Category Archives: anthropology

Sex and Evolution?

I like Michael Stoddart’s books in general–he has some great contributions to make and is one of a few popular scientists promoting olfaction. While reading his most recent book, I have been a bit frustrated by the simplistic view of human evolution and behavior. A recent Guardian piece by him “Smell evolution and the sex brain: Why we’re monogamous and use perfume” captures the source of my frustration. As a biological anthropologist, I find it hard to read the following sentence:

To keep male and female together to provide protection for babies, a suite of anatomical and physiological features evolved to promote the constant availability of sex throughout the year – irrespective of the monthly ovulation cycle.

The argument is that a suite of traits evolved (e.g., reduced sexual dimorphism, hidden estrus) to render human females receptive to sex at any time and this has led to monogamy–meanwhile male receptivity to sex is used as an explanation for purported male promiscuity. Huh! The constant male bias in science is at the heart of taxonomy–our class is called mammal because male scientists felt the key trait of mammals was the use of mammary glands to feed offspring.

Increasing the diversity of voices in academia has allowed us, slowly, to move away from teleological explanations for human behavior based on western society. In biological and evolutionary anthropology, human reproduction is a hot topic and more complicated. Stoddart does qualify his statement a bit:

Yet Homo Sapiens is the only species among the 5,500 kinds of mammal to maintain monogamous family relationships – or at least serially so – and to live in densely populated areas. This combination is extremely rare in nature.

Marriage, as an institution is barely thousands of years old (our species is 200,000 years old) and the concept of marrying for love younger still. Divorce is higher today partly because there are fewer economic and political structures keeping people together–religion is what is left and that doesn’t appear strong enough for most people–divorce was central in Henry the VIII’s split with the Pope. Most cultures are polygamous even if most end up practicing monogamy (mainly due to financial and/or political constraints–not enough money or power to gain more spouses). Perhaps the clearest statement we can make on pair-bonding is that humans can, and often do, come together in a pair-bond for a period of time with a goal of child rearing but this shared interest isn’t immediately linked to sexual monogamy–they are separate issues. The period of shared interest (if it occurs) enables the child to reach a point where the ‘village’ can take on some of the burden through formal and informal education. But, even western society regularly abandons its children–part of the year, I live next door to a youth shelter and drop-in center so I see it daily.

I suppose most humans are humanists–Jon Marks is a biological anthropologist who has written many books on the subject from an evolutionary perspective with a goal to distinguish us from all the other primates. I am not a humanist even if I do appreciate what we have accomplished as a species (there’s a lot to be ashamed of too…). I think there is an inherent fallacy in not recognizing that we are animals and that we cheat and lie and love and, yes, react to odors just as animals do. We may be enculturated to curb instincts but the instincts that we are enculturated to curb and how we do so vary cross-culturally. The goal to overcome our instincts with reason is a cultural one, not a biological or evolutionary one.

And, contrary to this blanket statement:

Today we have a global fragrance market equal to the GDP of a medium-sized country. But because our nose (unlike the VNO) ultimately sends all smells for rational analysis by the brain, we do not slavishly respond to sex smells in the way dogs or mice do. An alluring perfume may help a relationship, but no perfume comes with a guarantee!

odors are first processed in the areas of the emotional center of the brain where memories are also deal with–we react to odors before the frontal lobe (where reasoning attempts to modulate instinct) gets the data and formulates a response. Maybe we wear perfume because it smells good–it takes us to places we want to be or reminds of us of memories we love or smells like things we love to eat–maybe wearing perfume is about sensuality not mating. Why is so much academic work reductionist? But, perhaps that is why I am a biological anthropologist, rather than a biologist. Still, I take the point that we may not react to odors with the full behavioral response other animals might, but we react nonetheless. The closing statement of the piece is perhaps the strangest, and to an anthropologist, the most off-putting:

And so we can live in at least relative harmony with our fellows, benefitting from the long-term genetic and evolutionary advantages provided by monogamy, while participating socially in everything society has to offer.

