For anyone interested, the paper I speak of is:

‘Eutrophication causes speciation reversal in whitefish adaptive radiations’ by Vonlanthen et al. in Nature volume 482, pages 357-363.

While there are many schools of thought on how this interbreeding took place, a common viewpoint is that Homos neanderthalensis and sapiens simply represented different radiations, and that the later (sapiens) simply displaced/absorbed the earlier (neanderthalensis) through either direct or indirect competition. The hybridisation of these species seems to have been treated by many workers as something that ‘just happened’ and really deserves greater thought. Could it be that climactic changes pressed neanderthal populations into an overlap with their expansive ‘modern’ relatives? Who says that sapiens was the only population on the move? Additionally, if climate change had the result of reducing neanderthal numbers then a shortage of mates may well have compounded this situaiton, drawing neanderthal populations closer to modern groups of out necessity. This could have fostered a situation of speciation reversal as described by Vonlanthen et al. with their lake fish. Worth thinking about, the person typing this article is, after all, a member of the resultant hybrid species.

Update: It seems that a recent paper has pressed the same viewpoint I was getting at above. I shall post on this shortly.

Anyhow, in my YouTube procrastinations I have stumbled across two terrific video bloggers dedicated to fighting for atheism and rationalist viewpoints. Much like these two, I’m no longer comfortable with allowing religious types to be involved with the media or politics and intend to take a more active stance in opposing those who would push their whacky convictions on others.

First up, we have AronRa, a Texan who has been a vocal opponent of the teaching of creationism in schools. Despite his terrifying visage, the man is exceptionally eloquent and one of the best arguers of rationalism I have ever come across.

Find him here: http://www.youtube.com/user/aronra?ob=

Secondly, we have Thunderf00t, the maker of a terrific serious exploring why it is that we laugh at creationists, among other brilliant vids. His videos are highly entertaining and from personal experience I can tell you that showing them to religious types is sure to make them blush if not storm off and never talk to you ever again (either way, good result).

Find him here: http://www.youtube.com/user/Thunderf00t

I hope you enjoy these! Should I have time, I’m considering a vlog of my own, though first I shall focus on getting more articles up on this blog! The cobwebs are growing thick and fast!

Introduction

The notion that human cultural innovation, and the consequential capacity to change the world around us, has allowed us to sufficiently divorce ourselves from the natural world as to escape natural selection, is pervasive. So much so that entire bodies of human sociobiological work have been built upon it, prime among these being the field of evolutionary psychology with its assumptions that our Neolithic minds have been unable to keep up with our rapidly changing, culturally constructed world (Laland & Brown, 2011). Recent work in molecular evolutionary biology has begun to seriously degrade the plausibility of such viewpoints. Utilising a survey of the human genome, Hawks et al. (2007) have argued, based on single nucleotide polymorphisms and linkage disequilibrium, that in response to human cultural innovations that have occurred within the last 10,000 years, human biological evolution has, far from conforming with the common view above, experienced a period of unprecedented acceleration. It would appear that rather than reducing selection pressures, our cultural innovations (namely agriculture and urbanisation), mobilised as a kind of niche construction (Laland, 2008), have generated potent selective pressures of their own.

The field of ‘gene-culture coevolution’ stands in an ideal location to offer explanations on how these man-made environmental alterations have in turn altered our genes at an unprecedented rate. While much of the early work in this field was theoretical/mathematical in nature (Feldman & Cavalli-Sforza, 1976; Laland & Brown, 2011), the mapping of the human genome and our increasing understanding of which genes are related to particular phenotypes has allowed workers in this field to assess with ever increasing accuracy which genes are likely to have been under recent, culturally mediated, selective pressure (Richerson, Boyd, & Henrich, 2010).

Wang et al. (2006), utilising molecular techniques, identified several functional groupings of genes that seem to have undergone strong recent selection. Among these groupings, three are of particular interest when viewed from the perspective of gene-culture coevolution: genes relating to food processing, genes involved in disease resistance and genes expressed in the brain. This essay shall evaluate a selection of alleles that fall within these three categories in an effort to assess the likelihood that cultural innovations in the last 10,000 years have influenced their selection. In following with the views of Diamond (1991), the position that agriculture, as a niche construction activity, is the key to the development of complex societies shall be taken. Genes that seem to have been placed under greater selective pressure by the adoption of this cultural innovation and associated dietary changes shall be explored first. Secondly, based upon the idea that an agricultural base allows populations of greater density to be built (Diamond, 1991), evidence of genetic change related to resistance of diseases endemic to highly populated areas shall be examined. Finally, evidence for recent selection of genes associated with brain function, the ultimate human tool for social interaction, shall be considered in the light of social changes generated by agriculture and increases in population density.

Agriculture, Diet and Genes

In considering the last 10,000 years, one human cultural innovation dwarfs all others for its flow on effects in terms of the human environment, agriculture (Diamond, 1991).  Agriculture is thought to have arisen independently in (and then culturally radiated out from) various regions, including the Fertile Crescent, Central and Northern Africa, East Asia and the Americas between 7,000 and 10,000 years ago (Diamond, 1991). It is conceivable that this ‘Neolithic Revolution’ marked the beginning of the evolutionary acceleration identified by Hawks et al. (2007). In generating a stable niche in terms of food availability, perhaps in response to a stabilising climate (Richerson, Boyd, & Bettinger, 2001), Neolithic humans likely found themselves consuming a much more homogenous diet and/or utilising nutrient sources previously less favoured (Richerson, et al., 2010). As shall be demonstrated, the resultant change in diet was adequate to increase selection for certain genes that allowed these early agriculturalists to make the most of the nutrient sources present.

