Abstract

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The hypothesis is forwarded that tolerance to our faeces smell is due to the presence in the scent of our own HLA molecules which are different in any individual . With the exception of identical twins each individual may therefore tolerate only its smell . The reasons supporting this explanation are discussed.

Introduction

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Everybody knows that the scent of the human faeces is disgusting and often intolerable . The only exception is the scent of the own faeces which is always tolerable and in certain cases even agreeable. It is quite evident that our smell is not better than the other people’s smell . We may easily understand by the odour the condition and the variation of our digestion and also when our smell is particularly disgusting for other people, but for us is always tolerable. At my best knowledge no explanation exists of this paradoxical situation. Habituation cannot be an explanation since our faeces are continuously changing smell since it is produced by the intestinal flora which is changing in dependence of food and other variables and surely we cannot habituate to all its possible variations. Furthermore we should suppose that our faeces smells is effectively different by that of all other persons and this is hard to believe and also apparently impossible because the smelling products of the intestinal flora are limited in number. I here suggest the hypothesis that we are tolerant to our faeces smell since in addition to the major components of the smell, mainly methylsulfide compounds (1 ),there is the odour of our Histocompatibility Leukocyte Antigen complex (HLA the name in humans of the Major Histocompatibility Complex ,MHC, in animals) which is absolutely unique for each individual. According the hypothesis the bacterial component of our faecal odour is identical to that of the other persons but differs for us because only in our faeces all the components of our HLA system are present and these are capable to make tolerable the smell of the bacterial flora . In conclusion , considering the HLA each individual has its own faecal odour different by that of all other individuals: the bacterial component is identical but the HLA component is different.

Main Text

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Why I suggest the HLA complex? More than 30 genes codify for number of phenotypes.the proteins of the HLA complex(for a review see 2). These proteins are divided in two groups: class I HLA are composed by a single protein and are found on the surface of all nucleated cells. Class II molecules are the product of one alpha and one beta gene and are found on the surface of the antigen presenting cells. High polymorphism is hallmark of the MHC in all vertebrates and of HLA in man. More than 2400 different alleles have been detected in class I antigens up to 2009 and a much higher number in class II genes (2 ).Based on the number of alleles identified in humans more than 17x 106 different combinations of HLA class I could exist and of course, considering the heterozigosity, a much higher. The result is that is impossible to find in the general population two persons with an identical HLA complex except for identical twins. This is a unique characteristic of the HLA system , the polymorphism of all other protein systems being order of magnitude lower than that of the HLA system. Because each human tolerate only the odour of his own faeces that means that the genetic system conferring his property must be extremely polymorphic , otherwise we should frequently encounter other persons sharing the same complex and we should tolerate the scent of his faeces , but even in absence of any statistic on this topic is a common experience of everybody that we tolerate only our own smell. These considerations makes likely that our tolerance may be determined only by the HLA system. It is possible for our olfactory system to detect the various HLA odours? All the previous considerations are valid only if we are able to detect and distinguish with the olfaction the different HLA phenotypes . For a long time the function of MHC and HLA have been considered only the immune response and regulation . Almost 35 years ago it was shown that genes at MHC loci influence behavioural decisions in mice controlling the mating preferences (3,4 ). Subsequently it became clear that MHC genes have similar role in fishes , birds and humans (for a review see 5 ).Further researches have established that in all these animals and in man the social behaviour was determined in part by MHC specific odour recognition ( in the urine in mouse and in the sweat in man ). In mice and even in humans clear-cut evidence exists that an individual can sense the composition and compatibility of immune system molecules of a cospecific with direct consequences on social behaviour (5 ). In mouse the Bruce effect conclusively demonstrate that all possible MHC phenotypes may be recognized by olfaction. The Bruce effect or pregnancy block (6 ) refers to the tendency for female rodents to terminate their pregnancies following exposure to the scent of an unfamiliar male (7 ). Because MHC molecules are transmembrane molecules they must be proteolitically shed from the cell surface to appear in the body fluids and is therefore difficult that the MHC molecules themselves are chemosignals. The MHC peptide ligands must be considered the most likely candidates for individuality signals . The olfactory assessment of MHC peptides at the level of individual neurons was examined in mice showing that MHC small peptides activate in a specific manner the two parts of the olfactory system , the vomeronasal organ and the main olfactory epithelium (8,9 ). The change of a single aminoacid in the peptide may change or even abolish the signal recognition . Even if there is a strong evidence that MHC peptides may be directly and specifically recognized by the olfactory system of mice till a concentration of 10-12M because the odortype identity can be detected by a distance some authors believe that MHC influences the concentration of volatile compounds in the urine of mice (12 ). At any rate mice through non volatile signals perhaps along with volatile one are capable of discriminate the MHC genotypes . In faeces it seems almost impossible that the different HL genotypes may influence the concentration of volatile compounds made by the bacterial flora . How the hypothesis may be tested? A direct demonstration is extremely difficult .Even in small inbred populations like Hutterites studied by Ober ( ) in which the HLA polymorphism is strongly reduced I think that is almost impossible to find two individuals sharing the same HLA alleles and that , according the hypothesis , should reciprocally tolerate their faecal scent. It is instead relatively easy to have a striking demonstration that the tolerance is genetically determined : Identical twins should reciprocally tolerate their faecal scent while dizygotic twins should not. Evidence already exists that odours of identical twins ( but not of dizygotic twins ) can be matched by human sniffers at rates better than chance , even when the twins are living apart. In addition , matching frequencies for identical twins odours were not significantly different from those for duplicate odours from the same individual(13) Even if positive this research would not strictly demonstrate that HLA identity is responsible of the phenomenon because all the genetic systems of twins are identical. It must be remembered however that the HLA system is the only genetic system which has enough polymorphism to account for the phenomenon . Perhaps a further interesting possibility would be to mix an extract of some our tissue, for instance blood with the source of some bad smell to see if we can tolerate it. The biological meaning of the tolerance It is generally accepted that a bad smell often indicate a dangerous product while good odours indicate non dangerous or useful substances (14 ). For instance for us one of the worst smell is the putrefaction sscent which indicate the presence of a cadaver , a clear signal of danger. The same scent is an exquisite perfume for vultures as indicates a source of food. There exception to this rule but are often a clear instance of olfactory mimicry. Some carnivorous plant emit from the leaves perfume of flowers to attract insects and many non dangerous animals emit disagreeable odours to discourage carnivores. The faeces of other people are dangerous for us as are a possible source of infection ; Our own faeces cannot surely be a source of infection for ourselves.We may appreciate by the scent the condition of our digestion but even when is bad we have no problem in tolerate it because never is dangerous for us. A second point is that tolerance of our scent surely strongly improve our life ( which otherwise would be intolerable) and evolutionary this could improve our fitness.

