Ethical futures in biological anthropology: Research, teaching, community engagement, and curation involving deceased individuals.

Although ethical reforms in biological anthropology have gained ground in recent years, there is still a scarcity of ethical standards for work involving historical documented collections (HDCs) at US museums and universities. These collections of deceased individuals were created in the late 19th to mid-20th centuries under anatomy laws that targeted socially marginalized communities and allowed for the dissection of these individuals without their consent. Due to the extensive information associated with the individuals and made available to researchers, these collections have served as foundational resources for theory and methods development in biological anthropology into the 21st century. Recognizing the need for ethical guidelines for research, teaching and training, community engagement, and curation involving HDCs, we held a workshop called "Ethical Futures for Curation, Research, and Teaching in Biological Anthropology" on November 15-17, 2021. Here we summarize the conversations and major points of consensus among the workshop participants on these topics in order to advance these ethical considerations more broadly across the field.

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.

Uncovering the Holocene roots of contemporary disease-scapes: bringing archaeology into One Health.

The accelerating pace of emerging zoonotic diseases in the twenty-first century has motivated cross-disciplinary collaboration on One Health approaches, combining microbiology, veterinary and environmental sciences, and epidemiology for outbreak prevention and mitigation. Such outbreaks are often caused by spillovers attributed to human activities that encroach on wildlife habitats and ecosystems, such as land use change, industrialized food production, urbanization and animal trade. While the origin of anthropogenic effects on animal ecology and biogeography can be traced to the Late Pleistocene, the archaeological record-a long-term archive of human-animal-environmental interactions-has largely been untapped in these One Health approaches, thus limiting our understanding of these dynamics over time. In this review, we examine how humans, as niche constructors, have facilitated new host species and 'disease-scapes' from the Late Pleistocene to the Anthropocene, by viewing zooarchaeological, bioarchaeological and palaeoecological data with a One Health perspective. We also highlight how new biomolecular tools and advances in the '-omics' can be holistically coupled with archaeological and palaeoecological reconstructions in the service of studying zoonotic disease emergence and re-emergence.

The Many Hosts of Mycobacteria 9 (MHM9): A conference report.

The Many Hosts of Mycobacteria (MHM) meeting series brings together basic scientists, clinicians and veterinarians to promote robust discussion and dissemination of recent advances in our knowledge of numerous mycobacterial diseases, including human and bovine tuberculosis (TB), nontuberculous mycobacteria (NTM) infection, Hansen's disease (leprosy), Buruli ulcer and Johne's disease. The 9th MHM conference (MHM9) was held in July 2022 at The Ohio State University (OSU) and centered around the theme of "Confounders of Mycobacterial Disease." Confounders can and often do drive the transmission of mycobacterial diseases, as well as impact surveillance and treatment outcomes. Various confounders were presented and discussed at MHM9 including those that originate from the host (comorbidities and coinfections) as well as those arising from the environment (e.g., zoonotic exposures), economic inequality (e.g. healthcare disparities), stigma (a confounder of leprosy and TB for millennia), and historical neglect (a confounder in Native American Nations). This conference report summarizes select talks given at MHM9 highlighting recent research advances, as well as talks regarding the historic and ongoing impact of TB and other infectious diseases on Native American Nations, including those in Southwestern Alaska where the regional TB incidence rate is among the highest in the Western hemisphere.

Earliest evidence of primate captivity and translocation supports gift diplomacy between Teotihuacan and the Maya.

A multimethod archaeometry study (zooarchaeological, isotopic, ancient DNA, paleobotanical, and radiocarbon dating) of a spider monkey sacrificed in the ceremonial center of Teotihuacan, Mexico (1 to 550 CE) is interpreted as a diplomatic gift exchange with neighboring Maya. Not only does this spider monkey provide the earliest known instance of primate translocation and captivity in Mesoamerica, it helps date incipient modes of interregional diplomacy between two major powers during Early Classic Mesoamerica: Teotihuacan and the Maya. Details of human-primate interaction include age at capture and transport (before ∼3 y of age), captive duration (over 2 y), anthropogenic diet (staple was maize, though secondary resources unique to anthropogenic diet including arrowroot and chili pepper were also found), context of sacrifice (tethered and associated with complete golden eagle and an array of other statecrafts), and general site context (including presence of Maya vessels and Maya-style murals). The timing of the spider monkey's sacrifice (250 to 300 CE) and its life history suggest a reconsideration of epigraphically attested militaristic involvement of Teotihuacan at certain Maya sites. We propose that a period of more multilateral and fluid ritual exchange with Maya dignitaries preceded the Teotihuacan state's eventual ascent to prominence.

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.

Indigenous oyster fisheries persisted for millennia and should inform future management.

Historical ecology has revolutionized our understanding of fisheries and cultural landscapes, demonstrating the value of historical data for evaluating the past, present, and future of Earth's ecosystems. Despite several important studies, Indigenous fisheries generally receive less attention from scholars and managers than the 17th-20th century capitalist commercial fisheries that decimated many keystone species, including oysters. We investigate Indigenous oyster harvest through time in North America and Australia, placing these data in the context of sea level histories and historical catch records. Indigenous oyster fisheries were pervasive across space and through time, persisting for 5000-10,000 years or more. Oysters were likely managed and sometimes "farmed," and are woven into broader cultural, ritual, and social traditions. Effective stewardship of oyster reefs and other marine fisheries around the world must center Indigenous histories and include Indigenous community members to co-develop more inclusive, just, and successful strategies for restoration, harvest, and management.