The domestication of rice, barley, wheat and other cereal crops, along with root vegetables like potatoes and yams, significantly increased the intake of starch for Neolithic farmers (Meisenberg, 2008).  This would have generated a positive selective pressure for genes allowing more efficient processing of this particular plant carbohydrate. Evidence of this is seen today, as the copy number of the gene AMY1, responsible for the production of salivary amylase (an enzyme that breaks starch into simpler sugars), seems to vary by population group in relation to their history of starch consumption (Ley, Lozupone, Hamady, Knight, & Gordon, 2008; Richerson, et al., 2010). Essentially, populations with a long history of agriculture and thus a starchy diet, have more copies of this particular gene. It is highly likely that this trend had its origins in the Neolithic agricultural revolution.

Molecular evidence derived from the DNA of Southern Chinese populations seems to indicate that fermentation of domesticated plants (the production of alcohol) followed soon after the advent of rice based agriculture in this region (Peng et al., 2010). This trend seems to be temporally true of other early agricultural centers also with various ancient populations (Egypt, Mesopotamia, Greece) seeming to have a long history of alcohol production, based on archaeological evidence (Dietler, 2006). The negative health affects of excessive alcohol consumption are well known today and it would seem that these produced selective pressure for genes that enhance the breakdown of this chemical (Peng, et al., 2010). In the case of the Chinese population mentioned, the enrichment of a certain class of alcohol dehydrogenase sequence polymorphism, dated to approximately 7,000-10,000 years ago, supports this notion (Peng, et al., 2010). Should alcohol consumption indeed generate selective pressures like those posed here, it is expected that other populations with a long history of alcohol consumption should show similar recent adaptations as a function of convergent evolution.

Agriculture, of course, encompasses more than the domestication of plants. The domestication of animals is also thought to have generated pressure for genetic change in early farmers (Laland, Odling-Smee, & Myles, 2010). Perhaps the most well studied example of this relates to the consumption of milk and the persistence of lactase production in adults in populations with a history of this practice (Laland, et al., 2010; Richerson, et al., 2010). The presence of the gene responsible for the persistence of lactase production in European adults (the word persistence is used as all humans produce lactase as infants and generally cease production sometime after weaning in non-milk consuming populations) is estimated to have reached significant frequencies some 5,000-10,000 years ago, based on molecular evidence, and is absent in DNA extracted from ancient remains from earlier time periods (Laland, et al., 2010).  This matches relatively closely with our archaeological understanding of when animal domestication became widespread (Diamond, 1991). The genetic mechanisms behind lactase persistence in non-European populations present compelling evidence for the selective strength of this cultural innovation as different, independently selected, genes are responsible in some populations (Enattah et al., 2008).

In addition to the diet related adaptations mentioned above, agriculture enabled significant changes in human demography. With a stable, agriculture based, source of resources, populations became more sedentary and greater numbers of individuals were able to be supported by a given tract of land (Diamond, 1991). Hawks et al. (2007) have argued that this population boom was in fact responsible for the genetic diversity necessary to fuel the rapid digestive adaptations mentioned and as shall be demonstrated, was likely a crucial factor in the genetic adaptations relating to disease resistance and brain function to be expounded below.

Population Growth, Disease Burden and Genes of Resistance

            The Neolithic agricultural revolution allowed humans to live at densities that had been impossible prior (Diamond, 1991), in turn, this generated an environment in which infectious diseases were readily transmissible (Barnes, Duda, Pybus, & Thomas, 2011). It is conceivable that following outbreaks of diseases endemic to populated areas, individuals with a biological edge, alleles of resistance, would be more likely to pass these useful genes onto future generations. Several recent research projects seem to support this line of reasoning.

One of the most often discussed examples of recent human evolution relating to disease resistance is the advent, and subsequent increase in frequency, of the sickle cell (HbS) gene in response to high rates of infection with malaria in West Africa (Richerson, et al., 2010). In this case, it is thought that the cultivation of yams by West Africans generated large areas of standing water that had previously been non-existent in the area, allowing malaria harbouring mosquitos to proliferate (Laland, 2008). This combined with what was likely a growing agricultural population, created sufficient selective pressure that the HbS gene, only beneficial in a heterozygous state (Laland, 2008), was able to reach incredibly high frequencies for an otherwise fitness reducing, even lethal, gene (Mansilla-Soto, Rivière, & Sadelain, 2011). This speaks volumes for the selective pressures that must have been present, as nothing but an incredibly strong selective environment would encourage the presence of a gene that is only beneficial to 50% of offspring (see Appendix 1).

Tuberculosis is another disease with a long history in human populations, with remains containing molecular traces of this infection being identified from as long ago as 3,000 BCE in Egypt (Zink et al., 2003). It is highly likely that the disease is much older than this, though the debate surrounding its history as a human pathogen is still underway (Smith, Hewinson, Kremer, Brosch, & Gordon, 2009). Recent work on SLC11A1 1729 + 55del4, an allele associated with tuberculosis resistance, has uncovered a positive correlation between the frequency of this gene and the length of urban history for a given population (Barnes, et al., 2011) (Figure 1). This is strong evidence for the above assertion that increased population density should increase disease load and thus select for individuals with resistance to problem infectious diseases.

Figure 1. Time since first urban settlement is displayed on the x-axis while frequency of the allele for tuberculosis resistance is displayed on the y-axis. Mathematical lines of best fit are as published in Barnes et al. (2011). Adapted from Barnes et al. (2011).

It is highly likely that selective pressure from other known population diseases has played a similar role in recent human evolution. Wang et al. (2006) identified at least a half-dozen genes relating to host-pathogen interaction in addition to those given above, some of which with functions that are not yet adequately understood. It is reasonable to predict that should future research into genes associated with resistance to other infectious diseases historically endemic to areas of high population, be carried out (see Conclusion for suggestions), further evidence of how cultural lifestyle changes can influence human biological evolution will be found.

