Social, ecological, and developmental influences on fruit and invertebrate foraging strategies and gut microbial communities in white-faced capuchins (Cebus capucinus)

Primates are challenged by spatiotemporal variation in resource availability, and a central question in biological anthropology is how primates compensate for seasonal variation in food resources by adjusting their foraging strategies. How primates respond to variation in invertebrate availability has rarely been the focus of studies of primate foraging ecology. This dissertation examines the role of insectivory in shaping foraging strategies, elucidates developmental differences in invertebrate foraging strategies, and investigates the role of the gut microbiome in mediating dietary changes in white-faced capuchins. White-faced capuchins (Cebus capucinus) are an instructive model for examining the influences of changes in both fruit and arthropod availability on foraging strategies, as they devote a mean of 44.4% of feeding and foraging time to fruit, 38.0% to invertebrates, and 1.2% to vertebrates. A group of 20-22 white-faced capuchins was studied from January 2013 through January 2014 at La Suerte Biological Field Station in northeastern Costa Rica. Data was collected from individually recognizable adult and juvenile capuchins on diet (fruit, invertebrates, leaves, seeds, vertebrates, other), activity budget (feeding, foraging, traveling, resting, social, other), affiliative and agonistic interactions, nearest neighbor identity and distance, foraging subgroup size and spread, and geographic location at 2-minute intervals during 1-hour focal follows. Crown volume, diameter at breast height, number of food items in the crown, and average mass of five food items was collected for each tree in which the group fed for more than four minutes in order to assess patch productivity. Every two weeks, fruit resource availability was tracked using 25 100x4 meter phenology transects, and invertebrate resource availability was assessed using 10 composite insect traps and sweep net sites. Fecal samples were collected throughout the study period (n=225). DNA was extracted from fecal samples, and the COI mtDNA and the v3-v5 region of the 16S rRNA genes were amplified and sequenced to identify invertebrates consumed and the gut microbial community structure. The second chapter uses social network analysis to quantify group-level responses of white-faced capuchins to changes in food availability. The results indicate that increases in fruit abundance and decreases in patch density increase group cohesion (network density = 0.48±0.01 during periods of high abundance and patch density, network density = 0.40±0.07 during periods of low abundance and patch density), indicating that individuals may be decreasing group cohesion as fruit resources become less available in order to avoid feeding competition. Additionally, the abundance and distribution of invertebrate resources does not have a consistent effect on group cohesion, and the results suggest that capuchins do not see invertebrates as a uniform resource. In the third chapter of my dissertation, innovative molecular methods are used to identify the taxa of invertebrates present in the diet of white-faced capuchins and more closely investigates how animal prey foraging strategies are influenced by invertebrate availability, and the role of ontogeny on the development of foraging skills in capuchins. This chapter compares frequency with which DNA sequences assigned to specific Orders and Families of invertebrates are found in adult and juvenile feces, showing that juvenile capuchins are eating embedded, concealed, and highly mobile invertebrates, such as Gryllidae and Cercopidae, less often when compared with adults. Additionally, the results indicate that white-faced capuchins are consuming a greater diversity of arthropod prey than other New World monkey species, with the exception of squirrel monkeys, with 29 Orders, 90 Families, and 287 genera of invertebrates identified in their diet. Finally, chapter four examines how changes in fruit and invertebrate foraging behavior and dietary choice influence gut microbial community structure and function in white-faced capuchins. This chapter shows that the relative abundance of several microbial genera have significant relationships with the minutes per hour spent feeding and foraging on several fruit species and invertebrate Families. In addition, these same fruit and invertebrate taxa have significant relationships with the relative abundance of predicted microbial metabolic functional pathways in the gut. This dissertation presents a multi-level approach to studying white-faced capuchin foraging ecology, and the findings underscore the importance of looking beyond food abundance and distribution as the primary factors driving nonhuman primate foraging strategies. The results suggest that models of primate foraging strategies should include not only ecological and social information, but also individual-level factors such as physiology, personality, genetic traits, and commensal microbial relationships. The integrative multifaceted approach to primate foraging ecology in this dissertation provides a framework with which to begin to truly understand the complexity and plasticity of primate foraging strategies

