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Detecting the Smell of Disease and Injury: Scoping Evolutionary and Ecological Implications

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Chemical Signals in Vertebrates 14

Abstract

Sickness , along with most other health conditions , smell ; and in order to avoid infection and contamination , humans and other animals alike have evolved to find these odours repugnant . Indeed, so evolved is the selective advantage offered by detecting disease , that even changes to metabolites triggered by immune and stress responses are detectable. Here, we first review mechanisms of how different health conditions can modify host odour profiles, and how these changes can affect social interactions in general. In the second part, we focus on the two contexts that render individuals most vulnerable to evolutionary selection pressures: reproduction and predation . Linked to sexual selection and inter-specific eavesdropping , we discuss the ecological and game-theoretic consequences of olfactory detectability of health conditions, where we use examples from the published literature to illustrate what host behaviours may have evolved to avoid and/or conceal their disadvantageous odour changes.

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References

  • Ackerl K, Atzmueller M, Grammer K (2002) The scent of fear. Neuroendocrinol Let 23(2):79–84

    Google Scholar 

  • Albone ES, Perry GC (1976) Anal sac secretion of the red fox, Vulpes vulpes; volatile fatty acids and diamines: implications for a fermentation hypothesis of chemical recognition. J Chem Ecol 2(1):101–111

    Article  CAS  Google Scholar 

  • Amundsen T, Sundstrøm S, Buvik T, Gederaas OA, Haaverstad R (2014) Can dogs smell lung cancer? First study using exhaled breath and urine screening in unselected patients with suspected lung cancer. Acta Oncol 53(3):307–315

    Article  PubMed  Google Scholar 

  • Arakawa H, Cruz S, Deak T (2011) From models to mechanisms: odorant communication as a key determinant of social behavior in rodents during illness-associated states. Neurosc Biobehav Rev 35(9):1916–1928

    Article  Google Scholar 

  • Aubert A (1999) Sickness and behaviour in animals: a motivational perspective. Neurosc Biobehav Rev 23(7):1029–1036

    Article  CAS  Google Scholar 

  • Barreto RE, Miyai CA, Sanches FHC, Giaquinto PC, Delicio HC, Volpato GL (2013) Blood cues induce antipredator behavior in Nile tilapia conspecifics. PLoS ONE 8(1):e54642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernard JF, Bester H, Besson JM (1996) Involvement of the spino-parabrachio-amygdaloid and-hypothalamic pathways in the autonomic and affective emotional aspects of pain. In: Progress in brain research, vol 107. Elsevier, pp 243–255

    Google Scholar 

  • Boccia ML (1983) A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys. Int J Primatol 4(4):399–418

    Article  Google Scholar 

  • Bodner L (1991) Effect of parotid submandibular and sublingual saliva on wound healing in rats. Comp Biochem Physiol A 100(4):887–890

    Article  CAS  PubMed  Google Scholar 

  • Brown RE, Macdonald DW (eds) (1985) Social ddours in mammals. Clarendon Press, Oxford

    Google Scholar 

  • Brown RE, Schellinck HM (1995) Effects of selective depletion of gut bacteria on the odours of individuality in rats. In: Apfelbach R, Muller-Schwarze D, Reutter K, Weiler E (eds) Chemical signals in vertebrates 7. Pergamon Press, New York, pp 267–271

    Google Scholar 

  • Budgett HM, Edwards L (1933) Hunting by scent. Charles Scribner’s Sons

    Google Scholar 

  • Buesching CD, Jordan N (2019) Chapter 8: the social function of latrines: a hypothesis-driven research approach. In: Buesching CD, Mueller CT (eds) Chemical signals in vertebrates 14. Springer, Cham

    Chapter  Google Scholar 

  • Burghardt GM (1970) Intraspecific geographical variation in chemical food cue preferences of newborn garter snakes (Thamnophis sirtalis). Behaviour 36(3)

