Redefining the treponemal history through pre-Columbian genomes from Brazil.

The origins of treponemal diseases have long remained unknown, especially considering the sudden onset of the first syphilis epidemic in the late 15th century in Europe and its hypothesized arrival from the Americas with Columbus' expeditions1,2. Recently, ancient DNA evidence has revealed various treponemal infections circulating in early modern Europe and colonial-era Mexico3-6. However, there has been to our knowledge no genomic evidence of treponematosis recovered from either the Americas or the Old World that can be reliably dated to the time before the first trans-Atlantic contacts. Here, we present treponemal genomes from nearly 2,000-year-old human remains from Brazil. We reconstruct four ancient genomes of a prehistoric treponemal pathogen, most closely related to the bejel-causing agent Treponema pallidum endemicum. Contradicting the modern day geographical niche of bejel in the arid regions of the world, the results call into question the previous palaeopathological characterization of treponeme subspecies and showcase their adaptive potential. A high-coverage genome is used to improve molecular clock date estimations, placing the divergence of modern T. pallidum subspecies firmly in pre-Columbian times. Overall, our study demonstrates the opportunities within archaeogenetics to uncover key events in pathogen evolution and emergence, paving the way to new hypotheses on the origin and spread of treponematoses.

Genomic history of coastal societies from eastern South America.

Sambaqui (shellmound) societies are among the most intriguing archaeological phenomena in pre-colonial South America, extending from approximately 8,000 to 1,000 years before present (yr BP) across 3,000 km on the Atlantic coast. However, little is known about their connection to early Holocene hunter-gatherers, how this may have contributed to different historical pathways and the processes through which late Holocene ceramists came to rule the coast shortly before European contact. To contribute to our understanding of the population history of indigenous societies on the eastern coast of South America, we produced genome-wide data from 34 ancient individuals as early as 10,000 yr BP from four different regions in Brazil. Early Holocene hunter-gatherers were found to lack shared genetic drift among themselves and with later populations from eastern South America, suggesting that they derived from a common radiation and did not contribute substantially to later coastal groups. Our analyses show genetic heterogeneity among contemporaneous Sambaqui groups from the southeastern and southern Brazilian coast, contrary to the similarity expressed in the archaeological record. The complex history of intercultural contact between inland horticulturists and coastal populations becomes genetically evident during the final horizon of Sambaqui societies, from around 2,200 yr BP, corroborating evidence of cultural change.

The diet at the onset of the Andean Civilization: New stable isotope data from Caral and Áspero, North-Central Coast of Peru.

OBJECTIVES: The subsistence system of the first urban centers with monumental architecture from the North-Central Coast of Peru, the core area for the social complexity process of Central Andes, has been debated since the late 1960s. To shed light on this aspect, we report paleodietary data from the two most important sites of the Supe Valley: Caral (3000-200 BC), the major settlement of the middle valley, and Áspero (3000-1800 BC), a notable coastal settlement. Our main objective was to test the Maritime Foundations of Andean Civilization hypothesis. MATERIALS AND METHODS: Stable isotope values (δ13 Ccol , δ13 Cap , and δ15 N) from 52 individuals (70 samples: 44 bones and 26 teeth) were analyzed using conventional methods and Bayesian Mixing Models to address the role of marine products and plants in people's diet at both sites over time. RESULTS: Our results suggest high C3 carbohydrate consumption (55%-68% total calories in Áspero and >70% in Caral). The consumption of marine resources was stable for Áspero between 3300 and 1800 BC, but it decreased for Caral between 2550 and 200 BC. DISCUSSION: Marine protein was more important in Áspero than in Caral over time. C3 plants, possibly tubers, formed the foundation of the diet in both sites during the Formative period (~3000-200 BC). Maize was a marginal food (<12% of calories) at least until 800 BC (29% of calories). The Maritime Foundations hypothesis does not completely account for these findings. Our results suggest the predominance of crop-focused agriculture during the evaluated period.