There probably should be more biological anthropologists writing popular press books on human evolution and this gives me even more motivation to get my long overdue book Smell of Evolution out!

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The Scent of a Man

A new study (published here) suggest that scientists unable to replicate  behavioral studies in rats and mice may be due to the presence of male researchers.

The presence of male experimenters produced a stress response in mice and rats equivalent to that caused by restraining the rodents for 15 minutes in a tube or forcing them to swim for three minutes. This stress-induced reaction made mice and rats of both sexes less sensitive to pain.

The chemical signals emitted by males of any species are detectable by other species. Since males secrete these pheromones at higher concentrations than women, the effects tend to be limited to male researchers. Rats and mice acclimatize over time to the male researchers, suggesting an ‘easing’ in period prior to experimentation or perhaps, even better, even more effort to promote women in science!

Since there is growing evidence that humans respond to pheromones, I wonder if there is a similar effect caused by male researchers on human subjects; namely, is stress induced in males and females when experiments are conducted by men? Outside the lab, does the scent of a man induce stress and reduce pain response, but in a good way? I’ll end with ‘Boys‘ by Robots in Disguise.

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Is there a connection between dietary repetition and food preferences?

A Science News Post (brought to my attention earlier in the summer by @elizabethjrowe) presents research trends in food science: the pairing of retronasal olfaction and taste reception in studying flavour and the knowledge pairing of culinary experts and scientists within a relatively new journal Flavour. I am glad that food sensation (for lack of a better word to describe the complex process of perception, taste, smell, hedonic value, and preference) is getting increasing amounts of attention! From an anthropological perspective, however, the evolutionary and cultural underpinnings of these studies is still missing from the dialogue–something I hope to rectify in the coming years!

The article leans towards the idea that repetition is the driver of food preference–and it starts in the womb. Support for this idea is presented by referencing the study on babies whose mothers ate anise and garlic during pregnancy (and therefore were not averse to the odors post-natally).  I assume the reference is to Schaal et al. 2000. That paper was great and is a start to exploring cross-cultural differences in the interaction between odor perception and food preference–but there also might be variation in olfactory receptors within the sample from the Alsace region (where anise is a common food additive but the population history of which is complex).

A taste and smell scientist is quoted as supporting the idea of repetition shaping diet: “What makes lasagna loved is that the odors have been paired to a source of calories.” Odors stimulate appetite but arguing for a causative relationship among odors, loving a food, and its caloric value is premature. We have so much yet to learn about the genetic architecture of individual and population odor profiles, which ligands bind to which receptors, odor processing, perception, and consciousness let along variation among all these things. All these known unknowns make olfaction a great place to work (and the unknown unknowns exciting things to be discovered)!

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The piggy smell of Eurasian genetic landscapes

Between 6000-4000 years ago (according to study published in Nature Communications), indigenous Mesolithic hunter-gatherers acquired pigs from Neolithic farmers immigrating to Europe. I have been interested in Pleistocene pigs for a while (and their continued association with humans into the Holocene). The reason for my interest is that pigs produce a lot of androstenone (a sex steroid), especially males, and humans vary in their genotypic/phenotypic perception of androstenone.

Human variation in androstenone perception depends on two non synonymous SNPs (Keller et al. 2007), R88W and T133M. These SNPs appear to play a role in meat preference: Lunde et al. (2012) found that wild type humans (RT/RT) rated the meat of non-castrated male pigs less favorably than those with variant alleles (RT/WM and WM/WM). HapMap and 1000 Genomes are great resources but do not capture the variation local human populations, let alone the anthropological underpinnings of variation. In my lab and using a wide mix of global human populations, I found significant variation in androstenone perception frequencies, with higher frequencies of mutations throughout Eurasia–an area heavily invested in pig meat throughout human prehistory; in Japanese and Northern Europeans, the frequency of homozygote recessive mutations is much higher and these areas have a rich history with pigs–especially Japan.

