating approximately to 1250-1450 CE) were paleopathologically assessed for presence of dental calculus and oral disease. DNA was extracted from calculus, and partial uracil deglycosylase-treated double-stranded DNA libraries were shotgun-sequenced using Illumina technology. DNA preservation was assessed, the microbial community was taxonomically profiled, and phylogenomic analyzes were conducted. RESULTS: Paleopathological analysis revealed signs of oral diseases such as caries and periodontitis. Calculus samples from 26 Ancestors yielded oral microbiomes with minimal extraneous contamination. Anaerolineaceae bacterium oral taxon 439 was found to be the most abundant bacterial species. Several Ancestors showed high abundance of bacteria typically associated with periodontitis such as Tannerella forsythia and Treponema denticola. Phylogenomic analyzes of Anaerolineaceae bacterium oral taxon 439 and T. forsythia revealed biogeographic structuring; strains present in the Wichita Ancestors clustered with strains from other pre-contact Native Americans and were distinct from European and/or post-contact American strains. DISCUSSION: We present the largest oral metagenome dataset from a pre-contact Native American population and demonstrate the presence of distinct lineages of oral microbes specific to the pre-contact Americas.

Remembering St. Louis individual-structural violence and acute bacterial infections in a historical anatomical collection.

Incomplete documentary evidence, variable biomolecular preservation, and limited skeletal responses have hindered assessment of acute infections in the past. This study was initially developed to explore the diagnostic potential of dental calculus to identify infectious diseases, however, the breadth and depth of information gained from a particular individual, St. Louis Individual (St.LI), enabled an individualized assessment and demanded broader disciplinary introspection of ethical research conduct. Here, we document the embodiment of structural violence in a 23-year-old Black and/or African American male, who died of lobar pneumonia in 1930s St. Louis, Missouri. St.LI exhibits evidence of systemic poor health, including chronic oral infections and a probable tuberculosis infection. Metagenomic sequencing of dental calculus recovered three pre-antibiotic era pathogen genomes, which likely contributed to the lobar pneumonia cause of death (CoD): Klebsiella pneumoniae (13.8X); Acinetobacter nosocomialis (28.4X); and Acinetobacter junii (30.1X). Ante- and perimortem evidence of St.LI's lived experiences chronicle the poverty, systemic racism, and race-based structural violence experienced by marginalized communities in St. Louis, which contributed to St.LI's poor health, CoD, anatomization, and inclusion in the Robert J. Terry Anatomical Collection. These same embodied inequalities continue to manifest as health disparities affecting many contemporary communities in the United States.

What does it mean to be wild? Assessing human influence on the environments of nonhuman primate specimens in museum collections.

OBJECTIVES: Natural history collections are often thought to represent environments in a pristine natural state-free from human intervention-the so-called "wild." In this study, we aim to assess the level of human influence represented by natural history collections of wild-collected primates over 120 years at the Smithsonian Institution's National Museum of Natural History (NMNH). MATERIALS AND METHODS: Our sample consisted of 875 catarrhine primate specimens in NMNH collections, representing 13 genera collected in 39 countries from 1882 to 2004. Using archival and accession information we determined the approximate locations from which specimens were collected. We then plotted location coordinates onto publicly available anthrome maps created by Ellis et al. (Global Ecology and Biogeography, 2010, 19, 589), which delineate terrestrial biomes of human population density and land use worldwide since the 1700s. RESULTS: We found that among primates collected from their native ranges, 92% were from an environment that had some level of human impact, suggesting that the majority of presumed wild-collected primate specimens lived in an environment influenced by humans during their lifetimes. DISCUSSION: The degree to which human-modified environments may have impacted the lives of primates currently held in museum collections has been historically ignored, implicating unforeseen consequences for collection-based research. While unique effects related to commensalism with humans remain understudied, effects currently attributed to natural phenomena may, in fact, be related to anthropogenic pressures on unmanaged populations of primates.

Population-level assessment of atlas occipitalization in artificially modified crania from pre-Hispanic Peru.

Atlas occipitalization (AO) is a spinal anomaly, characterized by the fusion of the first cervical vertebra and occipital bone, with a complex etiology that can arise from congenital and environmental causes. AO has been reported in three regions of pre-Hispanic Peru in skeletal remains with artificial cranial modification (ACM), which involves the use of compression devices to permanently alter cranial shape and may have affected the fusion of the atlas and occipital bone. The aims of this study were to gain insights into AO's etiology by testing correlations between AO and ACM presence/type and geographic region as well as to characterize morphological variation associated with AO. We investigated the geographic distribution of AO and its potential relationship to ACM in a large sample of human crania from eight coastal and highland regions of pre-Hispanic Peru, held at the Smithsonian's National Museum of Natural History (n = 608, 1300-1500 CE). Eleven cases of AO were observed in three coastal regions-including two previously unreported regions-at an overall frequency of 1.8%. The frequency of AO did not differ significantly between crania with and without ACM, in general or by type, suggesting that ACM is not an etiological factor that influences AO in this sample. AO was observed at a significantly higher rate in the southern coastal region of Arequipa than in any other region. Genetic, dietary, and epidemiological conditions are evaluated as factors possibly shaping the geographic distribution of AO along the central and southern coasts of Peru.