    Article  Google Scholar 

  • Cocke R, Del Thiessen D (1986) Chemocommunication among prey and predator species. Anim Learn Behav 14(1):90–92

    Article  Google Scholar 

  • Conte MP, Schippa S, Zamboni I, Penta M, Chiarini F, Seganti L, Osborn J, Falconieri P, Borrelli O, Cucchiara S (2006) Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut 55(12):1760–1767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornu JN, Cancel-Tassin G, Ondet V, Girardet C, Cussenot O (2011) Olfactory detection of prostate cancer by dogs sniffing urine: a step forward in early diagnosis. Europ Urol 59(2):197–201

    Article  Google Scholar 

  • Corrêa-de-Santana E, Paez-Pereda M, Theodoropoulou M, Nihei OK, Gruebler Y, Bozza M, Arzt E, Villa-Verde DMS, Renner U, Stalla J, Stalla GK (2006) Hypothalamus–pituitary–adrenal axis during Trypanosoma cruzi acute infection in mice. J Neuroimmunol 173(1–2):12–22

    Article  PubMed  CAS  Google Scholar 

  • Curtis VA (2014) Infection-avoidance behaviour in humans and other animals. Tr Immunol 35(10):457–464

    Article  CAS  Google Scholar 

  • Cushing BS (1984) A selective preference by least weasels for oestrous versus dioestrous urine of prairie deer mice. Anim Behav 32(4):1263–1265

    Article  Google Scholar 

  • Dantzer R (2001) Cytokine-induced sickness behavior: mechanisms and implications. Ann NY Acad Sci 933(1):222–234

    Article  CAS  PubMed  Google Scholar 

  • Dehnhard M (2011) Mammal semiochemicals: understanding pheromones and signature mixtures for better zoo-animal husbandry and conservation. Int Zoo Yearb 45(1):55–79

    Article  Google Scholar 

  • Edwards JC, Barnard CJ (1987) The effects of Trichinella infection on intersexual interactions between mice. Anim Behav 35(2):533–540

    Article  Google Scholar 

  • Ehman KD, Scott ME (2001) Urinary odour preferences of MHC congenic female mice, Mus domesticus: implications for kin recognition and detection of parasitized males. Anim Behav 62(4):781–789

    Article  Google Scholar 

  • Ezenwa VO, Williams AE (2014) Microbes and animal olfactory communication: where do we go from here? Bioessays 36(9):847–854

    Article  PubMed  Google Scholar 

  • Fialová J, Roberts SC, Havlíček J (2016) Consumption of garlic positively affects hedonic perception of axillary body odour. Appetite 97:8–15

    Article  PubMed  Google Scholar 

  • Fiore M, Aloe L (2001) Neuroinflammatory implication of Schistosoma mansoni infection in the mouse. Arc Physiol Biochem 109(4):361–364

    Article  CAS  Google Scholar 

  • Fourie CE (2012) Vigilance behaviour and its endocrine correlates in Plains zebra (Equus burchelli) living in a predator-free landscape (Doct diss), Univ Pretoria

    Google Scholar 

  • Gable TD, Windels SK, Bruggink JG, Homkes AT (2016) Where and how wolves (Canis lupus) kill beavers (Castor canadensis). PLoS ONE 11(12):e0165537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Galef BG (1987) Social influences on the identification of toxic foods by Norway rats. Anim Learn Behav 15(3):327–332

    Article  Google Scholar 

  • Gosling LM, Petrie M (1981) The economics of social organization. In: Townsend CR, Calow P (eds) Physiological ecology. Blackwell Scientific Publications, Oxford, pp 315–345

    Google Scholar 

  • Guerrero-Flores H, Apresa-García T, Garay-Villar Ó, Sánchez-Pérez A, Flores-Villegas D, Bandera-Calderón A, García-Palacios R, Rojas-Sánchez T, Romero-Morelos P, Sánchez-Albor V, Mata O (2017) A non-invasive tool for detecting cervical cancer odor by trained scent dogs. BMC Cancer 17(1):79

    Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218(4570):384–387

    Article  CAS  PubMed  Google Scholar 

  • Hammer RP Jr, Zhou L, Cheung S (1994) Gonadal steroid hormones and hypothalamic opioid circuitry. Horm Behav 28(4):431–437

    Article  CAS  PubMed  Google Scholar 

  • Hardin DS, Anderson W, Cattet J (2015) Dogs can be successfully trained to alert to hypoglycemia samples from patients with type 1 diabetes. Diab Ther 6(4):509–517

    Article  CAS  Google Scholar 

  • Hart BL, Powell KL (1990) Antibacterial properties of saliva: role in maternal periparturient grooming and in licking wounds. Physiol Behav 48(3):383–386

    Article  CAS  PubMed  Google Scholar 

  • Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol:681–692

    Article  Google Scholar 

  • Hughes NK, Kelley JL, Banks PB (2009) Receiving behaviour is sensitive to risks from eavesdropping predators. Oecolog 160(3):609–617

    Article  Google Scholar 

  • Hughes NK, Korpimäki E, Banks PB (2010) The predation risks of interspecific eavesdropping: weasel–vole interactions. Oikos 119(7):1210–1216

    Article  Google Scholar 

  • Hurst JL, Beynon RJ (2004) Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26(12):1288–1298

    Article  CAS  PubMed  Google Scholar 

  • Kavaliers M, Colwell DD (1993) Aversive responses of female mice to the odors of parasitized males: neuromodulatory mechanisms and implications for mate choice. Ethology 95(3):202–212

    Article  Google Scholar 

  • Kavaliers M, Colwell DD (1995a) Discrimination by female mice between the odours of parasitized and non-parasitized males. Proc R Soc Lond B 261(1360):31–35

    Article  CAS  Google Scholar 

  • Kavaliers M, Colwell DD (1995b) Odours of parasitized males induce aversive responses in female mice. Anim Behav 50(5):1161–1169

    Article  Google Scholar 

  • Kavaliers M, Fudge MA, Colwell DD, Choleris E (2003) Aversive and avoidance responses of female mice to the odors of males infected with an ectoparasite and the effects of prior familiarity. Behav Ecol Sociobiol 54(5):423–430

    Article  Google Scholar 

  • Kavaliers M, Choleris E, Pfaff DW (2005) Genes, odours and the recognition of parasitized individuals by rodents. Tr Parasitol 21(9):423–429

    Article  CAS  Google Scholar 

  • Kent S, Bluthe RM, Dantzer R, Hardwick AJ, Kelley KW, Rothwell NJ, Vannice JL (1992) Different receptor mechanisms mediate the pyrogenic and behavioral effects of interleukin 1. Proc Nat Acad Sci 89(19):9117–9120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kent A, Ehlers B, Mendum T, Newman C, Macdonald DW, Chambers M, Buesching CD (2018) Genital tract screening finds widespread infection with Mustelid Gammaherpesvirus 1 in the European Badger (Meles meles). J Wildl Dis 54(1):133–137

    Article  CAS  PubMed  Google Scholar 

  • Kim JJ, Jung MW (2018) Fear paradigms: the times they are a-changin’. Curr Op Behav Sci 24:38–43

    Article  Google Scholar 

  • Klein SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79(3):441–449

    Article  CAS  PubMed  Google Scholar 

  • Knapp LA, Robson J, Waterhouse JS (2006) Olfactory signals and the MHC: a review and a case study in Lemur catta. Am J Primatol 68(6):568–584

    Article  CAS  PubMed  Google Scholar 

  • Kokko H, Ranta E, Ruxton G, Lundberg P (2002) Sexually transmitted disease and the evolution of mating systems. Evol 56(6):1091–1100

    Article  Google Scholar 

  • Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc Roy Soc Lond B 270(1515):653–664

