Kara C. Hoover

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.

Occupation Mediates Ecosystem Services with Human Well-Being

The 2005 Millennium Ecosystem Assessment linked ecosystem services, the benefits people obtain from ecosystems, directly with four constituents of human well-being: security, basic material for good life, health, and freedom of choice and action. No explicit model of the role of human activity in the transformation of ecosystem services into well-being was, however, developed by the Assessment and the connective relations between ecosystem services and human well-being remain poorly understood. The authors of this paper argue that the concept of “occupation” is a crucial addition to understanding these connective relations. It is proposed that human well-being, human activity, and ecosystem services are mediated by, i.e., connected through the medium of, occupational performance. Some implications of this proposal for the study of the human dimensions of global environmental change are briefly discussed.

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.

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).

Market Smells: Olfactory Detection and Identification in the Built Environment

The majority of studies on human olfaction are conducted under pristine lab conditions with pure odors delivered to the nostrils. While useful for extending our knowledge of human odor detection and perception as well as integration with the other senses, these experiments tell us little about how humans smell in natural environments; increasingly, the natural environment is the built environment. We must expand our focus of inquiry in order to understand how the human sense of smell operates to discern input from a welter of environmental sensory signals. This is critical because our sense of smell is increasingly challenged by the anthropogenic effects of modern life (which are also impacting animal populations and human populations leading non-urbanized or post-industrial lifestyles). To gather data on human ability to detect identify odors in the built environment, we asked volunteers at we asked volunteers at two different London-area food markets (one urban, one suburban) to smell four odors that were previously validated for UK populations. We were mainly interested in knowing how strong environmental signals (e.g., fish stalls, cooking foods) interfere with the ability to detect and identify odors under the nose. The results indicate that the sensory rich environment of the markets disrupted odor detection and identification ability when compared to lab-based results for UK populations. Further, we found that odors from cooking food were particularly and significantly disruptive. The larger implications of the study are that we must consider the human ecology of olfaction in addition to lab-based studies if we are to understand the functional use of our sense of smell. The applied implication of the study is that olfactory environments vary and that variation results in different lived experiences of the sensory environment.ABSTRACT We know little about human olfactory ability in natural settings—for humans, this includes both natural and built environments. Our knowledge derives from clinics and lab experiments using samples of convenience, often students and usually WEIRD. But, humans live in odor rich environments, most are not western, and many are not industrialized or formally educated. The problem is that we lack field methods for studying olfactory ability outside the lab and cannot fully understand olfaction within an ecological setting. To explore what clinical methods might be transferrable from the lab to the field, we completed three experiments in a variety of settings with and without repeated measures. Odor purity and background odors at test sites are not mitigated because the larger research question of interest is to understand the impact of varying test environments on olfactory ability—how our sense of smell operates in daily life. Results suggest that olfactory ability is much worse in non-lab settings than in the lab and that variation in testing due to the environment does not cause significantly different outcomes. Further, we find the that forced choice method for the short odor identification tests introduces a learning bias wherein participants tend to get better at naming odors in the first trial due to having seen ‘correct’ answers on the forced choice list. Challenges of studying human olfaction in non-lab settings include recruiting participants, minimizing test time, and avoiding subject learning. We report two broader implications of this research. First, comparing field-collected to lab-collected data is not meaningful for understanding human olfactory ecology. The fundamental differences in test conditions (pure single odors in an air-controlled lab versus odor mixtures with variable environmental conditions) preclude robust comparisons. While clinical diagnoses are essential to, in particular, geriatric health, they cannot inform an understanding olfactory performance in an evolutionarily salient way. Second, superior female olfactory ability appeared to be upheld in our field-based studies and we postulate that perhaps there is evolutionary explanation given that females produce most of the food in foraging societies and engage in human-environment interactions in such a way that forces them to learn odors rapidly. These data are the first to explore methods issues on testing olfactory ability in the field in an anthropologically and evolutionarily meaningful way.We know little about human olfactory ability in natural settings, for humans this includes urban and rural built environments. Our knowledge derives from clinics and lab experiments using samples of convenience, often students and usually WEIRD. But, humans live in odor rich environments, most are not western, and many are not industrialized or educated. The problem is that we lack field methods for studying olfactory ability outside the lab and cannot fully understand olfaction within an ecological setting. To understand the impact of varying test environments on olfactory ability, we conducted two tests: short odor identification in two locations, repeated measures short odor identification in three locations. Odor purity and background odors are not mitigated as the goal is to assess olfactory ability in quotidian life. Results indicated that environment is not a significant factor in olfactory ability and that olfactory ability is much worse in natural settings than in the lab. Further testing of the influence of variation in air quality and volatiles during non-lab testing bouts is a logical next step. More importantly, how can we reconcile measures of healthy olfaction in the lab with olfactory dysfunction in natural settings? Finally, widening representation of human populations (including indigenous groups practicing traditional subsistence) is a logical next step in understanding how much the built environment is disrupting our sense of smell. This study is a valuable first step in exploring the human ecology of olfaction.Objectives We know little about human olfactory ability in natural settings because current knowledge derives from lab-based studies using non-representative 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) fails to assess functional olfactory ability. Functional olfactory ability (naming correct odor source) is significantly better in females, 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 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.We know little about human olfactory ability in natural settings, for humans this includes urban and rural built environments. Our knowledge derives from clinics and lab experiments using samples of convenience, often students and usually WEIRD. But, humans live in odor rich environments, most are not western, and many are not industrialized or educated. The problem is that we lack field methods for studying olfactory ability outside the lab and cannot fully understand olfaction within an ecological setting. To understand the impact of varying test environments on olfactory ability, we conducted two tests: short odor identification in two locations, repeated measures short odor identification in three locations. Odor purity and background odors are not mitigated as the goal is to assess olfactory ability in quotidian life. Results indicated that environment is not a significant factor in olfactory ability and that olfactory ability is much worse in natural settings than in the lab. Further testing of the influence of variation in air quality and volatiles during non-lab testing bouts is a logical next step. More importantly, how can we reconcile measures of healthy olfaction in the lab with olfactory dysfunction in natural settings? Finally, widening representation of human populations (including indigenous groups practicing traditional subsistence) is a logical next step in understanding how much the built environment is disrupting our sense of smell. This study is a valuable first step in exploring the human ecology of olfaction.