Human microbiome variation associated with race and ethnicity emerges as early as 3 months of age

Human microbiome variation is linked to the incidence, prevalence, and mortality of many diseases and associates with race and ethnicity in the United States. However, the age at which microbiome variability emerges between these groups remains a central gap in knowledge. Here, we identify that gut microbiome variation associated with race and ethnicity arises after 3 months of age and persists through childhood. One-third of the bacterial taxa that vary across caregiver-identified racial categories in children are taxa reported to also vary between adults. Machine learning modeling of childhood microbiomes from 8 cohort studies (2,756 samples from 729 children) distinguishes racial and ethnic categories with 87% accuracy. Importantly, predictive genera are also among the top 30 most important taxa when childhood microbiomes are used to predict adult self-identified race and ethnicity. Our results highlight a critical developmental window at or shortly after 3 months of age when social and environmental factors drive race and ethnicity-associated microbiome variation and may contribute to adult health and health disparities

Análisis del genoma mitocondrial de dos individuos inhumados en el sitio arqueológico CG14E01 “Isla Larga” (Rocha, Uruguay)

CG14E01 “Isla Larga” is a site with a moundlike structure (cerrito de indios) located in Rocha (Uruguay), with a chronology spanning the period from 3600 years BP to the 17th century. Evidence of various interethnic interactions has been found at the site, namely, two Tupiguarani urns and some European glass beads. Connected with this evidence, three primary burials, one male and two female, were recovered. The goal of this paper is to analyze the complete mitochondrial genome of the female individuals, one of which shows perimortem trauma. The DNA of both individuals was extracted from teeth, and their mitochondrial genome sequence was obtained by means of high through put sequencing. The authenticity of the sequences was verified through the analysis of postmortem DNA damage in the mapped reads. Both individuals were found to belong to a previously unregistered haplotype of the founding American haplogroup C1b, sharing the mutations 185A, 3116T, 3203T, 14397G, and 14502C. In view of the considerations made by other researchers about the mounds as territorial markers, the possibility that this structure could have served as a burial location for individuals related by kinship gains strength. On the other hand, the elements of the context and the evidence of trauma allow a second perspective, related to the interethnic dynamics described in the regional ethnohistorical record.CG14E01 “Isla Larga” es un sitio con estructura monticular (“cerrito de indios”) localizado en el departamento de Rocha (Uruguay), con una cronología que se extiende de 3600 años AP al siglo XVII. En este sitio se registran evidencias vinculadas con diversos contactos interétnicos en la forma de dos urnas Tupiguaraní y cuentas de vidrio de origen europeo. Asociados a estas evidencias se recuperaron tres enterramientos primarios, uno masculino y dos femeninos. El objetivo de este trabajo consiste en analizar el mitogenoma completo de los individuos femeninos, que presentan desgaste dental acentuado y que en un caso presenta trauma perimortem. El ADN de los dos individuos fue extraído a partir de piezas dentales y su secuencia genómica mitocondrial fue obtenida mediante secuenciación masiva, verificándose su autenticidad por el análisis de las modificaciones postmortem  del ADN en las lecturas mapeadas. Ambos individuos pertenecen a un haplotipo hasta ahora no registrado del haplogrupo fundador americano C1b, compartiendo las mutaciones 185A, 3116T, 3203T y 14502C. En virtud de consideraciones hechas por otros investigadores a propósito del “cerrito” como marcador territorial, la posibilidad de que la estructura haya servido de lugar de inhumación para individuos unidos por lazos de parentesco es sugerente. Por otra parte, los elementos del contexto y la evidencia de trauma añaden una segunda perspectiva, vinculada con las dinámicas interétnicas descriptas en el registro etnohistórico de la región