    Article  Google Scholar 

  • Lee H, Noh J (2016) Pair exposure with conspecific during fear conditioning induces the link between freezing and passive avoidance behaviors in rats. Neurosci Res 108:40–45

    Article  PubMed  Google Scholar 

  • Leinders-Zufall T, Cockerham RE, Michalakis S, Biel M, Garbers DL, Reed RR, Zufall F, Munger SD (2007) Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc Nat Acad Sci 104(36):14507–14512

    Article  CAS  Google Scholar 

  • Lönnstedt OM, McCormick MI, Meekan MG, Ferrari MC, Chivers DP (2012) Learn and live: predator experience and feeding history determines prey behaviour and survival. Proc Roy Soc Lond B: rspb20112516

    Google Scholar 

  • Marks I (1988) Blood-injury phobia: a review. Am J Psych 145(10):1207

    Article  CAS  Google Scholar 

  • Meier AS, Bukusi EA, Cohen CR, Holmes KK (2006) Independent association of hygiene, socioeconomic status, and circumcision with reduced risk of HIV infection among Kenyan men. JAIDS 43(1):117–118

    PubMed  Google Scholar 

  • Morales-Montor J, Mohamed F, Ghaleb AM, Baig S, Hallal-Calleros C, Damian RT (2001) In vitro effects of hypothalamic–pituitary–adrenal axis (HPA) hormones on Schistosoma mansoni. J Parasitol 87(5):1132–1139

    CAS  PubMed  Google Scholar 

  • Moshkin M, Litvinova N, Litvinova EA, Bedareva A, Lutsyuk A, Gerlinskaya L (2012) Scent recognition of infected status in humans. J Sex Med 9(12):3211–3218

    Article  PubMed  Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford University Press, New York

    Google Scholar 

  • Müller-Schwarze D (1980) Chemical signals in alarm behavior of deer. In Chemical signals. Springer, Boston, MA, pp 39–51

    Chapter  Google Scholar 

  • Müller-Schwarze D (2016) Chemical signals in vertebrates 13: where we stand and what might be next. In: Chemical signals, vol 13. Springer, Boston, MA, pp 11–16

    Chapter  Google Scholar 

  • Nunn CL (2003) Behavioural defences against sexually transmitted diseases in primates. Anim Behav 66(1):37–48

    Article  Google Scholar 

  • Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. Tr Ecol Evol 13(10):391–396

    Article  CAS  Google Scholar 

  • Olsson MJ, Lundström JN, Kimball BA, Gordon AR, Karshikoff B, Hosseini N, Sorjonen K, Olgart Höglund C, Solares C, Soop A, Axelsson J (2014) The scent of disease: human body odor contains an early chemosensory cue of sickness. Psychol Sci 25(3):817–823

    Article  PubMed  Google Scholar 

  • Osterkamp J, Wahl U, Schmalfuss G, Haas W (1999) Host-odour recognition in two tick species is coded in a blend of vertebrate volatiles. J Comp Physiol 185(1):59–67

    Article  CAS  Google Scholar 

  • Pfeiffer W (1962) The fright reaction of fish. Biol Rev 37(4):495–511

    Article  CAS  PubMed  Google Scholar 

  • Pfister JA (1999) Behavioral strategies for coping with poisonous plants. In: Launchbaugh K, Sanders KD, Mosley JC (eds) Grazing behavior of livestock and wildlife. Idaho Forest, Wildlife, and Range Experimental Station Bulletin, vol 70, pp 45–59

    Google Scholar 

  • Poirotte C, Massol F, Herbert A, Willaume E, Bomo PM, Kappeler PM, Charpentier MJ (2017) Mandrills use olfaction to socially avoid parasitized conspecifics. Sci Adv 3(4):e1601721

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • SanMiguel A, Grice EA (2015) Interactions between host factors and the skin microbiome. Cell Mol Life Sci 72(8):1499–1515

