Impacts of plant-based foods in ancestral hominin diets on the metabolism and function of gut microbiota in vitro

Ancestral human populations had diets containing more indigestible plant material than present-day diets in industrialized countries. One hypothesis for the rise in prevalence of obesity is that physiological mechanisms for controlling appetite evolved to match a diet with plant fiber content higher than that of present-day diets. We investigated how diet affects gut microbiota and colon cells by comparing human microbial communities with those from a primate that has an extreme plant-based diet, namely, the gelada baboon, which is a grazer. The effects of potato (high starch) versus grass (high lignin and cellulose) diets on human-derived versus gelada-derived fecal communities were compared in vitro. We especially focused on the production of short-chain fatty acids, which are hypothesized to be key metabolites influencing appetite regulation pathways. The results confirmed that diet has a major effect on bacterial numbers, short-chain fatty acid production, and the release of hormones involved in appetite suppression. The potato diet yielded greater production of short-chain fatty acids and hormone release than the grass diet, even in the gelada cultures, which we had expected should be better adapted to the grass diet. The strong effects of diet on hormone release could not be explained, however, solely by short-chain fatty acid concentrations. Nuclear magnetic resonance spectroscopy found changes in additional metabolites, including betaine and isoleucine, that might play key roles in inhibiting and stimulating appetite suppression pathways. Our study results indicate that a broader array of metabolites might be involved in triggering gut hormone release in humans than previously thought. IMPORTANCE: One theory for rising levels of obesity in western populations is that the body's mechanisms for controlling appetite evolved to match ancestral diets with more low-energy plant foods. We investigated this idea by comparing the effects of diet on appetite suppression pathways via the use of gut bacterial communities from humans and gelada baboons, which are modern-day primates with an extreme diet of low-energy plant food, namely, grass. We found that diet does play a major role in affecting gut bacteria and the production of a hormone that suppresses appetite but not in the direction predicted by the ancestral diet hypothesis. Also, bacterial products were correlated with hormone release that were different from those normally thought to play this role. By comparing microbiota and diets outside the natural range for modern humans, we found a relationship between diet and appetite pathways that was more complex than previously hypothesized on the basis of more-controlled studies of the effects of single compounds.

On the evolutionary origins of obesity: a new hypothesis

Obesity is an escalating threat of pandemic proportions, currently affecting billions of people worldwide and exerting a devastating socioeconomic influence in industrialized countries. Despite intensive efforts to curtail obesity, results have proved disappointing. Although it is well recognized that obesity is a result of gene-environment interactions and that predisposition to obesity lies predominantly in our evolutionary past, there is much debate as to the precise nature of how our evolutionary past contributed to obesity. The “thrifty genotype” hypothesis suggests that obesity in industrialized countries is a throwback to our ancestors having undergone positive selection for genes that favored energy storage as a consequence of the cyclical episodes of famine and surplus after the advent of farming 10 000 years ago. Conversely, the “drifty genotype” hypothesis contends that the prevalence of thrifty genes is not a result of positive selection for energy-storage genes but attributable to genetic drift resulting from the removal of predative selection pressures. Both theories, however, assume that selection pressures the ancestors of modern humans living in western societies faced were the same. Moreover, neither theory adequately explains the impact of globalization and changing population demographics on the genetic basis for obesity in developed countries, despite clear evidence for ethnic variation in obesity susceptibility and related metabolic disorders. In this article, we propose that the modern obesity pandemic in industrialized countries is a result of the differential exposure of the ancestors of modern humans to environmental factors that began when modern humans left Africa around 70 000 years ago and migrated through the globe, reaching the Americas around 20 000 years ago. This article serves to elucidate how an understanding of ethnic differences in genetic susceptibility to obesity and the metabolic syndrome, in the context of historic human population redistribution, could be used in the treatment of obesity in industrialized countries

Paleoamerican Morphology in the Context of European and East Asian Late Pleistocene Variation: Implications for Human Dispersion Into the New World

