Genetic and functional odorant receptor variation in the Homo lineage.

Humans, Neanderthals, and Denisovans independently adapted to a wide range of geographic environments and their associated food odors. Using ancient DNA sequences, we explored the in vitro function of thirty odorant receptor genes in the genus Homo. Our extinct relatives had highly conserved olfactory receptor sequence, but humans did not. Variations in odorant receptor protein sequence and structure may have produced variation in odor detection and perception. Variants led to minimal changes in specificity but had more influence on functional sensitivity. The few Neanderthal variants disturbed function, whereas Denisovan variants increased sensitivity to sweet and sulfur odors. Geographic adaptations may have produced greater functional variation in our lineage, increasing our olfactory repertoire and expanding our adaptive capacity. Our survey of olfactory genes and odorant receptors suggests that our genus has a shared repertoire with possible local ecological adaptations.

Sexual dimorphism and biomechanical loading in occipital bone morphological variation.

We explore the contribution of biological sex and biomechanical activity from subsistence to occipital bone variation. Previous studies have used occipital bone traits to determine biological sex and identify ancestry to differing degrees of success. Biomechanical stress from variation in subsistence and gender-based divisions of labor could perhaps explain some of the noise in the signal for these grouping variables. To explore this possibility, we used metric (foramen magnum length and breadth, external occipital protuberance depth, lambda-inion length, bicondylar breadth) and nonmetric traits (general occipital form, presence of a nuchal crest, and nuchal line count). We collected original data and mined published data for our analysis using skeletal collections of Native American hunter-gatherers and horticulturalists, a historic military site, and contemporary study collections. We find that the foramen magnum area exhibits sexual dimorphism and is not influenced by subsistence, but the accuracy of sex estimation is only 71%, suggesting the chance of being correct at slightly more than two-thirds. All traits exhibited sex-based variation but only bicondylar breadth and lambda-inion metrics exhibited subsistence-based variation. Given the limited amount of variance explained by either sex or sex and subsistence, biomechanics may still play a role but not from the influence of subsistence practices in these datasets. Additional data from a wider array of skeletal samples, perhaps with known occupation, is warranted if we are to understand how occipital variation is shaped.

Developmental instability in wild Nigerian olive baboons (Papio anubis).

BACKGROUND: Developmental instability in archaeological samples can be detected through analysis of skeletal and dental remains. During life, disruptions to biological internal homeostasis that occur during growth and development redirect bodily resources to returning to homeostasis and away from normal processes such as symmetrical development. Because dental enamel does not remodel in life, any deviations from normal development are left behind. Even subtle disturbances to developmental trajectory may be detected in asymmetrical development of traits, specifically a random variation in sides termed fluctuating asymmetry. Human dental fluctuating asymmetry studies are common, but here we investigate the permanent dentition of a non-human primate Papio anubis, for potential fluctuating asymmetry relative to sex, weaning, and reproductive maturity. The sample stems from an outlier population that lives in the wettest and most humid habitat of any studied baboon group. METHODS: The skulls of adult baboons were collected after their natural death in Gashaka Gumti National Park, Nigeria. The permanent dentition of antimeric teeth (paired) were measured for maximum length and breadth using standard methods. The metrics were analyzed to assess the presence of fluctuating asymmetry in adult permanent mandibular and maxillary dentition. Measurement error and other forms of asymmetry (antisymmetry, directional asymmetry) were considered and dental measures expressing true fluctuating asymmetry were used to address three research questions. RESULTS: Males exhibit greater fluctuating asymmetry than females, suggesting that males experience greater overall instability during the developmental period. While weaning is not more stressful than other life history stages for males and females (using the first molar fluctuating asymmetry index as a proxy compared to other teeth), it is more stressful for females than males. The onset of reproduction is also not more stressful than other life history stages for males and females (using the third molar fluctuating asymmetry index as a proxy compared to other teeth), but it is more stressful for males than females. We explore possible explanations for these findings in the discussion.

Sensory disruption and sensory inequities in the Anthropocene.

Anthropogenic disruptions to animal sensory ecology are as old as our species. But what about the effect on human sensory ecology? Human sensory dysfunction is increasing globally at great economic and health costs (mental, physical, and social). Contemporary sensory problems are directly tied to human behavioral changes and activity as well as anthropogenic pollution. The evolutionary sensory ecology and anthropogenic disruptions to three human senses (vision, audition, olfaction) are examined along with the economic and health costs of functionally reduced senses and demographic risk factors contributing to impairment. The primary goals of the paper are (a) to sew an evolutionary and ecological thread through clinical narratives on sensory dysfunction that highlights the impact of the built environment on the senses, and (b) to highlight structural, demographic, and environmental injustices that create sensory inequities in risk and that promote health disparities.

Field-testing olfactory ability to understand human olfactory ecology.