Challenging definitions and diagnostic approaches for ancient rare diseases: The case of poliomyelitis.

OBJECTIVE: This paper aims to contribute to the definition of ancient rare diseases in skeletons displaying pathologies associated with paralysis. It uses a new suite of methods, which can be applied to challenging cases of possible paralysis in archaeologically-derived human skeletal material, specifically applied to the identification of poliomyelitis. MATERIALS: An adult male skeleton from Roman Halbturn, Austria. METHODS: Morphological and entheseal change analyses, CT scans, X-rays, cross-section morphology, and histology, alongside modern clinical, as well as historic, literature were used to discuss paralyses. RESULTS: The results suggest a diagnosis of poliomyelitis; now considered a rare disease, but perhaps ubiquitous in antiquity, thus complicating the definition of 'rare disease'. CONCLUSIONS: The integrated methodological procedures employed for this case constitutes a replicable and thorough approach to diagnosis, and explores the nature of ancient rare diseases. Due to the socio-environmental aspects of poliomyelitis transmission, it is likely that polio was likely not rare in the past. Therefore, the definition of 'rare diseases in the past' must include rarely occurring rarely diagnosed diseases due to biases and challenges within the archaeological and environmental record. SIGNIFICANCE: The developed suite of methods has not been applied to establish a diagnosis of polio in the past. LIMITATIONS: The individual considered in this study is fairly well-preserved; thus, this set of analyses may not be applicable to all remains where preservation is poor or highly fragmentary, and the discussion of rare diseases requires relatively secure diagnoses and context. SUGGESTIONS FOR FURTHER RESEARCH: Large collections and series of skeletal human remains are recommended to develop definitive conclusions.

Child development, physiological stress and survival expectancy in prehistoric fisher-hunter-gatherers from the Jabuticabeira II shell mound, South Coast of Brazil.

In this study, we shed light on the interdependency of child growth, morbidity and life expectancy in the fisher-hunter-gatherers of the Jabuticabeira II shell mound (1214-830 cal B.C.E. - 118-413 cal C.E.) located at the South Coast of Brazil. We test the underlying causes of heterogeneity in frailty and selective mortality in a population that inhabits a plentiful environment in sedentary settlements. We reconstruct osteobiographies of 41 individuals (23 adults and 18 subadults) using 8 variables, including age-at-death, stature, non-specific stress markers (cribra orbitalia, porotic hyperostosis, periosteal reactions, periapical lesions and linear enamel hypoplasia), as well as weaning patterns based on stable isotope data to examine how stress factors module growth and survival. Our results show that shorter adult statures were linked to higher morbidity around weaning age and higher chances of dying earlier (before 35 years) than taller adult statures. In addition, short juvenile stature was related to physiological stressors and mortality. The adult "survivors" experienced recurrent periods of morbidity during childhood and adulthood, possibly associated with the high parasite load of the ecosystem and dense settlement rather than to malnourishment. An association between early-stress exposure and premature death was not demonstrated in our sample. To explain our data, we propose a new model called "intermittent stress of low lethality". According to this model, individuals are exposed to recurrent stress during the juvenile and adult stages of life, and, nevertheless survive until reproductive age or later with relative success.

'One tooth one child': evaluating the effects of diet and fertility on the oral health of women from archaeological sites in South America.

Women from ancient societies have shown a higher prevalence of dental caries in comparison with men. Recent research has shown that the relationship between increased oestrogen production during pregnancy and decreased salivary flow is a possible cause for the higher levels of caries in women, which is in contrast to the traditional view of sexual division of labour resulting in unequal access to cariogenic food. In order to test these two hypotheses, individuals exhumed from 12 South American archaeological sites were examined for markers of oral health (caries, ante mortem tooth loss, deep caries, and enamel hypoplasia) and compared in terms of fertility (Crude Birth Rate) and subsistence systems. Our results suggest that diet and other cultural practices remain the most important factors affecting oral health and that the effects of hormones can be masked by them. Such findings add to the discussion regarding the availability of micronutrients in such societies affecting caries experience in pregnant women, because of their special nutritional requirements.