Cultural Change and the Human Brain: How Sociality Shapes Our Genes

            Ultimately, living in social groups, especially those of the size and complexity characteristic of large agricultural settlements (and eventually cities), relied upon the ability of ancient humans to successfully interact with one another. If cultural innovations, such as agriculture and following this settlements and cities, have produced selective pressures sufficient to change our genes with regard to food digestion and disease resistance, it is sensible to infer that changes to genes relating to our neurophysiology, and thus interactive capacities, should also be present. The findings of Wang et al. (2006) and Laland (2008), among others,  seem to suggest just this.

While the brain expressed genes identified by Wang et al. (2006) are thought to have undergone rapid, recent selection, their functions are unfortunately as of yet unknown. Laland (2008), however, lists 29 recently selected genes thought to be related to nervous system and brain ontogeny, brain function and, importantly, language skills and learning. The role of learning and communication in cultural innovation is extremely important (Laland & Hoppitt, 2003), it is thus unsurprising that genes relating to such functions have undergone recent selection in light of the societal changes discussed prior.

Perhaps more interestingly, work within the last two years has identified potentially recent polymorphisms of a gene that may represent a genetic consequence of selective pressures generated by a cultural interaction style. Chiao & Blizinsky (2009) reported that the 5-HTTLPR gene, associated with serotonin reuptake and thus mood, is present in long and short alleles that are geographically distributed in a manner fairly consistent with our notions of collectivist and individualist cultures (Figure 2). The short allele, argued to be related to collectivist cultures (Chiao & Blizinsky, 2009), essentially allows less reuptake of serotonin at the synapses, much the same affect exerted by many of today’s common antidepressant and antianxiety drugs (Bullock, Manias, & Galbraith, 2006). This has the mean result of elevating mood and, as Chiao & Blizinksy (2009) argue, reducing rates of behaviour that are harmful to social harmony (and thus fitness reducing, for both the errant individual and the group).

Furthermore, Chiao & Blizinksy (2009), relating back to the previous section on infectious disease, propose that collectivism seems to correlate with populations with a history of high disease burden and argue that selection for collectivist behaviour is somehow protective in this regard. This remains to be explored more comprehensively and may well represent a case of correlation as opposed to causation. While the question of how societies come to be collectivist or individualist to begin with remains largely unanswered, this study does provide a relatively robust example of a relationship that exists between a gene and an observable cultural selective pressure.  It is conceivable that such pressures have exerted impacts on other genes relating to behaviour or cognition. Genes relating to other neurotransmitters, perhaps dopamine or gamma-amino butyric acid, seem likely targets given their role in the regulation of human emotional states.

Figure 2. Distribution of the S (short) allele of the 5-HTTLPR gene in relation to individualism-collectivism and prevalence of anxiety across countries. Adapted from Chiao & Blizinsky (2009).

Conclusion

            Utilising modern molecular techniques, it is evident that a considerable number of human genes have undergone recent and rapid change (Hawks, et al., 2007). Many of these changes are estimated to have occurred within the last 10,000 years (Hawks, et al., 2007), a period of great cultural change that saw the adoption of agriculture and as a consequence sedentary settlements that, in some cases, grew to become the first urban centres (Diamond, 1991). Generally, niche construction activities are undertaken by animals in order to reduce the impact of environmental change, and this was likely the case for the first Neolithic farmers (Laland, 2008; Richerson, et al., 2001). The flow on effects of agriculture and subsequent human cultural innovation, however, produced a novel and rapidly changing environment with selective pressures of its own. It could be argued that these culturally mediated selective pressures outstripped their ecological predecessors for selective sway, generating a range of genetic adaptations related to diet, resistance to disease and neurophysiology (Barnes, et al., 2011; Chiao & Blizinsky, 2009; Laland, 2008; Richerson, et al., 2010), at a rate possibly unmatched in prior Homo evolution.

As further studies of the human genome for signatures of recent evolutionary change are performed, it is anticipated that further evidence for this period of rapid evolution will be found in gene-culture coevolutionary studies. Of particular interest to future researchers might be genes associated with resistance to dietary diseases (diabetes, obesity and vitamin D deficiency), other diseases endemic to highly populated areas (smallpox, the black death, influenza and more recently, HIV/AIDS) and the search for further evidence of cognitive changes related to an increasingly social lifestyle, especially where tolerance of non-kin is concerned.

In closing, it should be mentioned here that the above model, for the sake of brevity, has not considered how a lack of agricultural culture would manifest in the genetics of hunter-gatherer societies. It is predicted that, far from refuting the above, populations with limited exposure to agriculture, and as a consequence sedentary settlements of high population density, should display recent reactive selection only in accordance with the magnitude of their exposure. Should this hypothesis hold, it would be both complementary to, and supportive of, the main argument here given.

References

Barnes, I., Duda, A., Pybus, O. G., & Thomas, M. G. (2011). ANCIENT URBANIZATION PREDICTS GENETIC RESISTANCE TO TUBERCULOSIS. Evolution, 65(3), 842-848.

Bullock, S., Manias, E., & Galbraith, A. (2006). Fundamentals of Pharmacology. Frenchs Forest: Pearson Australia.

Chiao, J. Y., & Blizinsky, K. D. (2009). Culture-gene coevolution of individualism-collectivism and the serotonin transporter gene. Proceedings of The Royal Society: Biological Sciences, 277, 529-537.

Diamond, J. (1991). Guns, Germs and Steel. London: Jonathan Cape.

Dietler, M. (2006). Alcohol: Anthropological/Archaeological Perspectives. Annual Review of Anthropology, 35, 229-249.

Enattah, N. S., Jensen, T. G. K., Nielsen, M., Lewinski, R., Kuokkanen, M., Rasinpera, H., et al. (2008). Independent Introduction of Two Lactase-Persistence Alleles into Human Populations Reflects Different History of Adaptation to Milk Culture. The American Journal of Human Genetics, 82, 57-72.

Feldman, M. W., & Cavalli-Sforza, L. L. (1976). Cultural and biological evolutionary processes, selection for a trait under complex transmission. Theoretical Population Biology, 9, 238-259.