OBJECTIVES: We know little about human olfactory ability in natural settings because current knowledge derives from lab-based studies using nonrepresentative samples of convenience. The primary objective was to use a validated lab tool, the five-item odor identification test, to assess variation in olfactory ability in different environments. METHODS: Using the five-item test, we conducted two repeated measures experiments that assessed participant ability to correctly identify an odor source in different odor environments. We also examined consistency in odor labelling due to documented potential bias from idiosyncrasies in odor terms. RESULTS: We found no variation in olfactory ability due to environment, but this may be due to methodological biases. First, subjective bias results from idiosyncratic differences in participant labelling and researcher coding of answer correctness. Second, better ability to learn odors may provide an advantage to women. Third, reducing positive female learning bias by analyzing consistency in response (regardless of correct odor source identification) results in no sex differences but fails to assess the functional aspect of olfactory ability (naming the correct odor source). Fourth, functional olfactory ability is significantly better in women, especially in food-rich odor environments. CONCLUSIONS: Environment was not a significant factor in olfactory ability in this study but that result may be confounded by methodological biases. We do not recommend odor identification as a field tool. Functional olfactory ability exhibits a sex-based pattern but consistency in recognizing the same odor does not. Food-rich odors may enhance olfactory ability in females. We discuss evolutionary and ecological implications of superior female functional olfactory ability relative to food foraging activity.

Intragenus (Homo) variation in a chemokine receptor gene (CCR5).

Humans have a comparatively higher rate of more polymorphisms in regulatory regions of the primate CCR5 gene, an immune system gene with both general and specific functions. This has been interpreted as allowing flexibility and diversity of gene expression in response to varying disease loads. A broad expression repertoire is useful to humans-the only globally distributed primate-due to our unique adaptive pattern that increased pathogen exposure and disease loads (e.g., sedentism, subsistence practices). The main objective of the study was to determine if the previously observed human pattern of increased variation extended to other members of our genus, Homo. The data for this study are mined from the published genomes of extinct hominins (four Neandertals and two Denisovans), an ancient human (Ust'-Ishim), and modern humans (1000 Genomes). An average of 15 polymorphisms per individual were found in human populations (with a total of 262 polymorphisms). There were 94 polymorphisms identified across extinct Homo (an average of 13 per individual) with 41 previously observed in modern humans and 53 novel polymorphisms (32 in Denisova and 21 in Neandertal). Neither the frequency nor distribution of polymorphisms across gene regions exhibit significant differences within the genus Homo. Thus, humans are not unique with regards to the increased frequency of regulatory polymorphisms and the evolution of variation patterns across CCR5 gene appears to have originated within the genus. A broader evolutionary perspective on regulatory flexibility may be that it provided an advantage during the transition to confrontational foraging (and later hunting) that altered human-environment interaction as well as during migration to Eurasia and encounters with novel pathogens.

Early Holocene morphological variation in hunter-gatherer hands and feet.

BACKGROUND: The Windover mortuary pond dates to the Early Archaic period (6,800-5,200 years ago) and constitutes one of the earliest archaeological sites with intact and well-preserved human remains in North America. Unlike many prehistoric egalitarian hunter-gatherers, the Windover people may not have practiced a sex-based division of labor; rather, they may have shared the load. We explore how mobility and subsistence, as reconstructed from archaeological data, influenced hand and foot bone morphology at Windover. METHODS: We took length and width measurements on four carpal bones, four tarsal bones, and load-bearing tarsal areas (calcaneus load arm, trochlea of the talus). We analyzed lateralization using side differences in raw length and width measurements. For other hypothesis testing, we used log transformed length-width ratios to mitigate the confounding effects of sexual dimorphism and trait size variation; we tested between-sex differences in weight-bearing (rear foot) and shock-absorbing (mid foot) tarsal bones and between-sex differences in carpal bones. RESULTS: We identified no significant between-sex differences in rear and midfoot areas, suggesting similar biomechanical stresses. We identified no significant between-sex differences in carpal bones but the test was under-powered due to small sample sizes. Finally, despite widespread behavioral evidence on contemporary populations for human hand and foot lateralization, we found no evidence of either handedness or footedness. DISCUSSION: The lack evidence for footedness was expected due its minimal impact on walking gait but the lack of evidence for handedness was surprising given that ethnographic studies have shown strong handedness in hunter-gatherers during tool and goods manufacture. The reconstructed activity patterns suggested both sexes engaged in heavy load carrying and a shared division of labor. Our results support previous findings-both sexes had stronger weight-bearing bones. Male shock-absorbing bones exhibited a trend towards greater relative width (suggesting greater comparative biomechanical stress) than females which may reflect the typical pattern of male hunter-gatherers engaging in walking greater distances at higher speeds than females. While there were no significant between-sex differences in carpal bones (supporting a shared work load model), females exhibited greater variation in index values, which may reflect a greater variety of and specialization in tasks compared to males. Because carpals and tarsals are so well-preserved at archaeological sites, we had surmised they might be useful proxies for activity in the absence of well-preserved long bones. Tarsals provide a stronger signal of past activity and may be useful in the absence of, or in addition to, preferred bones. Carpals, however, may not be useful as the effect size of biomechanical stress (in this study at least) is low and would require larger samples than may be possible at archaeological sites.

