Abstract
The chemical environment, and the natural resources available in which our species has evolved has been crucial for the establishment of our medical practices. Here we present a brief review of the insights provided by chemical ecology to understand the evolution of medical practices since ancestral hominids to modern humans, as well as their implications for the search for new drugs of natural origin. Like for any other mammal, ecological and evolutionary processes have shaped how we relate to plant and animal chemicals, whether to avoid, transform and/or explore these compounds according to our needs. In addition, culture has played a key role in the way these chemicals are perceived by people and how they can be processed by different modes of use for ingestion, as well as providing cultural significance for their use (in medicine, for example) or their rejection altogether.
This is a preview of subscription content, access via your institution.
References
Aklillu E, Herrlin K, Gustafsson LL, Bertilsson L, Ingelman-Sundberg M (2002) Evidence for environmental influence on CYP2D6-catalysed debrisoquine hydroxylation as demonstrated by phenotyping and genotyping of Ethiopians living in Ethiopia or in Sweden. Pharmacogenetics 12:375–383
Albert RM, Bamford MK, Stanistreet IG et al (2018) River-fed wetland palaeovegetation and paleoecology at the HWK W site, Bed I, Olduvai Gorge. Rev Palaeobot Palynol 259:223–241
Albuquerque UP (2006) Re-examining hypotheses concerning the use and knowledge of medicinal plants: a study in the Caatinga vegetation of NE Brazil. J Ethnobiol Ethnomed 2:30
Albuquerque UP, Alves RRN (2016) Introduction to ethnobiology. Springer, New York
Albuquerque UP, Ferreira Júnior WS (2017) What do we study in evolutionary ethnobiology? Defining the theoretical basis for a research program. Evol Biol 44:206–215
Albuquerque UP, Andrade LH, Silva ACO (2005) Use of plant resource in a seasonal dry forest (Northeastern Brazil). Acta Bot Bras 19(1):27–38
Albuquerque UP, Ramos MA, Melo JG (2012) New strategies for drug discovery in tropical forests based on ethnobotanical and chemical ecological studies. J Ethnopharmacol 140(1):197–201
Albuquerque UP, Medeiros PM, Ferreira Júnior WS, Silva T, Silva R, Souza TG (2019) Social-ecological theory of maximization: basic concepts and two initial models. Biol Theory 14:73–85
Alencar NL, Araújo TAS, Amorim ELC, Albuquerque UP (2009) Can the apparency hypothesis explain the selection of medicinal plants in an area of Caatinga vegetation? Acta Bot Bras 23:910–911
Alencar NL, Araújo TAS, Amorim ELC, Albuquerque UP (2010) The inclusion and selection of medicinal plants in traditional pharmacopoeias—evidence in support of the diversification hypothesis. Econ Bot 1:68–79
Almeida CFCBR, Araújo EL, Silva TC, Amorim ELC, Maia MBDS, Albuquerque UP (2005) Life strategy and chemical composition as predictors of the selection of medicinal plants from the Caatinga (Northeast Brazil). J Arid Environ 62:127–142
Almeida CDFCBR, Cavalcanti De Amorim EL, Albuquerque UP (2011) Insights into the search for new drugs from traditional knowledge: an ethnobotanical and chemical-ecological perspective. Pharm Biol 49:864–873
Ankli A, Stich O, Heinrich M (1999) Yucatec Maya medicinal plants versus non medicinal plants: indige nous characterization and selection. Hum Ecol 27:557–580
Bartoshuk LM (2000) Comparing sensory experiences across individuals: recent psychophysical advances illuminate genetic variation in taste perception. Chem Senses 25:447–460
Bartoshuk LM, Duffy VB, Miller IJ (1995) PTC/PROP tasting: anatomy, psychophysics, and sex effects. Physiol Behav 56:1165–1171
Benz BF, Cevallos JE, Santana FM, Rosales JA, Graf SM (2000) Losing knowledge about plant use in the Sierra de Manatlán biosphere reserve, Mexico. Econ Bot 2:183–191