Hawks, J., Wang, E. T., Cochran, G. M., Harpending, H. C., & Moyzis, R. K. (2007). Recent acceleration of human adaptive evolution. Proceedings of the National Academy of Sciences, 104(52), 20753-20758.

Laland, K. N. (2008). Exploring gene-cultural interactions: insights from handedness, sexual selection and niche-construction case studies. Philosophical Transactions of The Royal Society: Biological Sciences, 363, 3577-3589.

Laland, K. N., & Brown, G. R. (2011). Sense & Nonsense (2nd ed.). Oxford: Oxford.

Laland, K. N., & Hoppitt, W. (2003). Do animals have culture? Evolutionary Anthropology: Issues, News, and Reviews, 12(3), 150-159.

Laland, K. N., Odling-Smee, J., & Myles, S. (2010). How culture shaped the human genome: bring genetics and the human sciences together. Nature Reviews: Genetics, 11, 137-148.

Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R., & Gordon, J. I. (2008). Worlds within worlds: evolution of the vertebrate gut microbiota. [10.1038/nrmicro1978]. Nat Rev Micro, 6(10), 776-788.

Mansilla-Soto, J., Rivière, I., & Sadelain, M. (2011). Genetic strategies for the treatment of sickle cell anaemia. British Journal of Haematology, 154(6), 715-727.

Meisenberg, G. (2008). On the Time Scale of Human Evolution: Evidence for Recent Adaptive Evolution. Mankind Quarterly, 48(4), 407-444.

Peng, Y., Shi, H., Qi, X., Xiao, C., Zhong, H., Ma, R. Z., et al. (2010). The ADH1B Arg47His polymorphism in East Asian populations and expansion of rice domestication in history. BMC Evolutionary Biology, 10(15), 1-8.

Richerson, P. J., Boyd, R., & Bettinger, R. L. (2001). Was Agriculture Impossible During the Pleistocene but Mandatory During the Holocene? A Climate Change Hypothesis. American Antiquity, 66(3), 387-411.

Richerson, P. J., Boyd, R., & Henrich, J. (2010). Gene-culture coevolution in the age of genomics. Proceedings of the National Academy of Sciences, 107(Supplement 2), 8985-8992.

Smith, N., Hewinson, R., Kremer, K., Brosch, R., & Gordon, S. (2009). Myths and misconceptions: the origin and evolution of Mycobacterium tuberculosis. Microbiology, 7, 537-544.

Wang, E. T., Kodama, G., Baldi, P., & Moyzis, R. K. (2006). Global landscape of recent inferred Darwinian selection for Homo sapiens. Proceedings of the National Academy of Sciences of the United States of America, 103(1), 135-140.

Zink, A. R., Sola, C., Reichl, U., Grabner, W., Rastogi, N., Wolf, H., et al. (2003). Characterizatio of Mycobacterium tuberculosis Complex DNAs from Egyptian Mummies by Spoligotyping. Journal of Clinical Microbiology, 41(1), 359-367.

Appendix 1.

A cross between two parents heterozygous for the HbS gene will result, statistically in: 25% homozygous HbS (potentially lethal), 50% heterozygous HbS (protection against malaria) and 25% homozygous non-HbS (no malaria protection, under high disease burden potentially deadly). Similarly, a cross between a non-HbS homozygote and a heterozygote will produce 50% heterozygote offspring but with the other 50% being non-HbS homozygotes. A cross involving a HbS homozygote is less likely due to the deleterious nature of this genotype.

Fortunately, as the title suggests, I yet draw breath. Unfortunately, my work-load has been the kind of heavy that would give an anvil pause, thus the sparseness of my bloggery of late. I have popped up a bit I wrote this semester on metacognition in non-primates, but have several more posts to come in the next few weeks on a range of topics, mostly revolving around my new found love for gene-culture co-evolution and the work of the ever insightful K. Laland.

See you all soon!

Introduction

Few academic discussions have evoked such debate as those of what separates our species, Homo sapiens, from other animals and, thus, defines us as human. Differences of mind and cognitive capacity are often of central importance in such discussions with several mental capacities being considered uniquely human, or at least functioning in a uniquely human way if shared with other animals (domain generality versus specificity for example) (Premack, 2007). One such capacity that has traditionally been considered uniquely human is metacognition (Metcalfe & Shimamura, cited in Kornell, 2009, p. 11), the ability to form a second order thought in considering a first order thought, or put simply ‘having knowledge about knowledge’ (Terrace & Son, 2009). Metacognition has also been philosophically tied to concepts of higher-order consciousness and as such has been important in shaping concepts of human sentience (Edelman & Seth, 2009; Smith, 2009).

Surprisingly, however, despite a wide research base in human psychology, relatively little work has been done, until recently, to assess the metacognitive capacity, or lack thereof, of other animals. Is our attribution of this capacity to ourselves as unique justified? A growing body of research would suggest not. The majority of this modest body of work has focused on the identification of metacognition in primates with some, albeit hotly disputed, success (Couchman, Coutinho, Beran, & Smith, 2010; Smith, 2009; Smith, Shields, & Washburn, 2003; Suda-King, 2008). In identifying metacognition in primates, we have, through attempts to identify what makes us unique, found an unexpected and interesting cognitive homology in our nearest phylogenetic relatives. This discovery raises several larger questions with wider ramifications for comparative psychology, animal cognition and our understanding of the evolution of the brain and cognition, questions that have only recently began to be explored in earnest by scientists (Smith, 2009; Terrace & Son, 2009). Is this ability truly unique to we primates? If it is not, how far back along the phylogenetic tree does it extend? Or if it is present in other animals, is it a case of homoplasy rather than true homology?

The following essay shall consider these questions through, firstly, an explanation of the theory of metacognition and how it is applied, followed by an overview of the few works to focus on metacognition in non-primate animals (NPAs). Problems with past work on animal metacognition shall then be explored before going on to consider the implications of metacognition research in more distantly related taxa and offering recommendations of organisms of focus for further metacognitive study, taking cues from both comparative psychology and neuroscience.