Currently, I am working through the archaeological data for human-pig interaction in Europe and Asia (with a special focus on Asia as the origin of all pigs–see here and here for starting places) to interpret the results of the genetic data. Both the archaeological data and genetic data are thin when taken across such a huge space but they are a starting point; a neat study would be to find a locale with a rich archaeological record, human population to test for the gene and perception, and a good ethnohistory on the relationship with pigs–something I am working on right now.

Combining data from the archaeological record and the genetic history of human populations adds depth to what could, on their own, be interesting but uncontextual datasets. Taken together, these datasets can paint a more detailed picture of the evolutionary inter-relationship between genes and diet.

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The Onges of the Andaman Islands and urban smell decay

A recent study by Ramesh Sahani on the changes to nutrition and body metrics (anthropometry) in the Onges of the Andaman islands shows that rapid forced settlement of a foraging population results in highly negative outcomes. Their body metrics now fall in line with overweight/obese body metrics and their diet has shifted radically: protein is now 10% of the diet (previously above 30%), calories have doubled, and physical activity has been cut in half.

The Onges are famous (to me) for their exquisitely rich odor/smell culture and language. So much of the traditional life is shaped by smell–e.g., the seasons, tribal/group membership, seasonal migrations–they even consider a lack of smell to be a sign of death!

The group that was forced to become sedentary will now live in a very different odorscape and this may, in turn, effect other changes among the people–identity confusion, disassociation from traditional rituals/practices, temporal dissonance. If I were a cultural anthropologist with the right connections, I might be tempted to jump on a plane and visit them right away.

Another problem with the smellscape of sedentary living is the impact it has on one’s nose. Urban living creates olfactory dysfunction. Two studies (here and here) in Mexico show olfactory impairment due to urbanization. The pollution in Mexico is mostly likely several orders of magnitude greater than in the Andaman Islands but we have yet to explore what the urban smellscape beyond pollution does to the sense of smell.  In his book, What the Nose Knows, Avery Gilbert imagines how chemical intraspecific communication (human to human via pheromones) is still functional in humans: somehow we are able to detect all kinds of social clues without other overt indicators (e.g., knowing when someone is slightly off before you talk to them even though they look normal). This is highly likely in my mind because even though many humans do not have a VNO (organ that detects pheromones), there are pheromone detection receptors that have migrated to the olfactory epithelium.

How might urbanized living be blunting signals and changing our social interaction spheres? We just don’t know…yet!

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The Use and Misuse of Allostatic Load in Bioanthropology

I have noticed a recent trend in bioarchaelogy referring to odontoskeletal stress markers as measures of allostatic load. Allostatic load was first described by McEwan and Stellar in 1993. They argue (quite well and rightly) that the concept of homeostasis (or internal maintenance of system functioning) fails to consider the complex biological negotiations over time within a body between internal systems (e.g., cardiovascular, immune, etc) and external forces (e.g., disease, socio-economic disparity)–a point Selye also raised in his work on stress. They specifically point to the well-established relationship between chronic stress (and stressors) and disease. They further point out that homeostasis fails to incorporate an understanding of allostatic load

“fluctuating or heightened neural or neuroendocrine response resulting from repeated or chronic environmental challenge that an individual reacts to as being particularly stressful”

and the environmental factors and genetic predispositions that contribute to/shape allostatic load–these things combined form individual susceptibility to disease (in bioarch, part of assessment of ‘frailty’ or elevated risk of death). The neural/neuroendocrine response which defines allostatic load is prolonged systemic exposure to endogenous cortisol (a hormone produced in response to stress). Cortisol levels (and our ability to recover from episodes of stress) vary significantly with age in humans. For a popular science review of cortisol levels and stress over the human lifespan, see this as a starting point then explore the rich body of lit on human cortisol.