Análisis del genoma mitocondrial de dos individuos inhumados en el sitio arqueológico CG14E01 “Isla Larga” (Rocha, Uruguay)

CG14E01 “Isla Larga” es un sitio con estructura monticular (“cerrito de indios”) localizado en el departamento de Rocha (Uruguay), con una cronología que se extiende de 3600 años AP al siglo XVII. En este sitio se registran evidencias vinculadas con diversos contactos interétnicos en la forma de dos urnas Tupiguaraní y cuentas de vidrio de origen europeo. Asociados a estas evidencias se recuperaron tres enterramientos primarios, uno masculino y dos femeninos. El objetivo de este trabajo consiste en analizar el mitogenoma completo de los individuos femeninos, que presentan desgaste dental acentuado y que en un caso presenta trauma perimortem. El ADN de los dos individuos fue extraído a partir de piezas dentales y su secuencia genómica mitocondrial fue obtenida mediante secuenciación masiva, verificándose su autenticidad por el análisis de las modificaciones postmortem del ADN en las lecturas mapeadas. Ambos individuos pertenecen a un haplotipo hasta ahora no registrado del haplogrupo fundador americano C1b, compartiendo las mutaciones 185A, 3116T, 3203T y 14502C. En virtud de consideraciones hechas por otros investigadores a propósito del “cerrito” como marcador territorial, la posibilidad de que la estructura haya servido de lugar de inhumación para individuos unidos por lazos de parentesco es sugerente. Por otra parte, los elementos del contexto y la evidencia de trauma añaden una segunda perspectiva, vinculada con las dinámicas interétnicas descriptas en el registro etnohistórico de la región.CG14E01 “Isla Larga” is a site with a moundlike structure (cerrito de indios) located in Rocha (Uruguay), with a chronology spanning the period from 3600 years BP to the 17th century. Evidence of various interethnic interactions has been found at the site, namely, two Tupiguarani urns and some European glass beads. Connected with this evidence, three primary burials, one male and two female, were recovered. The goal of this paper is to analyze the complete mitochondrial genome of the female individuals, one of which shows perimortem trauma. The DNA of both individuals was extracted from teeth, and their mitochondrial genome sequence was obtained by means of highthroughput sequencing. The authenticity of the sequences was verified through the analysis of postmortem DNA damage in the mapped reads. Both individuals were found to belong to a previously unregistered haplotype of the founding American haplogroup C1b, sharing the mutations 185A, 3116T, 3203T, 14397G, and 14502C. In view of the considerations made by other researchers about the mounds as territorial markers, the possibility that this structure could have served as a burial location for individuals related by kinship gains strength. On the other hand, the elements of the context and the evidence of trauma allow a second perspective, related to the interethnic dynamics described in the regional ethnohistorical record.Asociación de Antropología Biológica de la República Argentina (AABRA

Análisis del genoma mitocondrial de dos individuos inhumados en el sitio arqueológico CG14E01 “Isla Larga” (Rocha, Uruguay)