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.

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.

Human occipital bone sexual dimorphism in an Archiac period archaeological population

PREPRINT NOTES This paper was submitted for publication the International Journal of Osteoarchaeology in August of 2003. The paper was rejected roughly a year later due to scope and collection issues. I revisited the paper in 2007 with an eye to updating and resubmitting with additional data but the project was triaged from the publication pipeline due to the work involved relative to other projects more relevant to my research interests at the time. The current preprint paper contains updated references on occipital bone sexual dimorphism—all limited to the condylar region rather than the full suite of variation in the region. I am posting this to the preprint server to contribute the findings to the larger scientific community in the hopes that I might have time to revisit the paper as a student project. A more rigorous study would need to expand the sample either to a study collection that has remains with known sex (either verified via molecular sexing techniques or using a modern study collection) or additional comparative collections from hunter-gatherer populations. If a student is interested in taking up the topic and assuming lead authorship on a co-authored paper, I’d be happy to collaborate and see this piece through the publication pipeline. ABSTRACT This paper presents the results of a comprehensive study of sexual dimorphism in the human occipital region of the skull using the remains of 39 prehistoric adults from the prehistoric Windover (6,000-8,000 BP). The results of a discriminant analysis classified 64% of the individuals correctly (using osteologically identified sex). Sexual dimorphism in this population may not be prevalent due to environmental stress.

Intragenus variation in a Chemokine Receptor Gene (CCR5) in Homo

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.