Knowledge about Knowledge

As stated in the introduction, metacognition refers to the ability of an individual to have knowledge of knowledge, or as Terrace & Son (2009) describe it, form a mental representation of a mental representation. Human beings routinely do this when we discuss our feelings, in self-ascribing our mental states we build a secondary representation of a primary representation (Arango-Munoz, 2010). Expressions of uncertainty, especially regarding memory or in relation to an anticipated task, are also considered metacognitive activities as the individual is required to assess the accuracy (secondary representation) of a memory (primary representation) and in turn answer with certainty or with uncertainty (Terrace & Son, 2009). Edelman & Seth (2009) have also stated that a link may exist between this process and self-consciousness, an important factor in investigations of sentience in animals.

Kornell (2009), in agreement with the philosophy of Arango-Munoz (2010) (at least at the gross level of division), further stated that metacognition can be divided into two functional categories, the first being monitoring, the second being control. The monitoring category of metacognitive function is where an individual undergoes the process of forming second-order representations, as described prior (Kornell, 2009). The control category, particularly in the case of certainty judgments of memory, sees the individual act on secondary representations that indicate uncertainty, in order to reduce this uncertainty, or withdraw from the task (Kornell, 2009). An example of active uncertainty reduction could be someone deciding to re-check an instruction manual after deciding that they could not accurately recall instructions. This active seeking of clarification has been observed in primates also in the form of hint requests (Kornell, 2009; Terrace & Son, 2009) but has unfortunately not been seen in NPAs.

Despite the lack of evidence for active uncertainty reduction in NPAs, an ability that could be considered a strong indicator of metacognition as we understand it in humans, a small body of evidence has began to accumulate that suggests that some animals have the capacity to withdraw from affirmative answering, by declaring uncertainty, should they consider a given task too difficult (Terrace & Son, 2009). This can be considered a metacognitive response, as it requires the organism to assess its certainty and respond accordingly. How discrimination and metamemory tasks have been used to measure this in NPAs shall be discussed below.

The Search for Metacognition in Non-Primate Animals

Thus far, work on assessing metacognition in NPAs has focused primarily on three vertebrate species; the bottlenosed dolphin, the rat and the pigeon. Each of the works based on these organisms has utilised discrimination tasks, either utilising metamemory or not, of controlled difficulty, in order to elicit responses of uncertainty should the subject be capable of them.

In one of the first attempts to assess NPAs for metacognition, Smith et al. (1995) attempted to assess whether dolphins differed greatly from humans in their capacity to opt-out of difficult trials in order to move on to tasks with which they had a greater chance of success. This was achieved through having the subjects (human or dolphin) listen to a tone that could be classified as either ‘high’ or ‘low’, though the tone itself could range in frequency anywhere between these two extremes (Smith, et al., 1995). A correct response would result in reward, an incorrect response would lead to a time out. A third response, the uncertain response (UR), which triggered a new trial with guaranteed success, was also offered. Smith et al. (1995) found that in this trial, both humans and dolphins readily gave an UR to difficult trials (middle range frequencies) in order to move onto trials in which they were more likely to succeed. This was considered a metacognitive response as the animal was able to assess its certainty before responding (Smith, 2009), thus demonstrating the ability to form a second-order mental construct.

Foote & Crystal (2007) attempted a similar experiment utilising a more common model organism, the rat. In this experiment rats were offered rewards for successfully discriminating between sounds that could be deemed ‘long’ or ‘short’ (Foote & Crystal, 2007). If the animals selected the correct sound length, they were rewarded with six food pellets, while an incorrect answer yielded none. Foote & Crystal (2007) also offered the same third option seen in Smith et al. (1995), that of uncertainty, opting to end the trial for a smaller reward of three pellets. As with the dolphin trial, Foote & Crystal (2007) found that rats were also much more likely to opt for an UR in the case of difficult trials. These findings were further bolstered by the fact that Foote & Crystal (2007) also predicted, and found, that should an UR not be offered, accuracy during forced answers to difficult trials should be much lower than when an UR is offered. This gave weight to the conclusion of Foote & Crystal (2007), that rats were aware of their own cognitive state in a manner consistent with theories of metacognition, as if they were offered a chance to avoid high-risk, high-difficulty trials, they were likely to do so in order to increase their overall success.

Two notable pigeon based metacognition, or more specifically metamemory, experiments have been carried out, both reaching similar conclusions. The first, by Inman & Shettleworth (1999), set out to formulate a useful method of assessment of nonverbal animals for metamemory, using pigeons as a model. In this trial, pigeons were shown visual stimuli before being given the opportunity to identify these among distractors some time after initial exposure for a food reward (Inman & Shettleworth, 1999). While they appeared to behave in a way consistent with metamemory, and thus metacognition, in their selection of the ‘safe’ option (similar to the UR in other trials) in relation to how much time had elapsed since first being shown the stimuli, they only did so after being shown the stimuli and distractors. Interestingly, the pigeons failed to commit to a trial or opt out in a way suggestive of metacognition if given this option before being shown the stimuli and distractors (Inman & Shettleworth, 1999). Inman & Shettleworth (1999) concluded that this inability to assess the accuracy of memory in anticipation of a trial was inconsistent with metacognition (the reasoning behind this shall be discussed below). Sutton & Shettleworth (2008) retested the assumptions of Inman & Shettleworth (1999) in the light of more recent and refined concepts of metacognition in non-humans and reached the same conclusion, that pigeons do not display metacognition.