Sensory Disruption in Modern Living and the Emergence of Sensory Inequities.

Modern lifestyles are disrupting the human senses-primarily sight, sound, and smell. Noise-induced hearing loss has been noted for centuries and increasing over time following the industrial era. From the mid-20th century, the numbers of individuals with myopia (the leading visual impairment) have been increasing globally. Historical evidence for olfactory dysfunction is not known but its etiological links to pollution suggest it increased following industrialization. Clinical interventions for sight and sound loss include preventative and corrective measures but none exist for olfactory dysfunction. Further, olfactory loss is linked to multiple negative health outcomes across physical, mental, and social domains. Due to the global rates of exposure to pollution, olfaction is a global health concern. The environmental injustice inherent in human society (locally and globally) results in inequitable risk for sensory loss by the most vulnerable populations and creates an even deeper gradient in health disparity. Situated within the environmental justice and health disparity literature, this paper introduces the term sensory inequity to describe variation in sensory environments based on socio-economic status (which is often entwined with race and education). A key challenge to risk management is awareness of sensory inequity experienced by vulnerable populations and incorporating that awareness into basic research and policy.

Frequency and developmental timing of linear enamel hypoplasia defects in Early Archaic Texan hunter-gatherers.

Digital photographs taken under controlled conditions were used to examine the incidence of linear enamel hypoplasia defects (LEHs) in burials from the Buckeye Knoll archaeological site (41VT98 Victoria county, Texas), which spans the Early to Late Archaic Period (ca. 2,500-6,500 BP uncorrected radiocarbon). The majority (68 of 74 burials) date to the Texas Early Archaic, including one extremely early burial dated to 8,500 BP. The photogrammetric data collection method also results in an archive for Buckeye Knoll, a significant rare Archaic period collection that has been repatriated and reinterred. We analyzed the incidence and developmental timing of LEHs in permanent canines. Fifty-nine percent of permanent canines (n = 54) had at least one defect. There were no significant differences in LEH frequency between the maxillary and mandibular canines (U = 640.5, n1 = 37, n2 = 43, p = .110). The sample studied (n = 92 permanent canines) had an overall mean of 0.93 LEH defect per tooth, with a median of one defect, and a mode of zero defects. Average age at first insult was 3.92 (median = 4.00, range = 2.5-5.4) and the mean age of all insults per individual was 4.18 years old (range = 2.5-5.67). Age at first insult is consistent with onset of weaning stress-the weaning age range for hunter-gatherer societies is 1-4.5. Having an earlier age of first insult was associated with having more LEHs (n = 54, rho = -0.381, p = 0.005).

Global Survey of Variation in a Human Olfactory Receptor Gene Reveals Signatures of Non-Neutral Evolution.

Allelic variation at 4 loci in the human olfactory receptor gene OR7D4 is associated with perceptual variation in the sex steroid-derived odorants, androstenone, and androstadienone. Androstadienone has been linked with chemosensory identification whereas androstenone makes pork from uncastrated pigs distasteful ("boar taint"). In a sample of 2224 individuals from 43 populations, we identified 45 OR7D4 single nucleotide polymorphisms. Coalescent modeling of frequency-site-spectrum-based statistics identified significant deviation from neutrality in human OR7D4; individual populations with statistically significant deviations from neutrality include Gujarati, Beijing Han, Great Britain, Iberia, and Puerto Rico. Analysis of molecular variation values indicated statistically significant population differentiation driven mainly by the 4 alleles associated with androstenone perception variation; however, fixation values were low suggesting that genetic structure may not have played a strong role in creating these group divisions. We also studied OR7D4 in the genomes of extinct members of the human lineage: Altai Neandertal and Denisovan. No variants were identified in Altai but 2 were in Denisova, one of which is shared by modern humans and one of which is novel. A functional test of modern human and a synthesized mutant Denisova OR7D4 indicated no statistically significant difference in responses to androstenone between the 2 species. Our results suggest non-neutral evolution for an olfactory receptor gene.

Evolution of olfactory receptors.