Early American crania show a different morphological pattern from the one shared by late Native Americans. Although the origin of the diachronic morphological diversity seen on the continents is still debated, the distinct morphology of early Americans is well documented and widely dispersed. This morphology has been described extensively for South America, where larger samples are available. Here we test the hypotheses that the morphology of Early Americans results from retention of the morphological pattern of Late Pleistocene modern humans and that the occupation of the New World precedes the morphological differentiation that gave rise to recent Eurasian and American morphology. We compare Early American samples with European Upper Paleolithic skulls, the East Asian Zhoukoudian Upper Cave specimens and a series of 20 modern human reference crania. Canonical Analysis and Minimum Spanning Tree were used to assess the morphological affinities among the series, while Mantel and Dow-Cheverud tests based on Mahalanobis Squared Distances were used to test different evolutionary scenarios. Our results show strong morphological affinities among the early series irrespective of geographical origin, which together with the matrix analyses results favor the scenario of a late morphological differentiation of modern humans. We conclude that the geographic differentiation of modern human morphology is a late phenomenon that occurred after the initial settlement of the Americas. Am J Phys Anthropol 144:442-453, 2011. (c) 2010 Wiley-Liss, Inc.

Plasmodium falciparum Accompanied the Human Expansion out of Africa

Plasmodium falciparum is distributed throughout the tropics and is responsible for an estimated 230 million cases of malaria every year, with a further 1.4 billion people at risk of infection [1-3]. Little is known about the genetic makeup of P. falciparum populations, despite variation in genetic diversity being a key factor in morbidity, mortality, and the success of malaria control initiatives. Here we analyze a worldwide sample of 519 P. falciparum isolates sequenced for two housekeeping genes (63 single nucleotide polymorphisms from around 5000 nucleotides per isolate). We observe a strong negative correlation between within-population genetic diversity and geographic distance from sub-Saharan Africa (R(2) = 0.95) over Africa, Asia, and Oceania. In contrast, regional variation in transmission intensity seems to have had a negligible impact on the distribution of genetic diversity. The striking geographic patterns of isolation by distance observed in P. falciparum mirror the ones previously documented in humans [4-7] and point to a joint sub-Saharan African origin between the parasite and its host. Age estimates for the expansion of P. falciparum further support that anatomically modern humans were infected prior to their exit out of Africa and carried the parasite along during their colonization of the world.

Stone tool use by adult wild bearded capuchin monkeys (Cebus libidinosus). Frequency, efficiency and tool selectivity

Chimpanzees have been the traditional referential models for investigating human evolution and stone tool use by hominins. We enlarge this comparative scenario by describing normative use of hammer stones and anvils in two wild groups of bearded capuchin monkeys (Cebus libidinosus) over one year. We found that most of the individuals habitually use stones and anvils to crack nuts and other encased food items. Further, we found that in adults (1) males use stone tools more frequently than females, (2) males crack high resistance nuts more frequently than females, (3) efficiency at opening a food by percussive tool use varies according to the resistance of the encased food, (4) heavier individuals are more efficient at cracking high resistant nuts than smaller individuals, and (5) to crack open encased foods, both sexes select hammer stones on the basis of material and weight. These findings confirm and extend previous experimental evidence concerning tool selectivity in wild capuchin monkeys (Visalberghi et al., 2009b; Fragaszy et al., 2010b). Male capuchins use tools more frequently than females and body mass is the best predictor of efficiency, but the sexes do not differ in terms of efficiency. We argue that the contrasting pattern of sex differences in capuchins compared with chimpanzees, in which females use tools more frequently and more skillfully than males, may have arisen from the degree of sexual dimorphism in body size of the two species, which is larger in capuchins than in chimpanzees. Our findings show the importance of taking sex and body mass into account as separate variables to assess their role in tool use. (C) 2011 Elsevier Ltd. All rights reserved.