Metacognition in NPAs: Problems, Perspectives and Prospects

As can be seen, two broadly different approaches have been taken in attempting to identify metacognition in NPAs. Firstly, as is seen in Smith et al. (1995) and Foote & Crystal (2007), discrimination trials that do not rely on memory have been used. Secondly, trials based on metamemory tasks have also been used, as seen in the pigeon based experiments of Inman & Shettleworth (1999) and Sutton & Shuttleworth (2008). This division between discrimination based tasks in the presence of the focal stimuli, termed ‘concurrent’ trials by Terrace & Son (2009), and metamemory trials based on assessment of memory accuracy, corresponds with an important schism in how metacognition is defined and applied to animal behaviour.

As discussed, both Smith et al. (1995) and Foote & Crystal (2007) have argued that the results of their concurrent discrimination trials are indicative of animal metacognition and awareness. Terrace & Son (2009) opposed this by arguing that the results of these experiments were at best ambiguous for the reason that the task was performed in the presence of the stimuli, allowing for simpler non-metacognitive explanations.  This concern was also expressed by Inman & Shettleworth (1999) in reference to the dolphin experiments of Smith et al. (1995).

The prime non-metacognitive process put forward as a plausible explanation for the results seen in the concurrent trials, was explained by Kornell (2009) in what was termed the ‘third response problem’. Kornell (2009) stated that it is possible that the animals under trial learned to associate middle-range stimuli with the third response, rendering it simply a conditioned choice made in order to obtain a reward rather than a true UR indicative of metacognition and thus high-order consciousness. If this was the case, the behaviour observed neither proved nor disproved the presence of metacognition. In order to be more certain, Terrace & Son (2009) advised that such experiments should always attempt to assess retrospective or prospective metamemory (prospective metamemory being the task on which the pigeons failed), as they are better indicators of true metacognition than concurrent URs.

In more recent work, Smith (2009), contra Kornell (2009), Terrace & Son (2009) and the earlier opinions of Inman & Shettleworth (1999) asserts that the making of URs, is per se, evidence of metacognition. While Smith (2009) does not dispute that conditioning of the sort proposed above could occur, he does assert that the observed results, as a function of parsimony, are most likely true URs indicative of consciousness without necessitating the kinds of metamemory trials utilised by others.

Regardless of the technicalities of definition, it is evident that, whether partially or in full, some cognitive faculties we would have traditionally attributed only to ourselves, or to our nearest primate relatives, are present in some form in other animals of relatively distant relatedness (mammals with millions of years of divergence from our line). Future trials could, perhaps, attempt both concurrent and metamemory based trials in order to determine whether metacognition is present in a more comprehensive fashion and in doing so allow us to form more concrete assertions about its evolutionary past.

Future Directions in NPA Focused Metacognition Research

The evidence available for metacognition in NPAs raises interesting questions about the evolutionary history of this ability that could perhaps be answered through further exploration of the capabilities of animals other than those already discussed. These could be other mammal species in order to discover whether this is a ubiquitous mammalian trait, or more distantly related organisms, to either further push back the ‘metacognitive family tree’, or identify where distantly related organisms have developed this capacity as a function of convergent evolution.

Despite the fact that the only positive evidence for metacognition has been found in mammals (Terrace & Son, 2009), recent research on similarities between the brain structure of such vastly different creatures as the marine ragworm and the mouse has suggested that many organisms share more neural commonalities than we would have traditionally admitted (Strausfeld, 2010; Tomer, Denes, Tessmar-Raible, & Arendt, 2010). Does this suggest that cognitive functions like metacognition may also be more deeply ingrained phylogenetically than we had suspected? Additionally, convergence is a realistic scenario here also, as metacognition is considered an adaptive tool for maximising efficiency of behaviour (Sutton & Shettleworth, 2008), rendering it entirely possible that it arose separately on more than one occasion. Two animal groups of use to future research focused on the answering of these questions are the Corvids, the family of birds to include the ravens and crows, and molluscs of the order Octopoda.

The Corvids, in particular the ravens and crows, are well known for feats of memory and problem solving in lab settings (Edelman & Seth, 2009). Some groups of crows have even been observed to actively engage in tool construction in the wild (Edelman & Seth, 2009), another behaviour that has been considered uniquely human in the past. Tool production implies the ability to plan actions, a trait that along with metacognition is associated with high-order consciousness and sentience (Edelman & Seth, 2009). Despite the failure of the pigeon, another avian, to perform successfully in metacognitive tasks as defined by Inman & Shettleworth (1999) (though Smith, 2009, may disagree), Corvids may perform better. If the metamemory based definition of metacognition is to be followed this would indicate a positive case of metacognition occurring as a result of convergence (conversely, if the per se argument of Smith, 2009, were taken it could indicate a deep phylogenetic heritage). Should Corvids fail also, it would go some of the way to suggesting an absence of metacognitive capacity in birds.

Molluscs of the order Octopoda, the octopi, are also potentially good models for studies of metacognition. As with the Corvids, these animals, particularly the species Octopus vulgaris, have demonstrated incredible adaptability, problem solving capacity and memory in lab settings (Edelman & Seth, 2009). Additionally, this species has shown a surprising capacity for observational learning and retention, demonstrating a greater affinity for learning from fellows than through conditioning (Fiorito & Scotto, 1992). Should metacognition be present in Octopus vulgaris, explanations other than convergence would be extremely difficult to propose given the exceptional phylogenetic distance of this species from the vertebrates studied so far.

Conclusion

In our attempts to identify what makes us unique, especially cognitively, we have discovered numerous, surprising functional analogues in animals. While the majority of these have been found in our nearest primate relatives, one cognitive capacity, that of ‘having knowledge about knowledge’, metacognition, has been identified, at least tentatively, in other mammal species of quite distant relation to ourselves. Unfortunately, however, due to differences of definition of behaviour indicative of metacognition, and a sheer lack of data, we are unable to readily explore the evolutionary history of this cognitive capacity. Should researchers come to some agreement on how to define this capacity, important as it is to our notions of sentience as they stand, perhaps future investigations of other, more distantly related, animals will yield some greater understanding of how widespread this faculty is and how, via homology or homoplasy, it came to be so.