Middle Holocene plant cultivation on the Atlantic Forest coast of Brazil?

This work provides robust oral pathology and stable isotope evidence on Bayesian mixing model for an unexpectedly high consumption of carbohydrates by a Middle Holocene coastal population of the Atlantic Forest of South America, an area traditionally viewed as peripheral to early centres of food production on the continent. A diversified economy with substantial consumption of plant resources was in place at the shellmound (or sambaqui) of Morro do Ouro, in Babitonga Bay, and supported a dense population at ca 4500 cal BP. This dietary composition is unique when compared with that of other contemporary and later groups in the region, including peoples who used ceramics and domesticated crops. The results corroborate independent dietary evidence, such as stone tool artefacts for plant processing and plant microremains in dental calculus of the same individuals, and suggest plant cultivation possibly took place in this region at the same time as the development of early agriculture in Amazonia and the La Plata Basin. Our study situates the Atlantic Forest coast of Brazil on the map of early plant management in the Neotropics.

Oral pathology patterns in late farmers of the Central Andes: A comparative perspective between coastal and highland populations.

Aiming at future comparisons with earlier hunter-gatherers or transitional populations, this paper intends to characterize and describe the oral pathology pattern of late agriculturalists from Central Andes dating to the Late Intermediate Period (LIP) and Inca periods (1000-1532 CE), and identify differences and/or similarities between coastal and highland populations. Although the botanical inventories of the LIP suggest carbohydrate-rich diets and similar components, it has been hypothesized that coastal and highland populations had, nevertheless, substantially different oral pathology patterns. We evaluated 14 indicators of oral pathology from Los Pinos (n=200) and Armatambo (n=25) sites in the Central Coast and two chronological phases from Laguna de los Cóndores site (LC-Inca, n=23; and LC-LIP, n=55), in the Peruvian northern highlands. The results showed a recurrent pattern of oral pathologies characterized by cervical caries (above 30%), extra-occlusal caries (above 60%), high rates of gross-gross caries, high frequency of ante mortem tooth loss, and signals of periodontal disease among these four populations. The diets of the coast were slightly more abrasive than those of the highlands. Oral pathology patterns were compatible with a slightly more cariogenic diet in the coast than in the highlands. In all four populations, those patterns were modulated by other common factors such as consumption of fermented drinks (maize beer - chicha) and the coca leaf chewing habit.

Long-term resilience of late holocene coastal subsistence system in Southeastern South america.

Isotopic and molecular analysis on human, fauna and pottery remains can provide valuable new insights into the diets and subsistence practices of prehistoric populations. These are crucial to elucidate the resilience of social-ecological systems to cultural and environmental change. Bulk collagen carbon and nitrogen isotopic analysis of 82 human individuals from mid to late Holocene Brazilian archaeological sites (∼6,700 to ∼1,000 cal BP) reveal an adequate protein incorporation and, on the coast, the continuation in subsistence strategies based on the exploitation of aquatic resources despite the introduction of pottery and domesticated plant foods. These results are supported by carbon isotope analysis of single amino acid extracted from bone collagen. Chemical and isotopic analysis also shows that pottery technology was used to process marine foods and therefore assimilated into the existing subsistence strategy. Our multidisciplinary results demonstrate the resilient character of the coastal economy to cultural change during the late Holocene in southern Brazil.

Paleoamerican diet, migration and morphology in Brazil: archaeological complexity of the earliest Americans.