References

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(1) Moore JG, et al. Gas -chromatographic and mass- spectrometric analysis of the odor of human feces Gastroenterology;1987, 93: 1321-9 (2) Shankarkumar U. The Human Leukocyte Antigen (HLA) system Int J Hum Genet 2004; 4: 91-103 (3)Yamazaki K et al.Control of mating preferences in mice by genes in the major histocompatibility complex J exp med 1976; 144: 1324-35 (4)Penn D , Potts W. How do major histocompatibility complex genes influence odor and mating preferences? Adv Immunol 1998; 69: 411-36 (5) Boehm T, Zufall F MHC peptides and the sensory evaluation of genotype Trends in Neurosciences 2006; 29: 100-7 (6) Bruce HM An exteroreceptive block to pregnancy in the mouse Nature 1959; 184: 105 (7) Zufall F, Lenders- Zufall T. Mammalian pheroormone sensing Curr Op Neurobiol 2007; 17: 483-9 (8) Leinders-Zufall T et al.MHC class I peptides as chemosensory signals in the vomeronasal organ Science 2004;305: 1033-37 (9) Slev PR et al. Sensory neurons with MHC-like peptide binding properties : disease consequences Curr Op Immunol 2006; 18: 608-16 (10) Kwak J et al. In search for chemical basis for MHC odourtypes Proc Biol Sci 2010; 277:2417-25 (11) Kwak J et al. Major histocompatibility complex-regulated odortypes: peptide free urinary volatile signals Physiol & Behavior 2009; 96: 184-88 (12) Weitkamp LR, Ober C . Ancestral and recombinant 16-locus HLA haplotypes in the Hutterites Immunogenet 1999;49: 491-7 (13) Roberts SC et al . Body odor similarity in noncohabiting twins Chem Senses 2005; 30: 651-6 (14) Stevenson RJ. An initial Evaluation of the functions of human olfaction Chem Senses 2010; 35: 3-20

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