References

Arango-Munoz, S. (2010). Two Levels of Metacognition. Philosophia, 39, 71-82.

Couchman, J. J., Coutinho, M. V. C., Beran, M. J., & Smith, D. J. (2010). Beyond Stimulus Cues and Reinforcement Signals: A New Approach to Animal Metacognition. Journal of Comparative Psychology, 124(4), 356-368.

Edelman, D. B., & Seth, A. K. (2009). Animal consciousness: a synthetic approach. Trends in Neurosciences, 32(9), 476-484.

Fiorito, G., & Scotto, P. (1992). Observational Learning in Octopus vulgaris. Science, 256, 545-547.

Foote, A. L., & Crystal, J. D. (2007). Metacognition in the Rat. Current Biology, 17(6), 551-555.

Inman, A., & Shettleworth, S. J. (1999). Detecting Metamemory in Nonverbal Subjects: A Test With Pigeons. Journal of Experimental Psychology, 25(3), 389-395.

Kornell, N. (2009). Metacognition in Humans and Animals. Current Directions in Psychological Science, 18(1), 11-15.

Leal, M., & Powell, B. (2011). Behavioural flexibility and problem solving in a tropical lizard. Biology Letters.

Metcalfe, J., & Shimamura, A. P. (1994). Metacognition: Knowing about knowing. Cambridge, MA: MIT Press.

Premack, D. (2007). Human and animal cognition: Continuity and discontinuity. Proceedings of the National Academy of Sciences, 104(35), 13861-13867.

Smith, J. D. (2009). The study of animal metacognition. Trends in Cognitive Sciences, 13(9), 389-396.

Smith, J. D., Schull, J., Strote, J., McGee, K., Egnor, R., & Erb, L. (1995). The Uncertain Response in the Bottlenosed Dolphin (Tursiops truncatus). Journal of Experimental Psychology, 124(4), 391-408.

Smith, J. D., Shields, W. E., & Washburn, D. A. (2003). The comparative psychology of uncertainty monitoring and metacognition. Behavioral and Brain Sciences, 26, 317-373.

Strausfeld, N. J. (2010). Brian Homology: Dohrn of a New Era? Brain, Behavior and Evolution, 76, 165-167.

Suda-King, C. (2008). Do orangutans (Pongo pygmaeus) know when they do not remember? Animal Cognition, 11, 21-42.

Sutton, J. E., & Shettleworth, S. J. (2008). Memory Without Awareness: Pigeons Do Not Show Metamemory in Delayed Matching to Sample. Journal of Experimental Psychology, 34(6), 266-282.

Terrace, H. S., & Son, L. K. (2009). Comparative metacognition. Current Opinion in Neurobiology, 19(1), 67-74.

Tomer, R., Denes, A. S., Tessmar-Raible, K., & Arendt, D. (2010). Profiling by Image Registration Reveals Common Origin of Annelid Mushroom Bodies and Vertebrate Pallium. Cell, 142(5), 800-809.

I’ve been too snowed under to write anything interesting of late (despite having read dozens of terrific articles!), so I thought I would share this wonderful lecture by John Hawks. His stance on the speed of human evolution has been quite a paradigm changer. To those of you who believe that one of the defining features of modern Homo sapiens is a large brain, pay close attention to the early part of his lecture. Turns out your ancient ancestors may have put you to shame.

Enjoy!

The general issue is as follows. I will explain how it affects both sides of this argument shortly.

As a post-graduate in the field of biological anthropology with a firm background in biology, and as a consequence the rudiments of genetics, I’m acutely aware of pleiotropy, epistasis, allometry and other factors that can see a given gene influencing multiple phenotypic traits, genes influencing one another and morphological traits affecting each other out of mechanical necessity. In short, I’m cautious about viewing a given trait (physical or behavioural should someone believe it to have some non-environmental basis) and exclaiming ‘this trait was selected for by natural selection and must therefore have a survival function’, this survival function fallacy births innumerable evolutionary scenarios that are likely to be absolute garbage. When wrangling with evolutionary ideas for a given organism I find it useful to have one of two approaches.

1) This is the most desirable approach though it is very rarely practical. Work from the genes up. Gene x produces protein y that influences cells of type a, b and c and thus tissue type z and so on and so forth. From this perspective one can see where the genetic influence begins to wane and the environmental factors begin to have more influence. Think of a connective tissue disorder as a convenient example, like Marfan syndrome, where a problem gene causes defective fibrillin produciton. This single gene, coding for a single protein, has multiple phenotypic effects that are then acted upon by the environment. I stress here that this same principle applies to genetic influencers of behaviour, a gene relating to a neural structure that has survival benefits would also drag with it numerous other effects that can be neutral or even slightly negative providing the cost doesn’t outweigh the benefit. Taking a magnifying glass to one of the incidental traits (what Gould would have called a ‘spandrel’) and looking for an evolutionary scenario that fits its selection is participating in the survival function fallacy.

2) Don’t start with the organism, start with the environment. If you cannot work from the genes up, work from the ecosystem down. Before conjuring evolutionary explanations for traits in a given organism, first make sure its environment is understood. This may help to sort important traits from those that are simply coincidental (pleiotropic perhaps etc.). Choose virtually any book on human evolution and you will see the consequences of starting the analysis with the organism. Scientists who start with any given hominin’s remains and then try to impose environments onto these remains will have a hard time sorting the wheat from the chaff, often with laughable results that damage reputations and waste the time of researchers and readers alike.

Gould & Lewontin summed up the perils of an ‘adaptionist’ approach very nicely in their 1979 paper ‘The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptionist programme’.

So, how does all of this relate to the work of those looking for the biological or genetic bases of behaviour? Put simply, are we really sure that any given behavioural pattern or what the ethologists would have called ‘instinct’ (convenient language, this is an outmoded notion) HAS a survival function? Was it simply pulled along with something that did? Is it a spandrel? This is perhaps my greatest criticism of a field of work that I do, otherwise, have great faith in. Workers in modern sociobiology and its offspring could perhaps benefit from working from one of the two approaches I outlined above.

