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The Future of Smelling

Coming on the heels of a grant proposal, I am starting to think about my upcoming paper for the American Association for the Advancement of Science meetings in Boston in February. My talk will focus on the future of human smelling in a panel called ‘How We Came To Our Senses: Ecology, Evolution, and Future of Human Sensation’ The panel also features my colleagues Dr. Nathaniel Dominy (Dartmouth College), Dr. Amanda Melin (University of Calgary), and Dr. Paul Breslin (Monell Chemical Senses). This panel is a lovely step forward for my research which has focused on the evolution of our sense of smell and modern human variation in ability to detect specific odors (as limited by the small number of receptor-ligand knowns). I have written before about our early efforts to rebuild ancient noses which was picked up in several media outlets. I hope to get the final results of the Old Noses out in early 2018 along with the human variation data (stay tuned for some sneak-peak blog posts). For now, though, I want to focus on the next steps.

While visiting Durham University in the UK this fall, I have been thinking about modern cities and smellscapes–a contrast to where I would normally be, rural Alaska. Namely, I have been thinking about how a thread of anthropological research on environmental inequities is highly relevant to modern smellscapes. Specifically, sensory environments in cities are not equal and some people bear the burden of negative sensory input on a regular basis–garbage, noise, greater concentrations of pollution (e.g., bus routes), urban decay. The higher your socio-economic status, the more you can afford to elevate your place of living out of the sensory fray and surround yourself with positive sensory landscapes. The access to positive sensory landscapes is only going to become more polarized: urban population density projections show an increase from 54% to 66% by 2050 (UN)–in Europe 73% of the population lives in urban areas and 82% in the US. Africa and Asia are not as urbanized but projections show great increases in those areas in the few decades.

We are already very mismatched to the modern urban smellscape–our evolutionary sensory tuning took place in lush environments in Africa, rich with natural odors of plants and animals and other humans. We were in deep and regular contact with the environment–actively engaged (and anyone who has engage in any kind of smell training–perfume and wine mainly–knows how important that regular exposure is. In fact, some research has shown that hunter-gatherers can detect odors in more more dilute forms. Now, we find ourselves in built environments with manufactured odors (think Lush, Subway, and any number of modern chains with bespoke smells) and pollutants (which also diminish our capacity to smell well as seen here and here). This is true of urban areas but also true of rural areas with high activity in farming, mining, and manufacturing–all of which produce anthropogenic waste.

What does that mean for us? We are at greater risk of reduced capacity to smell (smell-ability) and increasingly find ourselves in environments with unnatural odors, high concentrations of harmful odors, and an inequitable distribution of positive sensory input. Smell loss and exposure to negative smellscapes (e.g., living near a piggery, manufacturing plant, or landfill–to name a few) increases risk for depression as well as reduces quality of life. No one has yet looked at impacts of artificial smells. An impaired sense of smell can result in eating issues as well as exposure to danger (not smelling rotten foods, toxins). Urban futures must focus on equitable in the sensory landscape, reduction in artificial sensory stimuli, and mitigation of negative sensory input across the urban setting. These efforts should be paramount to protect a sense that most people don’t think about but that performs vital day to day functions. I plan to launch several projects in the coming year that will address many of these unknowns and advance awareness of sensory inequities–this work will be embedded in my current work establishing the general architecture of human smelling in the distant evolutionary past and modern distribution of variation So, stay tuned!!

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Sensory perception and the trigeminal nerve

I recently made black beans and rice for a sunny deck party in Alaska at the cabin. The remainder from the deck party went to another party that included many SE Asians. I made it mild (5 jalapenos and chili powder), or so I thought, but both parties reported back that it was too spicy to eat more than a small portion. This led me to ponder the what leads to variation in sensory perception of data generated by the trigeminal nerve.

The trigeminal nerve (with regards to eating) is responsible for heat and cold detection (e.g., mint feels cool, chili feels hot) as well as other components of texture (e.g., crunchiness, density, sponginess) and is a perfect partner for chemosensing (taste and smell, collectively known as flavour). Between these cranial nerves (I-olfaction; V-trigeminal; VII and IX-taste), we get a full rich experience in the mouth.