Human biologists evaluate allostatic load relative to disease susceptibility in studies of living human populations for which they have data on cortisol levels alongside  biological, cultural, and psychosocial stresses contemporaneous to actual disease incidence. Bioarchaeologists certainly benefit from their work on the theoretical level because it elucidates an area of human biology that cannot be captured in the archaeological record but may inform our interpretation of stress markers in similar contexts. The use of the term in bioarchaeology to describe stress markers, however, is highly problematic. Certain techniques and methods sometimes allow estimation of duration and timing of disease and/or nutritional episodes that contribute to generalized stress but we cannot measure allostatic load (cortisol levels). The implication of calling traditional odontoskeletal markers (for which we have limited information on causation and other factors that are undetectable in the archaeological record) a measure of allostatic load (as described by McEwan and Stellar) is that these markers are direct proxies for elevated cortisol (allostatic load)–we have no evidence of this nor an idea of the scale of the relationship. The term is clearly interpreted broadly rather than as originally described (and currently used in human biology). Rather, allostatic load, for now, appears to be a synonym for stress markers.

A key point McEwan and Stellar make is that allostatic load is very precisely determined on an individual level–this then can be taken to the level of the population with a robust dataset in living humans. We simply do not have experimental data that allow us to extrapolate allostatic load from a few odontoskeletal makers. And, the final piece of the disease process system discussed by McEwan and Stellar, genetic predispositions, is barely given consideration in interpreting stress markers in the archaeological record. In the past, one could mention there is a genetic component to a process but then move past it by by arguing that it is immeasurable in the record. The mushrooming of new genetics technology and DNA recovery and repair techniques now allow us to examine these contributions (look at Saqqaq and Denisova) but few are doing so yet (hopefully that will increase as the analysis cost decreases more and more). Bone chemistry is a possible avenue of examining cortisol levels but the caveats that apply to stable isotope studies (a general search in google scholar for stable isotope anthropology will turn up papers that raise the issues) would come into play if it were even possible.

Bioarchaeology is a rich field and informs us about past population health and disease process relative to the archaeological record (among many other things) but it has its limitations, ones that are discussed in the literature and at conferences regularly. The dialogue about problems in bioarchaeology and improving and new technologies have allowed us to resolve or fine tune some old problems (e.g., aDNA to find instances of plague or TB) even as new ones crop up. That said, every field has its limits; most life scientists lack contextual approaches and many have limited understanding of cultural and evolutionary context. The movement in the field of bioarchaeology toward taking terms from other biological disciplines is sometimes a move in the right direction because it makes our work more accessible outside our specialization. Sometimes, however, it appears to be an attempt to legitimize our work to another community rather than celebrating the difference, recognizing the limits, and highlighting the legitimate contribution we make. I’ll end with by referring to anyone whose read this far to a great abstract from Rachel Leahy and Doug Crews from the 2013 AAPAs that critically considers the issue and draws a bridge a between skeletal frailty and living human frailty and allostatic load: In sickness and in death: What do age, stress, and illness in life tell us about skeletal remains?

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Clandestine trysts and human evolution

Recent advances in the field of paleogenomics (the study of ancient genomes) have uncovered the story of inter-species mating in those early days out of Africa before dispersal into Eurasia. Prior to these studies we’ve had little evidence supporting either cultural interaction with archaic humans or inter-breeding.

Clandestine trysts or common practice? The draft sequence of the Neanderthal genome published in 2010 revealed that we mated with Neanderthals in the Near East enough to share 1-4% of our DNA with them. On the heels of the draft sequence of the Neandertal genome, the same team published the Denisovan genome using DNA extracted from an exceptionally preserved finger bone from remains found in Denisova Cave in Siberia. The archaeological data at Denisova show a mixed toolkit with elements of Upper- and Middle-Paleolithic industries. Molar morphology indicated Denisovans were distinct from both modern and known archaic humans. The genomic data indicate Denisovans were indeed a new species with unique genomic markers. The power of modern genomics allows us to also find evidence of mating with modern humans, specifically modern Melanesians who share 4-6% of their genomes with Denisovans. Were these matings clandestine trysts or was there more at stake—some flow of genes to modern humans that helped us adapt to the novel environments of Europe and Asia?