Billing J, Sherman PW (1998) Antimicrobial functions of spices: why some like it hot. Q Rev Biol 73:3–49
Brett JA, Heinrich M (1998) Culture, perception and the environment: the role of chemosensory perception. Angew Bot 72:67–69
Brito E, Gomes E, Falé PL, Borges C et al (2018) Bioactivities of decoctions from Plectranthus species related to their traditional use on the treatment of digestive problems and alcohol intoxication. J Ethnopharmacol 220:147–154
Bryant JP, Kuropat PJ, Cooper SM, Frisby K, Owen-Smith N (1989) Resource availability hypothesis of plant antiherbivore defence tested in a South African savanna ecosystem. Nature 340:227–229
Carrera-Bastos P, Fontes-Villalba M, O’Keefe JH et al (2011) The western diet and lifestyle and diseases of civilization. Res Rep Clin Cardiol 2:15–35
Carrión JS, Walker MJ (2018) Background to Neanderthal presence in Western Mediterranean Europe. Quat Sci Rev. https://doi.org/10.1016/j.quascirev.2018.10.011
Casagrande DG (2000) Human taste and cognition in Tzeltal Maya medicinal plant use. J Ecol Anthropol 4:57–69
Chacón-Fuentes M, Parra L, Lizama M, Seguel I, Úrzua A, Quiroz A (2017) Plant flavonoid content modified by domestication. Environ Entomol 2017:1–10. https://doi.org/10.1093/ee/nvx126
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899
Dobson CM (2004) Chemical space and biology. Nature 432:824–828
Drijfhout F (2017) Chemical ecology. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0003265.pub3
Endara MJ, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398
Esteban I, Albert RM, Eixea A, Zilhão J, Villaverde V (2017) Neanderthal use of plants and past vegetation reconstruction at the Middle Paleolithic site of Abrigo de la Quebrada (Chelva, Valencia, Spain). Archaeol Anthropol Sci 9:265–278
Fabrega H (1997) Evolution of sickness and healing. University of California Press, Berkeley
Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochemical interactions between plants and insects, vol 10. Springer, Boston, pp 1–40
Gaillard MDP, Glauser G, Robert CAM, Turlings TCJ (2018) Fine-tuning the ‘plant domestication-reduced defense’ hypothesis: specialist vs generalist herbivores. New Phytol 217:355–366
Gama ADS, Paula M, Silva RRV, Ferreira Junior WS, Medeiros PM (2018) Exotic species as models to understand biocultural adaptation: challenges to mainstream views of human–nature relations. PLoS One 134:e0196091
Geck MS, Cabras S, Casu L, Reyes GarcÃa AJ, Leonti M (2017) The taste of heat: how humoral qualities act as a cultural filter for chemosensory properties guiding herbal medicine. J Ethnopharmacol 198:499–515
Gopisankar MG (2017) CYP2D6 pharmacogenomics. Egypt J Med Hum Genet 18:309–313
Gottlieb OR, Borin MRMB, Brito NRS (2002) Integration of ethnobotany and phytochemistry: dream or reality? Phytochemistry 60:145–152
Hardy K (2018) Plant use in the lower and middle palaeolithic: food, medicine, and raw materials. Quat Sci Rev 191:393–405
Hardy K, Buckley S, Collins MJ, Estalrrich A, Brothwell D, Copeland L et al (2012) Neanderthal medics? Evidence for food, cooking, and medicinal plants entrapped in dental calculus. Naturwissenschaften 99:617–626
Hardy K, Buckley S, Huffman M (2016) Doctors, chefs or hominin animals? Non-edible plants and Neanderthals. Antiquity 90:1373–1379
Hardy K, Radini A, Buckley S, Blasco R, Copeland Les et al (2017) Diet and environment 1.2 million years ago revealed through analysis of dental calculus from Europe’s oldest hominin at Sima del Elefante, Spain. Sci Nat 104:1–5
Hardy BL, Moncel M, Despriée J, Courcimault G, Voinchet P (2018) Middle Pleistocene hominin behavior at the 700 ka Acheulean site of la Noira (France). Quatern Sci Rev 199:60–82
Hart BL, Hart LA (2018) How mammals stay healthy in nature: the evolution of behaviours to avoid parasites and pathogens. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2017.0205