Is there variation in how the nerve operates or something at the level of perception? With the chemosenses, we can look at the receptors and other accessory agents in the sensing process but not as much with the trigeminal nerve. So, is it learned–eat hotter foods to tolerate more heat? If the latter, we loop back to the notion of preference and how it is shaped. My mother is Irish so I grew up with well prepared but not spicy food. Two weeks most summers though, she would go home to Carrandine and my father would take over the kitchen and bring the heat to burritos and chili. Despite so little hot food influence in my formative years, I prefer hot foods and carry chili peppers in my bag. Only 3 times in my life have I had food that was at my tolerance limit and this includes many authentically prepared dishes in personal homes in Asia, Europe, and the US. I also love anything minty–the stronger the better. My aggressive palate is also very sensitive to textures–I have no objection to mushroom flavour (broth/sauce) but cannot eat a mushroom. If I were a neuroscientist, I would probably make this my field of inquiry–uncover what drives this preference impulse and how such variation within and among cultures.

A not-so-great movie  (Perfect Sense, 2011) explored a global phenomenon in which humans gradually lost of each of the five traditional senses. When the sense of smell was lost, chefs focused on contrasting the basic tastes. When taste was lost, they concentrated on novel textures and colors to try to engage the palate (and keep their kitchens open). This engagement with multiple senses is the focus on cross-modal sensory science which has a core idea derived from common sense: all the senses contribute to the experience of eating and drinking. Afterall, anyone can identify the value of a carefully presented plate compared to cafeteria ‘slop’ on a plate. But, these sensory scientists want to uncover what the various roles of non-chemosensing components have in overall food/drink perception and hedonic value (positive-pleasure; negative-displeasure). For example, does color have a great impact than shape or is it texture or the room ambiance or the plate itself (shape and color)? There is still so much to explore within the chemosenses, let alone how the senses integrate in the experience of food and drink. At the very least, we know what we like and some of us can carry chili peppers around to feed the heat!

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Consider Smell

Tomorrow, my colleagues and I will engage members of the public to consider smell from the molecular level to the streets of London! Following two events in Nottingham, tomorrow’s event will focus on a workshop format in the morning where Zoologist/Behavourial Geneticist Matthew Cobb of the University of Manchester and I will give an interactive lecture/workshop on the molecular level of smell from odorants to perception with an evolutionary spin. We’ll talk about our recent paper showing how one gene linked to smell may have been selected in Eurasian populations and contemplate what the evolutionary setting for smell selection may have been. After a small tastes multisensory lunch, our group will take a smell walk led by Designer Kate McLean of Canterbury Christ Church University (sensorymaps.com) and Geographer Julia Feuer-Cotter of the University of Nottingham. For  more info see: www.considersmell.com

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What Neandertals smelt…

My recent research has had a little news coverage today which is lovely. My esteemed colleague, Dr. Matthew Cobb of the U of Manchester (@matthewcobb), fronted for our team today on BBC4 Inside Science (What Neandertals Smelt). The piece begins at 15:38 and runs for about 8 minutes.

The University of Manchester did a nice PR piece on our paper in Chemical Senses today as well. In short, we found a signature of natural selection acting on OR7D4, a gene that controls the receptor for androstenone. Androstenone is found in all mammals but male pigs have it in spades because it makes female pigs receptive to sex. Eurasians have a higher probability of desensitization to the compound based on their genetic code. We speculate a bit broadly that perhaps the decreased sensitivity to this compound made boar (which reeks of androstenone, among other things) more appealing as a food choice to our Neolithic ancestors. After all, pigs were first domesticated in Asia, where they have an evolutionary origin.

Perhaps the most fun part of this paper was the work done by my also esteemed colleague at Duke University (Dr. Hiroaki Matsunami) wherein his lab made the androstenone receptor based on sequence data from the Denisova paleogenome. My study of the ancient genes suggested that Altai Neandertal was similar to humans but Denisovans had a unique variant. This mutation did not make a real difference in the mutated gene’s functional response to the odor but the fact that we were able to demonstrate this was a big breakthrough.

Now, we are rebuilding about 30 more ancient olfactory receptors to see how different those were!

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Is odorant diversity driving olfactory receptor genetic variation?

Olfactory receptor genes have more variation than most gene families in the human genome. The only family with greater diversity is the major histocompatibility complex (MHC). Both families also exhibit high heterozygosity. Due to its association with disease, the MHC is well-studied. The explanation for the maintenance of MHC diversity is pathogen-driven selection–either through heterozygote advantage or frequency-dependent selection (see here for a review); a small number of papers (here’s two: and 2) have also argued for divergent allele advantage. A diversity of  pathogens will result in a diversity of MHC genes over time; as a species develops resistance to a disease, an evolutionary respones occurs in the disease-causing agent. The common analogy is the evolutionary arms race, also called the Red Queen Hypothesis.