CG14E01 “Isla Larga” es un sitio con estructura monticular (“cerrito de indios”) localizado en el departamento de Rocha (Uruguay), con una cronología que se extiende de 3600 años AP al siglo XVII. En este sitio se registran evidencias vinculadas con diversos contactos interétnicos en la forma de dos urnas Tupiguaraní y cuentas de vidrio de origen europeo. Asociados a estas evidencias se recuperaron tres enterramientos primarios, uno masculino y dos femeninos. El objetivo de este trabajo consiste en analizar el mitogenoma completo de los individuos femeninos, que presentan desgaste dental acentuado y que en un caso presenta trauma perimortem. El ADN de los dos individuos fue extraído a partir de piezas dentales y su secuencia genómica mitocondrial fue obtenida mediante secuenciación masiva, verificándose su autenticidad por el análisis de las modificaciones postmortem del ADN en las lecturas mapeadas. Ambos individuos pertenecen a un haplotipo hasta ahora no registrado del haplogrupo fundador americano C1b, compartiendo las mutaciones 185A, 3116T, 3203T y 14502C. En virtud de consideraciones hechas por otros investigadores a propósito del “cerrito” como marcador territorial, la posibilidad de que la estructura haya servido de lugar de inhumación para individuos unidos por lazos de parentesco es sugerente. Por otra parte, los elementos del contexto y la evidencia de trauma añaden una segunda perspectiva, vinculada con las dinámicas interétnicas descriptas en el registro etnohistórico de la región.CG14E01 “Isla Larga” is a site with a moundlike structure (cerrito de indios) located in Rocha (Uruguay), with a chronology spanning the period from 3600 years BP to the 17th century. Evidence of various interethnic interactions has been found at the site, namely, two Tupiguarani urns and some European glass beads. Connected with this evidence, three primary burials, one male and two female, were recovered. The goal of this paper is to analyze the complete mitochondrial genome of the female individuals, one of which shows perimortem trauma. The DNA of both individuals was extracted from teeth, and their mitochondrial genome sequence was obtained by means of highthroughput sequencing. The authenticity of the sequences was verified through the analysis of postmortem DNA damage in the mapped reads. Both individuals were found to belong to a previously unregistered haplotype of the founding American haplogroup C1b, sharing the mutations 185A, 3116T, 3203T, 14397G, and 14502C. In view of the considerations made by other researchers about the mounds as territorial markers, the possibility that this structure could have served as a burial location for individuals related by kinship gains strength. On the other hand, the elements of the context and the evidence of trauma allow a second perspective, related to the interethnic dynamics described in the regional ethnohistorical record.Asociación de Antropología Biológica de la República Argentina (AABRA

Análisis del genoma mitocondrial de dos individuos inhumados en el sitio arqueológico CG14E01 “Isla Larga” (Rocha, Uruguay)

CG14E01 “Isla Larga” es un sitio con estructura monticular (“cerrito de indios”) localizado en el departamento de Rocha (Uruguay), con una cronología que se extiende de 3600 años AP al siglo XVII. En este sitio se registran evidencias vinculadas con diversos contactos interétnicos en la forma de dos urnas Tupiguaraní y cuentas de vidrio de origen europeo. Asociados a estas evidencias se recuperaron tres enterramientos primarios, uno masculino y dos femeninos. El objetivo de este trabajo consiste en analizar el mitogenoma completo de los individuos femeninos, que presentan desgaste dental acentuado y que en un caso presenta trauma perimortem. El ADN de los dos individuos fue extraído a partir de piezas dentales y su secuencia genómica mitocondrial fue obtenida mediante secuenciación masiva, verificándose su autenticidad por el análisis de las modificaciones postmortem del ADN en las lecturas mapeadas. Ambos individuos pertenecen a un haplotipo hasta ahora no registrado del haplogrupo fundador americano C1b, compartiendo las mutaciones 185A, 3116T, 3203T y 14502C. En virtud de consideraciones hechas por otros investigadores a propósito del “cerrito” como marcador territorial, la posibilidad de que la estructura haya servido de lugar de inhumación para individuos unidos por lazos de parentesco es sugerente. Por otra parte, los elementos del contexto y la evidencia de trauma añaden una segunda perspectiva, vinculada con las dinámicas interétnicas descriptas en el registro etnohistórico de la región.CG14E01 “Isla Larga” is a site with a moundlike structure (cerrito de indios) located in Rocha (Uruguay), with a chronology spanning the period from 3600 years BP to the 17th century. Evidence of various interethnic interactions has been found at the site, namely, two Tupiguarani urns and some European glass beads. Connected with this evidence, three primary burials, one male and two female, were recovered. The goal of this paper is to analyze the complete mitochondrial genome of the female individuals, one of which shows perimortem trauma. The DNA of both individuals was extracted from teeth, and their mitochondrial genome sequence was obtained by means of highthroughput sequencing. The authenticity of the sequences was verified through the analysis of postmortem DNA damage in the mapped reads. Both individuals were found to belong to a previously unregistered haplotype of the founding American haplogroup C1b, sharing the mutations 185A, 3116T, 3203T, 14397G, and 14502C. In view of the considerations made by other researchers about the mounds as territorial markers, the possibility that this structure could have served as a burial location for individuals related by kinship gains strength. On the other hand, the elements of the context and the evidence of trauma allow a second perspective, related to the interethnic dynamics described in the regional ethnohistorical record.Asociación de Antropología Biológica de la República Argentina (AABRA