Hart G, Gaoue OG, Torre L et al (2017) Availability, diversification and versatility explain human selection of introduced plants in Ecuadorian traditional medicine. PLoS One 12(9):e0184369
Hayes JE, Bartoshuk LM, Kidd JR, Duffy VB (2008) Supertasting and PROP bitterness depends on more than the TAS2R38 gene. Chem Senses 33:255–265
Heinrich M (1998) Indigenous concepts of medicinal plants in Oaxaca, Mexico: lowland Mixe plant classification based on organoleptic characteristics. J Appl Bot (Angewandte Botanik) 72:75–81
Hernandez-Cumplido J, Giusti MM, Zhou Y, Kyryczenko-Roth V, Chen YH, Rodriguez-Saona C (2018) Testing the ‘plant domestication-reduced defense’ hypothesis in blueberries: the role of herbivore identity. Arthropod Plant Interact 12:483–493
Huffman MA (2001) Self-medicative behavior in the African great apes: an evolutionary perspective. Bioscience 51(8):651–661
Hutson JM (2018) The faunal remains from Bundu Farm and Pniel 6: examining the problematic Middle Stone Age archaeological record within the southern African interior. Quat Int 466:178–193
Ingelman-Sundberg M (2001) Pharmacogenetics: an opportunity for a safer and more efficient pharmacotherapy. J Intern Med 250:186–200
Ingelman-Sundberg M (2005) Genetic polymorphisms of cytochrome P 450 2D6 (CYP2D6): clinical consequences, evolutionary aspects and functional diversity. Pharmacogenom J 5:6–13
Johns T (1990) The origins of human diet and medicine. The University of Arizona, Tucson, AZ
Johns T (1999) The chemical ecology of human ingestive behaviors. Ann Rev Anthropol 28:27–50
Ferreira Júnior WS, Albuquerque UP (2018) A theoretical review on the origin of medicinal practices in humans: echoes from evolution. Ethnobiol Conserv 7:1–7
Ferreira Júnior WS, Campos LZO, Pieroni A, Albuquerque UP (2015) Biological and cultural bases of the use of medicinal and food plants. In: Albuquerque UP, Medeiros PM, Casas A (eds) Evolutionary ethnobiology. Springer, New York, pp 175–184
Kim UK, Jorgenson E, Coon H, Leppert M, Risch N, Drayna D (2003) Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science 299:1221–1225
Koshimizu K, Ohigashi H, Huffman MA (1994) Use of Vernonia amygdalina by wild chimpanzee: possible roles of its bitter and related constituents. Physiol Behav 56:1209–1216
Lalueza-Fox C, Gigli E, de la Rasilla M, Fortea J, Rosas A (2009) Bitter taste perception in Neanderthals through the analysis of the TAS2R38 gene. Biol Lett 5:809–811
Leonti M (2012) The co-evolutionary perspective of the food-medicine continuum and wild gathered and cultivated vegetables. Genet Resour Crop Evol 59:1295–1302
Leonti M, Ramirez RF, Sticher O, Heinrich M (2003) Medicinal flora of the Popoluca, México: a botanico-systematical perspective. Econ Bot 57:218–230
Leonti M, Cabras S, Castellanos ME, Challenger A, Gertsch J, Casu L (2013) Bioprospecting: evolutionary implications from a post-olmec pharmacopeia and the relevance of widespread taxa. J Ethnopharmacol 147:92–107
Lüdecke T, Kullmer O, Wacker U, Sandrock O, Fiebig J, Schrenk F, Mulch A (2018) Dietary versatility of Early Pleistocene hominins. PNAS 115:13330–13335
McClenon J (1997) Shamanic healing, human evolution, and the origin of religion. J Sci Study Relig 36:345–354
McKey D, Cavagnaro TR, Cliff J, Gleadow R (2010) Chemical ecology in coupled human and natural systems: people, manioc, multitrophic interactions and global change. Chemoecology 20:109–133
Medeiros PM, Ladio AH, Albuquerque UP (2013) Patterns of medicinal plant use by inhabitants of Brazilian urban and rural areas: a macroscale investigation based on available literature. J Ethnopharmacol 150:729–746
Medeiros PM, Pinto BLC, Nascimento VT (2015) Can organoleptic properties explain the differential use of medicinal plants? Evidence from Northeastern Brazil. J Ethnopharmacol 159:43–48