Inferences regarding the diet of extinct hominins: structural and functional trends in dental and mandibular morphology within the hominin clade

This contribution investigates the evolution of diet in the Pan – Homo and hominin clades. It does this by focusing on 12 variables (nine dental and three mandibular) for which data are available about extant chimpanzees, modern humans and most extinct hominins. Previous analyses of this type have approached the interpretation of dental and gnathic function by focusing on the identification of the food consumed (i.e. fruits, leaves, etc.) rather than on the physical properties (i.e. hardness, toughness, etc.) of those foods, and they have not specifically addressed the role that the physical properties of foods play in determining dental adaptations. We take the available evidence for the 12 variables, and set out what the expression of each of those variables is in extant chimpanzees, the earliest hominins, archaic hominins, megadont archaic hominins, and an inclusive grouping made up of transitional hominins and pre-modern Homo . We then present hypotheses about what the states of these variables would be in the last common ancestor of the Pan – Homo clade and in the stem hominin. We review the physical properties of food and suggest how these physical properties can be used to investigate the functional morphology of the dentition. We show what aspects of anterior tooth morphology are critical for food preparation (e.g. peeling fruit) prior to its ingestion, which features of the postcanine dentition (e.g. overall and relative size of the crowns) are related to the reduction in the particle size of food, and how information about the macrostructure (e.g. enamel thickness) and microstructure (e.g. extent and location of enamel prism decussation) of the enamel cap might be used to make predictions about the types of foods consumed by extinct hominins. Specifically, we show how thick enamel can protect against the generation and propagation of cracks in the enamel that begin at the enamel– dentine junction and move towards the outer enamel surface.

Adaptation to hard-object feeding in sea otters and hominins

The large, bunodont postcanine teeth in living sea otters (Enhydra lutris) have been likened to those of certain fossil hominins, particularly the ’robust’ australopiths (genus Paranthropus). We examine this evolutionary convergence by conducting fracture experiments on extracted molar teeth of sea otters and modern humans (Homo sapiens) to determine how load-bearing capacity relates to tooth morphology and enamel material properties. In situ optical microscopy and x-ray imaging during simulated occlusal loading reveal the nature of the fracture patterns. Explicit fracture relations are used to analyze the data and to extrapolate the results from humans to earlier hominins. It is shown that the molar teeth of sea otters have considerably thinner enamel than those of humans, making sea otter molars more susceptible to certain kinds of fractures. At the same time, the base diameter of sea otter first molars is larger, diminishing the fracture susceptibility in a compensatory manner. We also conduct nanoindentation tests to map out elastic modulus and hardness of sea otter and human molars through a section thickness, and microindentation tests to measure toughness. We find that while sea otter enamel is just as stiff elastically as human enamel, it is a little softer and tougher. The role of these material factors in the capacity of dentition to resist fracture and deformation is considered. From such comparisons, we argue that early hominin species like Paranthropus most likely consumed hard food objects with substantially higher biting forces than those exerted by modern humans.

Models of hybridization during range expansions and their application to recent human evolution

Several lines of genetic, archeological and paleontological evidence suggest that anatomically modern humans (Homo sapiens) colonized the world in the last 60,000 years by a series of migrations originating from Africa (e.g. Liu et al., 2006; Handley et al., 2007; Prugnolle, Manica, and Balloux, 2005; Ramachandran et al. 2005; Li et al. 2008; Deshpande et al. 2009; Mellars, 2006a, b; Lahr and Foley, 1998; Gravel et al., 2011; Rasmussen et al., 2011). With the progress of ancient DNA analysis, it has been shown that archaic humans hybridized with modern humans outside Africa. Recent direct analyses of fossil nuclear DNA have revealed that 1–4 percent of the genome of Eurasian has been likely introgressed by Neanderthal genes (Green et al., 2010; Reich et al., 2010; Vernot and Akey, 2014; Sankararaman et al., 2014; Prufer et al., 2014; Wall et al., 2013), with Papua New Guineans and Australians showing even larger levels of admixture with Denisovans (Reich et al., 2010; Skoglund and Jakobsson, 2011; Reich et al., 2011; Rasmussen et al., 2011). It thus appears that the past history of our species has been more complex than previously anticipated (Alves et al., 2012), and that modern humans hybridized several times with local hominins during their expansion out of Africa, but the exact mode, time and location of these hybridizations remain to be clarifi ed (Ibid.; Wall et al., 2013). In this context, we review here a general model of admixture during range expansion, which lead to some predictions about expected patterns of introgression that are relevant to modern human evolution.