Genomic breadcrumbs? Preliminary comparisons between Neandertal and human genes indicate significant differences in aspects of cognition, metabolism, and skeletal and skin morphology. But what about the inherited portion of the genome? Does it have a role in any functional aspect of our biology and physiology? Dr. Green, lead author on the draft sequence of the Neandertal genome described the inherited portion as ‘sparsely distributed across the genome, just a ‘bread crumbs’ clue of what happened in the past’. But two new papers tell a different story, suggesting that inter-breeding may have significantly contributed to successful adaptation to the new environments of Eurasia.

In the summer of 2011, another team identified a Neandertal origin for a unique cluster of co-inherited gene variants (a haplotype) in the non-coding segment of the dystrophin gene on the X-chromosome. This haplotype occurs at a frequency of 9% in all modern non-African human populations and likely first appeared in the genome prior to or very early in the migration out of Africa. The authors of the study posit that either this genetic (and/or cultural) exchange enabled successful modern human adaptations to the novel environments of Eurasia. There is an intriguing possibility that human males left Africa in greater numbers and mated with archaic females: an earlier study on modern human variation found the X-chromosome experienced more than expected genetic drift at the time of human migration out of Africa, a pattern not found in the migrations into East Asia and Europe.The authors of this study conclude that female effective population size was reduced compared to males due to some sex-biased process or natural selection affecting the X-chromosome in non-African populations.

Speculations that inherited genomic material conferred a fitness advantage gained further ground in a study published this summer in Nature. A Stanford University team identified HLA gene variants that are rare in modern Africans but significantly present in West Asians, again suggesting genetic admixture outside Africa prior to Eurasian expansion. HLA class I genes are critical to the immune system because they target and destroy pathogens. The authors of the study argue that inter-breeding restored HLA diversity that was reduced by a population bottleneck in migration out of Africa, citing examples of similar events in the evolutionary genetic history of the peopling of the Americas. Not only was diversity restored to modern humans but new immune variants specifically adapted to local pathogens may have been acquired in the process as well. HLA-A*11 (associated with Epstein-Barr virus protection), for example, has become a dominant form in non-African populations occurring at rates of 64% in East Asia and Oceania (and even more in Papua New Guinea) suggesting strong selection. The high frequency of these gene variants (as compared with other regions of the genome) may be explained by the need for the immune system to be flexible to new pathogens (particularly rapidly evolving viruses), rendering it more susceptible to the forces of natural selection.

The future of the past. If the data from these various studies is supported by future work, we may end up rethinking our relationship to our closest cousins – were we separate species? Even field biologists who have the array of genes, biology, physiology and behavior sometimes have trouble determining whether two groups be classed as separate species or not. For those working in paleoanthropology or paleogenomics, the dataset is even more limited and the creation of new taxa is temporary pending further data but useful as a heuristic tool.

The field of paleogenomics is relatively young and has a tremendous number of methodological and technical challenges to overcome before we can comfortably say that the sequences yielded are authentic and reliably represent the genetic data. A major challenge is verifying and authenticating the endogenous (or local) DNA in a specimen that has been potentially contaminated by microbes and human researchers. The past decade has been punctuated by marvelous advances that have helped us better understand recent human evolution and ourselves. The possibility that our advantage in global colonization derives from early acts of inter-breeding is a fascinating one. With the rapid advancements in technology and increased interest in ancient DNA, the future looks promising for unraveling the story of the immediate past.

  1. Green, R. E. et al., Science 328, 710 (2010).
  2. Reich, D. et al., Nature 468, 1053 (2010).

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Filed under anthropology, Anthropology and Evolution, Denisovan, Neandertal, race, Science, sex