Medeiros PM, Junior WSF, Ramos MA, Silva TC, Ladio AH, Albuquerque UP (2017) Why do people use exotic plants in their local medical systems? A systematic review based on Brazilian local communities. PLoS One. https://doi.org/10.1371/journal.pone.0185358
Mennella A, Pepino Y, Reed D (2005) Genetic and environmental determinants of bitter perception and sweet preferences. Pediatrics 115:216–222. https://doi.org/10.1542/peds.2004-1582
Mennella A, Spector A, Reed D, Coldwell SE (2013) The bad taste of medicines: overview of basic research on bitter taste. Clin Ther 35:1225–1246
Moerman DE, Pemberton RW, Kiefer D, Berlin B (1999) A comparative analysis of five medicinal floras. J Ethnobiol 19:49–67
Moreira X, Abdala-Roberts L, Gols R, Francisco M (2018) Plant domestication decreases both constitutive and induced chemical defences by direct selection against defensive traits. Sci Rep 8:12678
Morrogh-Bernard HC, Foitová I, Yeen Z et al (2017) Self-medication by orang-utans (Pongo pygmaeus) using bioactive properties of Dracaena cantleyi. Sci Rep 7:1–7
Nascimento VT, Vasconcelos MAS, Maciel MIS, Albuquerque UP (2012) Famine foods of Brazil’s seasonal dry forests: ethnobotanical and nutritional aspects. Econ Bot 66:22–34
Nebert DW (2008) Pharmacogenetics and pharmacogenomics. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0005558.pub2
Nebert DW, Dieter MZ (2000) The evolution of drug metabolism. Pharmacology 2000:124–135
O’Brien MJ, Laland KN (2012) Genes, culture, and agriculture: an example of human niche construction. Curr Anthropol 53(4):434–470
Paine OCC, Koppa A, Henry AG, Leichliter JN, Codron D et al (2018) Grass leaves as potential hominin dietary resources. J Hum Evol 117:44–52
Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, Werner J, Villanea FA, Mountain JL, Misra R, Carter NP, Lee C, Stone AC (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39:1256–1260
Pieroni A, Quave CL (2006) Functional foods or food medicines? On the consumption of wild plants among albanians and southern italians in Lucania. In: Pieroni A, Price LL (eds) Eating and healing. Haworth Press, New York, pp 101–129
Pieroni A, Nebel S, Quave C et al (2002) Ethnopharmacology of liakra: traditional weedy vegeta- bles of the Arbëreshë of the Vulture area in southern Italy. J Ethnopharmacol 81:165–185
Qin S, Shen L, Zhang A, Xie J, Shen W, Chen L, Tang J, Xiong Y, Yang L, Shi Y, Feng G, He L, Xing Q (2008) Systematic polymorphism analysis of the CYP2D6 gene in four different geographical Han populations in mainland China. Genomic 92:152–158
Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. In: Wallace JW, Mansell RL (eds) Biochemical interactions between plants and insects, vol 10. Springer, Boston, pp 168–213
Roach NT, Du A, Hatala KG, Ostrofsky KR et al (2018) Pleistocene animal communities of a 1.5 million-year-old lake margin grassland and their relationship to Homo erectus paleoecology. J Hum Evol 122:70–83
Rozin P, Gruss L, Berk G (1979) Reversal of innate aversions: attempts to induce a preference for chili peppers in rats. J Comp Physiol Psychol 93:1001–1014
Santoro FM, Nascimento ALB, Soldati GT, Ferreira Júnior WS, Albuquerque UP (2018) Evolutionary ethnobiology and cultural evolution: opportunities for research and dialog. J Ethnobiol Ethnomed 14:1. https://doi.org/10.1186/s13002-017-0199-y
Saslis-Lagoudakis CH, Savolainen V, Williamson EM, Forest F, Wagstaff SJ, Baral SR, Watson MF, Pendry CA, Hawkins JA (2012) Phylogenies reveal predictive power of traditional medicine in bioprospecting. PNAS 109:15835–15840
Shlichta JG, Cuny MAC, Hernandez-Cumplido J, Traine J, Benrey B (2018) Contrasting consequences of plant domestication for the chemical defenses of leaves and seeds in lima bean plants. Basic Appl Ecol 31:10–20
Silva TLL, Ferreira Júnior WS, Albuquerque UP (2020) Is there a biological basis in the selection of medicinal plants in the human species? an initial approach based on chemosensory perception of taste. Ethnobiol Conserv 9:3. https://doi.org/10.15451/ec2020-01-9.03-1-15