Long distance dispersal shaped patterns of human genetic diversity in Eurasia

Most previous attempts at reconstructing the past history of human populations did not explicitly take geography into account, or considered very simple scenarios of migration and ignored environmental information. However, it is likely that the Last Glacial Maximum (LGM) affected the demography and the range of many species, including our own. Moreover, long-distance dispersal (LDD) may have been an important component of human migrations, allowing fast colonization of new territories and preserving high levels of genetic diversity. Here, we use a high-quality microsatellite dataset genotyped in 22 populations to estimate the posterior probabilities of several scenarios for the settlement of the Old World by modern humans. We considered models ranging from a simple spatial expansion to others including LDD and a LGM-induced range contraction, as well as Neolithic demographic expansions. We find that scenarios with LDD are much better supported by data than models without LDD. Nevertheless, we show evidence that LDD events to empty habitats were strongly prevented during the settlement of Eurasia. This unexpected absence of LDD ahead of the colonization wave front could have been caused by an Allee effect, either due to intrinsic causes such as an inbreeding depression built during the expansion, or to extrinsic causes such as direct competition with archaic humans. Overall, our results suggest only a relatively limited effect of the LGM-contraction on current patterns of human diversity. This is in clear contrast with the major role of LDD migrations, which have potentially contributed to the intermingled genetic structure of Eurasian populations.

Distance from Sub-Saharan Africa Predicts Mutational Load in Diverse Human Genomes

The Out-of-Africa (OOA) dispersal ∼50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population genetics theory predicts an increase of mutational load in populations undergoing serial founder effects during range expansions. To test this hypothesis, we have sequenced full genomes and high-coverage exomes from seven geographically divergent human populations from Namibia, Congo, Algeria, Pakistan, Cambodia, Siberia, and Mexico. We find that individual genomes vary modestly in the overall number of predicted deleterious alleles. We show via spatially explicit simulations that the observed distribution of deleterious allele frequencies is consistent with the OOA dispersal, particularly under a model where deleterious mutations are recessive. We conclude that there is a strong signal of purifying selection at conserved genomic positions within Africa, but that many predicted deleterious mutations have evolved as if they were neutral during the expansion out of Africa. Under a model where selection is inversely related to dominance, we show that OOA populations are likely to have a higher mutation load due to increased allele frequencies of nearly neutral variants that are recessive or partially recessive.

Global patterns of DNA polymorphism in noncoding regions in human populations

DNA sequence variation is currently a major source of data for studying human origins, evolution, and demographic history, and for detecting linkage association of complex diseases. In this dissertation, I investigated DNA variation in worldwide populations from two ∼10 kb autosomal regions on 22q11.2 (noncoding) and 1q24 (introns). A total of 75 variant sites were found among 128 human sequences in the 22q11.2 region, yielding an estimate of 0.088% for nucleotide diversity (π), and a total of 52 variant sites were found among 122 human sequences in the 1q24 region with an estimated π value of 0.057%. The data from these two regions and a 10 kb noncoding region on Xq13.3 all show a strong excess of low-frequency variants in comparison to that expected from an equilibrium population, indicating a relatively recent population expansion. The effective population sizes estimated from the three regions were 11,000, 12,700, and 8,600, respectively, which are close to the commonly used value of 10,000. In each of the two autosomal regions, the age of the most recent common ancestor (MRCA) was estimated to be older than 1 million years among all the sequences and ∼600,000 years among non-African sequences, providing first evidence from autosomal noncoding or intronic regions for a genetic history of humans much more ancient than the emergence of modern humans. The ancient genetic history of humans indicates no severe bottleneck during the evolution of humans in the last half million years; otherwise, much of the ancient genetic history would have been lost during a severe bottleneck. This study strongly suggests that both the “out of Africa” and the multiregional models are too simple for explaining the evolution of modern humans. A compilation of genome-wide data revealed that nucleotide diversity is highest in autosomal regions, intermediate in X-linked regions, and lowest in Y-linked regions. The data suggest the existence of background selection or selective sweep on Y-linked loci. In general, the nucleotide diversity in humans is low compared to that in chimpanzee and Drosophila populations. ^