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.

The gut microbiome buffers dietary adaptation in Bronze Age domesticated dogs.

In an attempt to explore the role of the gut microbiome during recent canine evolutionary history, we sequenced the metagenome of 13 canine coprolites dated ca. 3,600-3,450 years ago from the Bronze Age archaeological site of Solarolo (Italy), which housed a complex farming community. The microbiome structure of Solarolo dogs revealed continuity with that of modern dogs, but it also shared some features with the wild wolf microbiome, as a kind of transitional state between them. The dietary niche, as also inferred from the microbiome composition, was omnivorous, with evidence of consumption of starchy agricultural foods. Of interest, the Solarolo dog microbiome was particularly enriched in sequences encoding alpha-amylases and complemented a low copy number of the host amylase gene. These findings suggest that Neolithic dogs could have responded to the transition to a starch-rich diet by expanding microbial functionalities devoted to starch catabolism, thus compensating for delayed host response.

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.

Components of a Neanderthal gut microbiome recovered from fecal sediments from El Salt.

A comprehensive view of our evolutionary history cannot ignore the ancestral features of our gut microbiota. To provide some glimpse into the past, we searched for human gut microbiome components in ancient DNA from 14 archeological sediments spanning four stratigraphic units of El Salt Middle Paleolithic site (Spain), including layers of unit X, which has yielded well-preserved Neanderthal occupation deposits dating around 50 kya. According to our findings, bacterial genera belonging to families known to be part of the modern human gut microbiome are abundantly represented only across unit X samples, showing that well-known beneficial gut commensals, such as Blautia, Dorea, Roseburia, Ruminococcus, Faecalibacterium and Bifidobacterium already populated the intestinal microbiome of Homo since as far back as the last common ancestor between humans and Neanderthals.

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.

Biogeographic problem-solving reveals the Late Pleistocene translocation of a short-faced bear to the California Channel Islands.

An accurate understanding of biodiversity of the past is critical for contextualizing biodiversity patterns and trends in the present. Emerging techniques are refining our ability to decipher otherwise cryptic human-mediated species translocations across the Quaternary, yet these techniques are often used in isolation, rather than part of an interdisciplinary hypothesis-testing toolkit, limiting their scope and application. Here we illustrate the use of such an integrative approach and report the occurrence of North America's largest terrestrial mammalian carnivore, the short-faced bear, Arctodus simus, from Daisy Cave (CA-SMI-261), an important early human occupation site on the California Channel Islands. We identified the specimen by corroborating morphological, protein, and mitogenomic lines of evidence, and evaluated the potential natural and anthropogenic mechanisms of its transport and deposition. While representing just a single specimen, our combination of techniques opened a window into the behavior of an enigmatic species, suggesting that A. simus was a wide-ranging scavenger utilizing terrestrial and marine carcasses. This discovery highlights the utility of bridging archaeological and paleontological datasets to disentangle complex biogeographic scenarios and reveal unexpected biodiversity for island systems worldwide.

Maritime Paleoindian technology, subsistence, and ecology at an ~11,700 year old Paleocoastal site on California's Northern Channel Islands, USA.

During the last 10 years, we have learned a great deal about the potential for a coastal peopling of the Americas and the importance of marine resources in early economies. Despite research at a growing number of terminal Pleistocene archaeological sites on the Pacific Coast of the Americas, however, important questions remain about the lifeways of early Paleocoastal peoples. Research at CA-SRI-26, a roughly 11,700 year old site on California's Santa Rosa Island, provides new data on Paleoindian technologies, subsistence strategies, and seasonality in an insular maritime setting. Buried beneath approximately two meters of alluvium, much of the site has been lost to erosion, but its remnants have produced chipped stone artifacts (crescents and Channel Island Amol and Channel Island Barbed points) diagnostic of early island Paleocoastal components. The bones of waterfowl and seabirds, fish, and marine mammals, along with small amounts of shellfish document a diverse subsistence strategy. These data support a relatively brief occupation during the wetter "winter" season (late fall to early spring), in an upland location several km from the open coast. When placed in the context of other Paleocoastal sites on the Channel Islands, CA-SRI-26 demonstrates diverse maritime subsistence strategies and a mix of seasonal and more sustained year-round island occupations. Our results add to knowledge about a distinctive island Paleocoastal culture that appears to be related to Western Stemmed Tradition sites widely scattered across western North America.

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.

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.

Comparison of extraction methods for recovering ancient microbial DNA from paleofeces.

OBJECTIVES: Paleofeces are valuable to archeologists and evolutionary biologists for their potential to yield health, dietary, and host information. As a rich source of preserved biomolecules from host-associated microorganisms, they can also provide insights into the recent evolution and changing ecology of the gut microbiome. However, there is currently no standard method for DNA extraction from paleofeces, which combine the dual challenges of complex biological composition and degraded DNA. Due to the scarcity and relatively poor preservation of paleofeces when compared with other archeological remains, it is important to use efficient methods that maximize ancient DNA (aDNA) recovery while also minimizing downstream taxonomic biases. METHODS: In this study, we use shotgun metagenomics to systematically compare the performance of five DNA extraction methods on a set of well-preserved human and dog paleofeces from Mexico (~1,300 BP). RESULTS: Our results show that all tested DNA extraction methods yield a consistent microbial taxonomic profile, but that methods optimized for ancient samples recover significantly more DNA. CONCLUSIONS: These results show promise for future studies that seek to explore the evolution of the human gut microbiome by comparing aDNA data with those generated in modern studies.