If we apply that same model to olfaction in light of a few recent findings. there might be something worth pursuing. We know we can smell millions of odors. Such a diversity of odorants in the environment that vary from region to region may result in incredible diversity in the human olfactory receptor subgenome–especially if we look at it from the perspective of divergent allele advantage.

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Stress and sex

A study from 2013 that documented sex differences in sleep needs (based on inflammatory markers) turned  my thoughts to stress susceptibility. I recently wrote about allostatic load, a measure of elevated cortisol (a stress hormone) in living human populations. While attempts to transfer the concept of allostatic load to the bioarchaeological record are lacking robusticity, there is a rich history of people writing about odonto-skeletal stress markers and variation within and among populations in the frequencies of these markers.

A commonly cited expectation is that male physiological vulnerability results in higher levels of stress markers unless otherwise culturally buffered by sex-biased investment in offspring. The assumption of sex-based differences in one stress marker (enamel hypoplasias) was reviewed and mostly dismissed by Guatelli-Steinberg and Lukacs (though read the paper to understand the weak effect sex may have in some cases, the data analyzed to make this conclusion, and other subtle findings). Instead, they find that the big effect in the development of sex differences is from culturally based sex-biased investment in children. The sex-bias is hard to show in the archaeological record: in other words, while the biological data may show a sex difference, determining if the differences are from sampling error (burials most often are small in sample size and non-representative) or cultural biases (interpretable often through the material culture record) is extremely challenging. 

According to a growing body of research (perhaps stemming from high rates of heart disease in modern females–number one killer), females have more inflammatory markers in their body and higher rates of inflammation. Inflammation is part of the native immune system and a basic sign of physiological stress. These findings, if they can be applied to past populations, suggest that females are not buffered biologically and archaeological data suggest that more often than not, females are also not buffered culturally.

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Resilience and adaptation/Canalization and stress

This is a very belated follow-up to a previous blog on the stress concept in biological anthropology. The utility of resilience in interpreting the archaeological record is under-rated as are the parallels of homeostasis and stress in human biology. I first became involved in studying resilience theory at UAF when I joined the RAP faculty. I presented some of this work in a seminar in Japan in 2009. After that and in a series of papers led by my archaeology colleague (Mark Hudson at NishiKyushu University Japan), we have explored resilience theory as a method of examining the archaeological record. We weren’t the first to think of this (here for a start). In the past two years, I have been looking at the parallels to concepts long used in biology, canalization and stress. The fundamental unit underlying these concepts is systemic integrity and external forces acting on that integrity. This concept appears across the academy with parallels in physics (surface tension), engineering, etc.

My interest is human biology from an evolutionary perspective (including the archaeological record). As biocultural beings, humans are shaped by biology and culture. When we look at evidence of physiological activity in the past, the context of those artifacts is key. Understanding when an organism is resistant to change (from external forces) while remaining internally coherent is, at the base of it, no different than understanding when a society is resistant to change while remaining internally coherent. Another way to understanding the competing forces of stability and change (in organisms or in society) is to look at how the system (biological or cultural) may adapt (or change, interpreted very loosely) in response to external forces. Adaptation is part of the resilience cycle. The difference between this and collapse is that the essential parts of the system (organismal or cultural) maintain integrity, as opposed to simply disappearing or being assimilated. More archaeological data are showing the persistence (in some capacity) of collapsed, dominated, or assimilated cultures (see here for some examples).

In modern societies, the system itself can be understood as well as the context; what cannot be understood is longitudinal change. Archaeological materials and their interpretation can provide the longitudinal data that measure system continuity (or lack thereof) after a period of prolonged or severe acute external stress; the challenge lies in reconstructing the system (and which components are essential). Combining these two datasets (contemporary and past) adds tremendous value to projections for the future–we get rich longitudinal data and rich system data, the combination of which provide a template for modelling future outcomes to responses to change.

Coming back to the biological parallel, we can use these sets of data to test resilience–was a population cultural resilient but biologically in decline or was a population experiencing improved biological conditions but cultural unstable. Since a key feature of modern resilience theory is both cultural and physiological well-being (again, defined broadly), a truly resilience system will show evidence of maintenance (or improvement) in both sectors. If we examine the data and find that a group shows cultural resilience but poor health or vice versa, were they truly resilient? Perhaps a better way to look at this is through the modified cycle of systems where resilience can be considered a reorganization. The moment (in archaeological time) when a system is experiencing external stress but maintaining culture and health is a precursor to the moment when the system is unsustainable and must reorganize. The maintenance of health and basic cultural values will persist even if the system appears to be dramatically changed. In some cases, the decline is too great and the system integrity is compromised and changes rather than adapts.

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