As for the opponents of sociobiology of any modern type under whatever monicker it now takes (behavioural ecology, evolutionary psychology, gene-culture co-evolution etc.), I find a slightly different criticism for their approach which also relates to an understanding of genetics. Firstly, as any good geneticist or biologist of current times will stress, no modern day researcher in these fields truly believes in the false dichotomy of nature or nature. It is agreed upon that there are biological components and environmental components, the question is a matter of scale. Secondly, something I see time and time again in the criticisms of biological approaches to understanding behaviour is this old chestnut ‘the gene to phenotype to selection model of natural selection when applied to behaviour ignores choice, culture and other human attributes’. As mentioned above, this view of genetics is at its most innocent a gross simplification and at its worst absolutely erroneous. Unfortunately it is also widespread on both sides of the fence. Being erroneous, it is of course, not the basis of a good argument for or against anything. I also will reiterate here that no good biologist or biological anthropologist denies the role of culture and choice in shaping human beings, even with the numerous models for the survival function of culture and ideas about comparative cognition. Suffice it to say, meme models and comparative cognitive studies, if carried our responsibly, do not have to damage our concept of free will or our pride as a species.

Time will tell how things progress in this field, and I will be watching closely. I will provide a further exploration of this idea next week with an example from real world research, the work of Belyaev on the domestication of silver foxes.

1) It would appear that in our early bipedal ancestors, and indeed cousins in the case of P. robustus,  it was more common for females to disperse from their place of birth and ally themselves with other ‘troops’ (for want of a better word) than it was for males. Males it would seem, enjoyed something of a ‘stay at home father’ lifestyle and had only relatively small ranges. This is in agreeance with what is seen in many modern human societies and those of our close extant relatives like the chimpanzees and bonobos (but not gorillas or other primates).

2) With the above point in mind, this challenges the notion that bipedalism evolved as a consequence of an increased need to move long distances, the so-called ‘endurance’ theories. Given my personal leanings toward the wading model put forward by Niemitz in Naturwissenschaften in 2007 and general unease with the unconvincing evidence for the endurance models I found these findings in Nature both exciting and in the best possible sense unsurprising.

There are of course other interpretations that are possible, such as the small home range being an example of a preferred habitat (cave-dwelling). If this were the case the species in question may roam further under more general circumstances but I find that unlikely. I anticipate that future evidence will support the ‘small range’ idea above as a general behavioural truth about our ancestors.

Citation:

“Strontium isotope evidence for landscape use by early hominins”

Copeland, S., Sponheimer, M., Ruiter, D., Lee-Thorp, J., Codron, D., Roux, P., Grimes, V. & Richards, M.

NatureVolume: 474, Pages:76–78 Date published:(02 June 2011)

Tracy, J., Hart, J. & Martens, J.

PLoS ONE 6(3) 2011

I’m not usually in the business of commenting on psychology papers, but for this one I’ll make an exception. Partially because it is an interesting experiment but mostly because intelligent design is about as intelligent as the average tuber. In short, the experiment demonstrates that if people have been contemplating death, they are more likely to favour the work of Michael Behe, an intelligent design (ID) proponent (and shamefully a scientist, though how he justifies calling himself both that AND an ID supporter only his imaginary friend on the clouds knows) than that of Richard Dawkins (no introduction necessary). Disappointing but understandable in some ways, everyone worries about death, especially the ones who tell you that they don’t, and it is much nicer to think that out there somewhere is someone/thing who will be waiting for you to tell you that everything will be alright, stroke your hair and buy you an ice-cream cone.

Thinking something is nice, however, doesn’t make it real. I’ve read a few fantasy novels in my day, I think the existence of dragons would be sweet, yet you don’t see me starting any expeditions to battle them all armoured and atop a steed, nor would you any other rational human being. But anything to do with old mate in the sky and people simply abandon their ability to reason because they are a bit scared of something. So scared that they will dedicate a whole life to placating this fear. I’m just as afraid of death as anyone else. I don’t know what will happen when I die and nor does anyone else, anyone who says otherwise is a charlatan. I’ll most likely just be gone, absent, much as I was before I was born. So I focus on life. My life is about science, science is about objective and universal truths, these truths are unaltered by my life or death. These are truths with or without the contextualising lens of culture. They are bigger than I am. See how I did that? I just found meaning in cold, hard, analytical science. No spacemen or magicians or dubious historical figures, no blokes in weird hats or bronze age literature. A fear of death doesn’t need to become a life long preoccupation.

Religion is setting mankind back, not moving us forward. To quote Bill Maher, “Grow up or die”. Sounds extreme, but take a look at the world. If you don’t think our tendency toward generating and then believing our own most illogical and self destroying phantasms is stinking up the place then you need to look a bit harder. Not just at the world today but at our history.

Hey, look, I know this post was more of a tirade than usual, but I don’t feel the need to be polite about religion. While religous organisations (and in turn the beliefs they peddle) often gain a tax exempt status, they are not exempt from objective analysis. If I have offended you I am empathetic, but not apologetic. No, the bible nor any other ‘holy’ book is not a valid defense, they are just books, there is no evidence to the contrary. I know some may claim to have ‘experienced’ god but many also claim to have ‘experienced’ alien abduction and we don’t take them very seriously (even where they have evidence, albeit dubious, where you have none). You can blame the space invading evangelicals on my campus for firing me up on this. It’s just such a pity to see otherwise intelligent people, people who have the capacity to do some real good for example; become a nurse, contribute to art, work for charity (non-religious), discover a treatment for a genetic disease or even just make really great hot-dogs, throwing away the only life they will get on pleasing a moody and judgmental invisible man/being/thing/whatever, that they have never met nor have any evidence even exists, essentially based on the fear of something they cannot change.