    Article  CAS  PubMed  Google Scholar 

  • Schellinck HM, Brown RE, Slotnick BM (1991) Training rats to discriminate between the odors of individual conspecifics. Anim Learn Behav 19(3):223–233

    Article  Google Scholar 

  • Sonenshine DE (2004) Pheromones and other semiochemicals of ticks and their use in tick control. Parasitology 129(S1):S405–S425

    Article  CAS  PubMed  Google Scholar 

  • Stefano GB, Scharrer B, Smith EM, Hughes Jr TK, Magazine HI, Bilfinger TV, Hartman AR, Fricchione GL, Liu Y, Makman MH (1996) Opioid and opiate immunoregulatory processes. Crit Rev Immunol 16(2)

    Article  CAS  Google Scholar 

  • Stevenson RJ, Case TI, Oaten MJ (2011) Effect of self-reported sexual arousal on responses to sex-related and non-sex-related disgust cues. Arch Sex Behav 40(1):79–85

    Article  PubMed  Google Scholar 

  • Tester AL (1963) The role of olfaction in shark predation. Pacif Sci 17:148–170

    Google Scholar 

  • Theis KR, Venkataraman A, Dycus JA, Koonter KD, Schmitt-Matzen EN, Wagner AP, Holekamp KE, Schmidt TM (2013) Symbiotic bacteria appear to mediate hyena social odors. Proc Nat Acad Sci 110(49):19832–19837

    Article  CAS  Google Scholar 

  • Tomás G, Merino S, Moreno J, Morales J, Martinez-De La Puente J (2007) Impact of blood parasites on immunoglobulin level and parental effort: a medication field experiment on a wild passerine. Funct Ecol 21(1):125–133

    Article  Google Scholar 

  • Van Valen L (1977) The red queen. Am Nat 111(980):809–810

    Article  Google Scholar 

  • Villasanta U (1972) Complications of radiotherapy for carcinoma of the uterine cervix. Am J Obstetr Gynecol 114(6):717–726

    Article  CAS  Google Scholar 

  • Vyas A (2013) Parasite-augmented mate choice and reduction in innate fear in rats infected by Toxoplasma gondii. J Exp Biol 216(1):120–126

    Article  PubMed  Google Scholar 

  • Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM (2007) Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Nat Acad Sci 104(15):6442–6447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walkden-Brown SW, Restall BJ, Norton BW, Scaramuzzi RJ, Martin GB (1994) Effect of nutrition on seasonal patterns of LH, FSH and testosterone concentration, testicular mass, sebaceous gland volume and odour in Australian cashmere goats. Reproduction 102(2):351–360

    Article  CAS  Google Scholar 

  • Weibull JW (1997) Evolutionary game theory. MIT Press

    Google Scholar 

  • Zhao D, Zhang F, Zhang W, He J, Zhao Y, Sun J (2013) Prognostic role of hormone receptors in ovarian cancer: a systematic review and meta-analysis. Int J Gynecol Canc 23(1):25–33

    Article  Google Scholar 

  • Zeng XN, Leyden JJ, Spielman AI, Preti G (1996) Analysis of characteristic human female axillary odors: qualitative comparison to males. J Chem Ecol 22(2):237–257

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

C.N holds a H.N. Southern Memorial Fellowship in Ecology (at Lady Margaret Hall), and C.D.B. held a Research Fellowship from the Poleberry foundation.

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  1. Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, Recanati-Kaplan Centre, Tubney, Abingdon, Oxfordshire, UK

    Chris Newman & Christina D. Buesching

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  2. Christina D. Buesching
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Correspondence to Christina D. Buesching .

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  1. Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, Abingdon, Oxfordshire, UK

    Christina D. Buesching

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Newman, C., Buesching, C.D. (2019). Detecting the Smell of Disease and Injury: Scoping Evolutionary and Ecological Implications. In: Buesching, C. (eds) Chemical Signals in Vertebrates 14. Springer, Cham. https://doi.org/10.1007/978-3-030-17616-7_17

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