Olfactory receptors are a specialized set of receptor cells responsible for the detection of odors. These cells are G protein-coupled receptors and expressed in the cell membranes of olfactory sensory neurons. Once a cell is activated by a ligand, it initiates a signal transduction cascade that produces a nerve impulse to the brain where odor perception is processed. Vertebrate olfactory evolution is characterized by birth-and-death events, a special case of the stochastic continuous time Markov process. Vertebrate fish have three general types of receptor cells (two dedicated to pheromones). Terrestrial animals have different epithelial biology due to the specialized adaptation to detecting airborne odors. Two general classes of olfactory receptor gene reflect the vertebrate marine heritage (Class I) and the derived amphibian, reptile, and mammal terrestrial heritage (Class II). While we know much about olfactory receptor cells, there are still areas where our knowledge is insufficient, such as intra-individual diversity throughout the life time, epigenetic processes acting on olfactory receptors, and association of ligands to specific cells.

Smell with inspiration: the evolutionary significance of olfaction.

The olfactory receptor gene family is the largest in the mammalian genome (and larger than any other gene family in any other species), comprising 1% of genes. Beginning with a genetic radiation in reptiles roughly 200 million years ago, terrestrial vertebrates can detect millions of odorants. Each species has an olfactory repertoire unique to the genetic makeup of that species. The human olfactory repertoire is quite diverse. Contrary to erroneously reported estimates, humans can detect millions of airborne odorants (volatiles) in quite small concentrations. We exhibit tremendous variation in our genes that control the receptors in our olfactory epithelium, and this may relate to variation in cross-cultural perception of and preference for odors. With age, humans experience differential olfactory dysfunction, with some odors remaining strong and others becoming increasingly faint. Olfactory dysfunction has been pathologically linked to depression and quality of life issues, neurodegenerative disorders, adult and childhood obesity, and decreased nutrition in elderly females. Human pheromones, a controversial subject, seem to be a natural phenomenon, with a small number identified in clinical studies. The consumer product industry (perfumes, food and beverage, and pesticides) devotes billions of dollars each year supporting olfactory research in an effort to enhance product design and marketing. With so many intersecting areas of research, anthropology has a tremendous contribution to make to this growing body of work that crosses traditional disciplinary lines and has a clear applied component. Also, anthropology could benefit from considering the power of the olfactory system in memory, behavioral and social cues, evolutionary history, mate choice, food decisions, and overall health.

Temporal variation and interaction between nutritional and developmental instability in prehistoric Japanese populations.

We examined nutritional and developmental instability in prehistoric Japan, using data from 49 individuals across 13 archaeological sites. Hypoplasia incidence was used as a measure of nutritional stress, and fluctuating asymmetry (of upper facial breath, orbital breadth, and orbital height) as an indirect assessment of developmental instability. Abundant resources due to a stable climate during the Middle Jomon (5,000-3,000 BP) encouraged population growth, which led to regional cultural homogeneity and complexity. A population crash on Honshu in the Late/Final Jomon (roughly 4,000-2,000 BP) led to regionally divergent subsistence economies and settlement patterns. We find that the nutritional stress was consistent between periods, but developmental instability (DI) decreased in the Late/Final Jomon. While the DI values were not statistically significant, the higher values for Middle Jomon may result from sedentism, social stratification, and differential access to resources. On Hokkaido, Jomon culture persisted until the Okhotsk period (1,000-600 BP), marked by the arrival of immigrants from Sakhalin. Nutritional stress was consistent between Middle and Late/Final Jomon, but DI increased in the Late/Final. Nutritional and developmental instability decreased from Late/Final to Okhotsk, suggesting a positive immigrant effect. We expected to find an association between stress markers due to the synergistic relationship between nutrition and pathology. The data support this hypothesis, but only one finding was statistically significant. While high critical values from small sample sizes place limits on the significance of our results, we find that the impact of environmental and cultural change to prehistoric Japanese populations was minimal.

Exploring the relationship between hypoplasia and odontometric asymmetry in Isola Sacra, an imperial Roman necropolis.

Anthropological studies reporting odontometric asymmetry values or dental enamel hypoplasia frequencies use these markers as a record of physiological perturbations occurring during dental development. While both markers indirectly suggest the amount of relative stress a population might have experienced, a relationship between the two has been explored only recently in the literature. In this study, we address the possibility of such a relationship in two ways. First, Kendall's tau B correlations test the degree of relationship on the level of the individual between hypoplasia presence/absence (P/A) and severity of hypoplasia appearance (PS) data for the anterior dentition and directional (DA) and fluctuating asymmetry (FA) data for concurrently developing molars pairs. Second, an F-test explores between-group (ranked hypoplastic individuals and non-hypoplastic individuals) variance about the mean, expecting the hypoplastic individuals to be more variable. The sample consists of 72 individuals from the Isola Sacra necropolis, which is associated with Portus, the port city of ancient Rome. Results indicated only a very weak predictive relationship between some variables and few significant differences in variation. However, variance follows trends in published literature. Possible explanations for the lack of interaction on the level of the individual include both etiological and genetic susceptibility factors that are significant in and of themselves as they suggest a more complex reading of the hard tissue evidence for stress in archaeological populations.