Singh M (2018) The cultural evolution of shamanism. Behav Brain Sci 6:1–83
Soranzo N, Bufe B, Sabeti PC, Wilson JF, Weale ME, Marguerie R, Meyerhof W, Goldstein DB (2005) Positive selection on a high-sensitivity allele of the human bitter-taste receptor TAS2R16. Curr Biol 15:1257–1265
Speed MP, Fenton A, Jones MG, Ruxton GD, Brockhurst MA (2015) Coevolution can explain defensive secondary metabolite diversity in plants. New Phytol 208:1251–1263
Stepp JR (2004) The role of weeds as sources of pharmaceuticals. J Ethnopharmacol 92:163–166
Stepp JR, Moerman DE (2001) The importance of weeds in ethnopharmacology. J Ethnopharmacol 75:19–23
Swati Sahoo BS (2019) Pharmacogenomic assessment of herbal drugs in affective disorders. Biomed Pharmacother 109:1148–1162
Teh LK, Bertilsson L (2012) Pharmacogenomics of CYP2D6: molecular genetics, interethnic differences and clinical importance. Drug Metab Pharmacokinet 27:55–67
Toneu IT, Jordan FM, Hawkins JA (2018) Comparative phylogenetic methods and the cultural evolution of medicinal plant use. Nat Plants. https://doi.org/10.1038/s41477-018-0226-6
Valussi M (2011) Functional foods with digestion-enhancing properties. Int J Food Sci Nutr 63:82–89
Voeks RA (1996) Tropical forest healers and habitat preference. Econ Bot 50:381–400
Voeks RA (2004) Disturbance pharmacopeias: medicine and myth from the humid tropics. Ann Assoc Am Geogr 94:868–888
Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4:e72
Wadley L (2015) Those marvellous millennia: the Middle Stone Age of southern Africa. Azania Archaeol Res Africa 50:155–226
Weckerle CS, Cabras S, Castellanos ME, Leonti M (2011) Quantitative methods in ethnobotany and ethnopharmacology: considering the overall flora-hypothesis testing for over- and underused plant families with the Bayesian approach. J Ethnopharmacol 137:837–847
Weyrich LS, Duchene S, Soubrier J et al (2017) Cooper Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus. Nature 544:357–361
Wink M (2008) Evolution of secondary plant metabolism. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0001922.pub2
Wu Y, Guo T, Mu Q, Wang J, Li X, Wu Y, Tian B, Wang ML, Bai G, Perumal R, Trick HN, Bean SR, Dweikat IM, Tuinstra MR, Morris G, Tesso TT, Yu J, Li X (2019) Allelochemicals targeted to balance competing selections in African agroecosystems. Nat Plants 5:1229–1236
Acknowledgements
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de NÃvel Superior—Brasil (CAPES)—Finance Code 001. Contribution of the INCT Ethnobiology, Bioprospecting and Nature Conservation, certified by CNPq, with financial support from FACEPE (Foundation for Support to Science and Technology of the State of Pernambuco—Grant number: APQ-0562-2.01/17). ISF thanks to CAPES/FACEPE (PNPD program) for providing a post-doctoral scholarship (Grant numbers: APQ-0700-2.05/16 and BCT-0259.22-05/17). Thanks to CNPq for the productivity grant awarded to UPA, and to the post-doctoral fellowship (151518/2018-1) granted to ALBN. To the reviewers who improved our paper with their comments.
Author information
Authors and Affiliations
Contributions
UPA and WSFJ: conceptualized the study, contributed to writing, and edited the final draft of the manuscript. ISF, LSX, PHG, ALBN, TCS, and RHS: contributed to writing and edited the final draft of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no conflict of interest.
Additional information
Handling Editor: Marko Rohlfs.
Rights and permissions
About this article
Cite this article
Albuquerque, U.P., do Nascimento, A.L.B., Silva Chaves, L. et al. The chemical ecology approach to modern and early human use of medicinal plants. Chemoecology 30, 89–102 (2020). https://doi.org/10.1007/s00049-020-00302-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-020-00302-8