Ancient and modern genomics of the Ohlone Indigenous population of California

Traditional knowledge, along with archaeological and linguistic evidence, documents that California supports cultural and linguistically diverse Indigenous populations. Studies that have included ancient genomes in this region, however, have focused primarily on broad-scale migration history of the North American continent, with relatively little attention to local population dynamics. Here, in a partnership involving researchers and the Muwekma Ohlone tribe, we analyze genomic data from ancient and present-day individuals from the San Francisco Bay Area in California: 12 ancient individuals dated to 1905 to 1826 and 601 to 184 calibrated years before the present (cal BP) from two archaeological sites and eight present-day members of the Muwekma Ohlone tribe, whose ancestral lands include these two sites. We find that when compared to other ancient and modern individuals throughout the Americas, the 12 ancient individuals from the San Francisco Bay Area cluster with ancient individuals from Southern California. At a finer scale of analysis, we find that the 12 ancient individuals from the San Francisco Bay Area have distinct ancestry from the other groups and that this ancestry has a component of continuity over time with the eight present-day Muwekma Ohlone individuals. These results add to our understanding of Indigenous population history in the San Francisco Bay Area, in California, and in western North America more broadly

Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints

The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns (n = 448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets

<i>trnL</i> outperforms <i>rbcL</i> as a DNA metabarcoding marker when compared with the observed plant component of the diet of wild white-faced capuchins (<i>Cebus capucinus</i>, Primates)

<div><p>DNA metabarcoding is a powerful tool for assessing the diets of wild animals, but there is no clear consensus on which proposed plant barcoding marker is most suitable for dietary analysis. This study compares two DNA plant barcoding markers that are commonly used for dietary analyses from degraded DNA, <i>rbcL</i> and <i>trnL</i>, to detailed dietary observations of wild white-faced capuchins (<i>Cebus capucinus</i>). Observational dietary data and fecal samples (n = 170) were collected for one year from a group of individually recognizable monkeys at La Suerte Biological Field Station, Costa Rica. DNA was extracted and portions of the <i>rbcL</i> and <i>trnL</i> chloroplast were amplified and sequenced on the Illumina MiSeq platform. Sequences were analyzed using <i>obitools</i>. Of the two barcoding markers tested, <i>trnL</i> yielded greater numbers of sequences with equal sequencing effort, higher resolution taxonomic identifications (albeit with a larger reference database), and identified a greater number of families also found in the observed diet. There was no relationship between observed capuchin feeding behavior and dietary composition based on either sequence occurrence or relative abundance of sequences using <i>rbcL</i> as a marker. However, dietary composition based on the relative abundance of <i>trnL</i> sequences was significantly positively associated with the observed percentage of feeding and foraging time capuchins’ spent on each plant species. Additionally, in 35% of cases, the relative abundance of <i>trnL</i> sequences assigned to particular plant families in fecal samples was highly positively correlated with time spent consuming plants from those same families. Our results indicate that <i>trnL</i> is a more robust DNA metabarcoding marker for plant dietary analysis and may potentially be used to quantitatively assess differences in diet within or between species.</p></div