During the early Holocene two main paleoamerican cultures thrived in Brazil: the Tradição Nordeste in the semi-desertic Sertão and the Tradição Itaparica in the high plains of the Planalto Central. Here we report on paleodietary singals of a Paleoamerican found in a third Brazilian ecological setting--a riverine shellmound, or sambaqui, located in the Atlantic forest. Most sambaquis are found along the coast. The peoples associated with them subsisted on marine resources. We are reporting a different situation from the oldest recorded riverine sambaqui, called Capelinha. Capelinha is a relatively small sambaqui established along a river 60 km from the Atlantic Ocean coast. It contained the well-preserved remains of a Paleoamerican known as Luzio dated to 9,945±235 years ago; the oldest sambaqui dweller so far. Luzio's bones were remarkably well preserved and allowed for stable isotopic analysis of diet. Although artifacts found at this riverine site show connections with the Atlantic coast, we show that he represents a population that was dependent on inland resources as opposed to marine coastal resources. After comparing Luzio's paleodietary data with that of other extant and prehistoric groups, we discuss where his group could have come from, if terrestrial diet persisted in riverine sambaquis and how Luzio fits within the discussion of the replacement of paleamerican by amerindian morphology. This study adds to the evidence that shows a greater complexity in the prehistory of the colonization of and the adaptations to the New World.

The usefulness of caries frequency, depth, and location in determining cariogenicity and past subsistence: a test on early and later agriculturalists from the Peruvian coast.

Dental markers have been used to unravel particularities of paleodiet, subsistence, social structure, and health. This article aims to compare oral pathology among four pre-Columbian groups with different degrees of agricultural and socio-cultural development but comparable ecological conditions who lived on the coastal desert of Peru. Three of these groups are assigned to distinct phases of the Formative Period (2500-1 BC), a time critical for our understanding of the development of agriculture and social complexity. The fourth group corresponds to the Late Intermediate Period (1000-1470 AD), when agriculture had its apogee and society was highly stratified. In this study we test whether there is an increase (1) in the frequency of carious lesions and (2) in caries depth, and (3) if there is a shift from occlusal to extra-occlusal caries locations with the development of agriculture. Therefore, we analyze the frequencies of carious lesions and antemortem tooth loss (AMTL), the caries distributions by age, sex, and type of tooth, as well as the tissues affected by, and the location of the carious lesions. Since there are no significant differences in the frequencies of carious lesions and AMTL between the groups, we reject hypothesis 1. In contrast, caries depth does increase, and caries location changes from occlusal to extra-occlusal sites with agricultural development. However, we can only corroborate hypothesis 2 and 3 when taking into consideration dental wear. Thus, we recommend that caries depth and locations should be used with evaluations of dental wear to reconstruct subsistence in ancient populations.

Syphilis at the crossroad of phylogenetics and paleopathology.

The origin of syphilis is still controversial. Different research avenues explore its fascinating history. Here we employed a new integrative approach, where paleopathology and molecular analyses are combined. As an exercise to test the validity of this approach we examined different hypotheses on the origin of syphilis and other human diseases caused by treponemes (treponematoses). Initially, we constructed a worldwide map containing all accessible reports on palaeopathological evidences of treponematoses before Columbus's return to Europe. Then, we selected the oldest ones to calibrate the time of the most recent common ancestor of Treponema pallidum subsp. pallidum, T. pallidum subsp. endemicum and T. pallidum subsp. pertenue in phylogenetic analyses with 21 genetic regions of different T. pallidum strains previously reported. Finally, we estimated the treponemes' evolutionary rate to test three scenarios: A) if treponematoses accompanied human evolution since Homo erectus; B) if venereal syphilis arose very recently from less virulent strains caught in the New World about 500 years ago, and C) if it emerged in the Americas between 16,500 and 5,000 years ago. Two of the resulting evolutionary rates were unlikely and do not explain the existent osseous evidence. Thus, treponematoses, as we know them today, did not emerge with H. erectus, nor did venereal syphilis appear only five centuries ago. However, considering 16,500 years before present (yBP) as the time of the first colonization of the Americas, and approximately 5,000 yBP as the oldest probable evidence of venereal syphilis in the world, we could not entirely reject hypothesis C. We confirm that syphilis seems to have emerged in this time span, since the resulting evolutionary rate is compatible with those observed in other bacteria. In contrast, if the claims of precolumbian venereal syphilis outside the Americas are taken into account, the place of origin remains unsolved. Finally, the endeavor of joining paleopathology and phylogenetics proved to be a fruitful and promising approach for the study of infectious diseases.