Ahead of the Game: Middle and Upper Palaeolithic Hunting Behaviors in the Southern Caucasus

Over the past several decades a variety of models have been proposed to explain perceived behavioral and cognitive differences between Neanderthals and modern humans. A key element in many of these models and one often used as a proxy for behavioral “modernity” is the frequency and nature of hunting among Palaeolithic populations. Here new archaeological data from Ortvale Klde, a late Middle–early Upper Palaeolithic rockshelter in the Georgian Republic, are considered, and zooarchaeological methods are applied to the study of faunal acquisition patterns to test whether they changed significantly from the Middle to the Upper Palaeolithic. The analyses demonstrate that Neanderthals and modern humans practiced largely identical hunting tactics and that the two populations were equally and independently capable of acquiring and exploiting critical biogeographical information pertaining to resource availability and animal behavior. Like lithic techno-typological traditions, hunting behaviors are poor proxies for major behavioral differences between Neanderthals and modern humans, a conclusion that has important implications for debates surrounding the Middle–Upper Palaeolithic transition and what features constitute “modern” behavior. The proposition is advanced that developments in the social realm of Upper Palaeolithic societies allowed the replacement of Neanderthals in the Caucasus with little temporal or spatial overlap and that this process was widespread beyond traditional topographic and biogeographical barriers to Neanderthal mobility.

Distribution of haplotypes from a chromosome 21 region distinguishes multiple prehistoric human migrations

Despite mounting genetic evidence implicating a recent origin of modern humans, the elucidation of early migratory gene-flow episodes remains incomplete. Geographic distribution of haplotypes may show traces of ancestral migrations. However, such evolutionary signatures can be erased easily by recombination and mutational perturbations. A 565-bp chromosome 21 region near the MX1 gene, which contains nine sites frequently polymorphic in human populations, has been found. It is unaffected by recombination and recurrent mutation and thus reflects only migratory history, genetic drift, and possibly selection. Geographic distribution of contemporary haplotypes implies distinctive prehistoric human migrations: one to Oceania, one to Asia and subsequently to America, and a third one predominantly to Europe. The findings with chromosome 21 are confirmed by independent evidence from a Y chromosome phylogeny. Loci of this type will help to decipher the evolutionary history of modern humans.

Direct radiocarbon dates for Vindija G1 and Velika Pećina Late Pleistocene hominid remains

New accelerator mass spectrometry radiocarbon dates taken directly on human remains from the Late Pleistocene sites of Vindija and Velika Pećina in the Hrvatsko Zagorje of Croatia are presented. Hominid specimens from both sites have played critical roles in the development of current perspectives on modern human evolutionary emergence in Europe. Dates of ≈28 thousand years (ka) before the present (B.P.) and ≈29 ka B.P. for two specimens from Vindija G1 establish them as the most recent dated Neandertals in the Eurasian range of these archaic humans. The human frontal bone from Velika Pećina, generally considered one of the earliest representatives of modern humans in Europe, dated to ≈5 ka B.P., rendering it no longer pertinent to discussions of modern human origins. Apart from invalidating the only radiometrically based example of temporal overlap between late Neandertal and early modern human fossil remains from within any region of Europe, these dates raise the question of when early modern humans first dispersed into Europe and have implications for the nature and geographic patterning of biological and cultural interactions between these populations and the Neandertals.