An evaluation of auditory exostoses in 621 prehistoric human skulls from coastal Brazil.

Auditory exostoses are bone anomalies located on the floor of the external auditory canal. They frequently develop in individuals who participate in water sports and other aquatic activities. Their etiology is probably multifactorial; development seems to be triggered by regular exposure to cold water as well as to low air temperatures and/or cold winds. The presence ofauditory exostoses has been recorded in human skull fossils that date back approximately 250,000 years. We conducted a study of auditory exostoses in 621 skulls of adult humans who had been part of a marine-dependent population that lived on the Brazilian coast between 5400 and 800 years ago. The overall frequency of exostoses was 22%, but there was a great variance among different subgroups (0 to 56%). In this article, we propose some possible explanations for this variance. We also hope that our study will stimulate multidisciplinary research aimed at deciphering the intricate bony messages contained in cryptic archaeologic remains.

An evolutionary approach to explain the high frequency of the polycystic ovary syndrome (PCOS).

Infertility and sterility are worldwide phenomena with a long history. At a first glance a condition causing sterility seems to be paradox in an evolutionary sense because it contradicts the biogenetical imperative. In the present paper an evolutionary explanation for the high prevalence rate of PCOS, the most common endocrine disorder causing female infertility, is presented. The symptomatology of PCOS is described and the high prevalence rates of PCOS are explained by means of Darwinian medicine, kin selection and allomothering.

Auditory exostoses as an aquatic activity marker: a comparison of coastal and inland skeletal remains from tropical and subtropical regions of Brazil.

Auditory exostoses are bone masses located in the external auditory canal. Currently, most researchers agree that the environment (especially water temperature, but also atmospheric temperature and wind action) plays a pivotal role in the development of this trait. This article discusses whether the presence of auditory exostoses can be used as an aquatic activity marker in bioarchaeological studies, especially in groups that inhabited tropical and subtropical regions. We analyzed 676 skeletons (5,000 years BP to historical times) from 27 coastal and inland native Brazilian groups. Very low frequencies of auditory exostoses were found in the inland groups (0.00-0.03), but the expected high frequency of auditory exostoses in the coastal groups was not always observed (0.00-0.56). These differences might be explained by the combination of water and atmospheric temperatures in conjunction with wind effects. In areas with mild atmospheric temperatures and wind chill factors, the coastal populations analyzed do not show high frequencies of auditory exostoses. However, high frequencies of auditory exostoses develop where cold atmospheric temperatures are further lowered by strong wind chill. Therefore, the association between aquatic activities, low atmospheric temperature, and wind chill is strongly correlated with the presence of auditory exostoses, but where these environmental factors are mild, the frequencies of auditory exostoses are not necessarily high. Concluding, auditory exostoses should be cautiously used as a marker of aquatic activity in bioarchaeological studies in tropical and subtropical regions, since these activities do not always result in the presence of this trait.

A new early Holocene human skeleton from Brazil: implications for the settlement of the New World.

Increasing skeletal evidence from the U.S.A., Mexico, Colombia, and Brazil strongly suggests that the first settlers in the Americas had a cranial morphology distinct from that displayed by most late and modern Native Americans. The Paleoamerican morphological pattern is more generalized and can be seen today among Africans, Australians, and Melanesians. Here, we present the results of a comparative morphological assessment of a late Paleoindian/early archaic specimen from Capelinha Burial II, southern Brazil. The Capelinha skull was compared with samples of four Paleoindian groups from South and Central America and worldwide modern groups from W.W. Howells' studies. In both analyses performed (classical morphometrics and geometric morphometrics), the results show a clear association between Capelinha Burial II and the Paleoindians, as well as Australians, Melanesians, and Africans, confirming its Paleoamerican status.