Are vipers prototypic fear-evoking snakes? A cross-cultural comparison of Somalis and Czechs
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
37928591
PubMed Central
PMC10620321
DOI
10.3389/fpsyg.2023.1233667
Knihovny.cz E-zdroje
- Klíčová slova
- cross-cultural comparison, evolutionary psychology, fear, ophidiophobia, specific phobias,
- Publikační typ
- časopisecké články MeSH
Snakes are known as highly fear-evoking animals, eliciting preferential attention and fast detection in humans. We examined the human fear response to snakes in the context of both current and evolutionary experiences, conducting our research in the cradle of humankind, the Horn of Africa. This region is characterized by the frequent occurrence of various snake species, including deadly venomous viperids (adders) and elapids (cobras and mambas). We conducted experiments in Somaliland and compared the results with data from Czech respondents to address the still unresolved questions: To which extent is human fear of snakes affected by evolutionary or current experience and local culture? Can people of both nationalities recognize venomous snakes as a category, or are they only afraid of certain species that are most dangerous in a given area? Are respondents of both nationalities equally afraid of deadly snakes from both families (Viperidae, Elapidae)? We employed a well-established picture-sorting approach, consisting of 48 snake species belonging to four distinct groups. Our results revealed significant agreement among Somali as well as Czech respondents. We found a highly significant effect of the stimulus on perceived fear in both populations. Vipers appeared to be the most salient stimuli in both populations, as they occupied the highest positions according to the reported level of subjectively perceived fear. The position of vipers strongly contrasts with the fear ranking of deadly venomous elapids, which were in lower positions. Fear scores of vipers were significantly higher in both populations, and their best predictor was the body width of the snake. The evolutionary, cultural, and cognitive aspects of this phenomenon are discussed.
Department of Biology Faculty of Education Amoud University Borama Somalia
Department of Zoology Faculty of Science Charles University Prague Czechia
Zobrazit více v PubMed
Abbate E., Albianelli A., Azzaroli A., Benvenutih M., Tesfamariam B., Bruni P., et al. . (1998). A one-million-year-old Homo cranium from the Danakil (Afar) depression of Eritrea. Nature 393, 458–460. doi: 10.1038/30954, PMID: PubMed DOI
Aga A. M., Hurisa B., Niwayesillassie B., Kebede G., Kerga S., Kebede A., et al. . (2014). Epidemiological survey of Snake bite in Ethiopia. Epidemiology 4, 1–5.
Ainsworth S., Petras D., Engmark M., Sussmuth R. D., Whiteley G., Albulescu L. O., et al. . (2018). The medical threat of mamba envenoming in sub-Saharan Africa revealed by genus-wide analysis of venom composition, toxicity and antivenomics profiling of available antivenoms. J. Proteome 172, 173–189. doi: 10.1016/j.jprot.2017.08.016, PMID: PubMed DOI
Akani G. C., Ebere N., Franco D., Eniang E. A., Petrozzi F., Politano E., et al. . (2013). Correlation between annual activity patterns of venomous snakes and rural people in the Niger Delta, southern Nigeria. J. Venom Anim. Toxins 19, 2–8. doi: 10.1186/1678-9199-19-2, PMID: PubMed DOI PMC
Almécija S., Hammond A. S., Thompson N. E., Pugh K. D., Moya-Sola S., Alba D. M. (2021). Fossil apes and human evolution. Science 372:eabb4363. doi: 10.1126/science.abb4363 PubMed DOI
Almeida I., Soares S. C., Castelo-Branco M. (2015). The distinct role of the amygdala, superior colliculus and Pulvinar in processing of central and peripheral snakes. Plos One 10:e0129949. doi: 10.1371/journal.pone.0129949 PubMed DOI PMC
Alves R. R. N., Silva V. N., Trovao D., Oliveira J. V., Mourao J. S., Dias T. L. P., et al. . (2014). Students' attitudes toward and knowledge about snakes in the semiarid region of northeastern Brazil. J. Ethnobiol. Ethnomed. 10, 1–8. doi: 10.1186/1746-4269-10-30 PubMed DOI PMC
Alves R. R. N., Vieira K. S., Santana G. G., Vieira W. L. S., Almeida W. O., Souto W. M. S., et al. . (2012). A review on human attitudes towards reptiles in Brazil. Environ. Monit. Assess. 184, 6877–6901. doi: 10.1007/s10661-011-2465-0, PMID: PubMed DOI
Amaral D. G. (2002). The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety. Biol. Psychiatry 51, 11–17. doi: 10.1016/S0306-4522(02)01001-1, PMID: PubMed DOI
Amaral D. G. (2003). The amygdala, social behavior, and danger detection. Ann. N. Y. Acad. Sci. 1000, 337–347. doi: 10.1196/annals.1280.015 PubMed DOI
Andrews P. (2020). Last common ancestor of apes and humans: morphology and environment. Folia Primatol. 91, 122–148. doi: 10.1159/000501557 PubMed DOI
Asadi A., Montgelard C., Nazarizadeh M., Moghaddasi A., Fatemizadeh F., Simonov E., et al. . (2019). Evolutionary history and postglacial colonization of an Asian pit viper (Gloydius halys caucasicus) into Transcaucasia revealed by phylogenetic and phylogeographic analyses. Sci. Rep. 9:1224. doi: 10.1038/s41598-018-37558-8 PubMed DOI PMC
Asfaw B., Gilbert W. H., Beyene Y., Hart W. K., Renne P. R., WoldeGabriel G., et al. . (2002). Remains of Homo erectus from bouri, middle awash, Ethiopia. Nature 416, 317–320. doi: 10.1038/416317a PubMed DOI
Ballouard J. M., Provost G., Barré D., Bonnet X. (2012). Influence of a field trip on the attitude of schoolchildren toward unpopular organisms: an experience with snakes. J. Herpetol. 46, 423–428. doi: 10.1670/11-118 DOI
Bar M., Neta M. (2006). Humans prefer curved visual objects. Psychol. Sci. 17, 645–648. doi: 10.1111/j.1467-9280.2006.01759 PubMed DOI
Barlow A., Wuster W., Kelly C. M. R., Branch W. R., Phelps T., Tolley K. A. (2019). Ancient habitat shifts and organismal diversification are decoupled in the African viper genus Bitis (Serpentes: Viperidae). J. Biogeogr. 46, 1234–1248. doi: 10.1111/jbi.13578 DOI
Begun D. R., Nargolwalla M. C., Kordos L. (2012). European Miocene hominids and the origin of the African ape and human clade. Evol. Anthropol. 21, 10–23. doi: 10.1002/evan.20329 PubMed DOI
Beligiannis N., Hermus M., Gootjes L., Van Strien J. W. (2022). Both low and high spatial frequencies drive the early posterior negativity in response to snake stimuli. Neuropsychologia 177:108403. doi: 10.1016/j.neuropsychologia.2022.108403 PubMed DOI
Bergström A., Stringer C., Hajdinjak M., Scerri E. M. L., Skoglund P. (2021). Origins of modern human ancestry. Nature 590, 229–237. doi: 10.1038/s41586-021-03244-5 PubMed DOI
Bertels J., Bayard C., Floccia C., Destrebecqz A. (2018). Rapid detection of snakes modulates spatial orienting in infancy. Int. J. Behav. Dev. 42, 381–387. doi: 10.1177/0165025417693955 DOI
Bertels J., Bourguignon M., De Heering A., Chetail F., De Tiège X., Cleeremans A., et al. . (2020). Snakes elicit specific neural responses in the human infant brain. Sci. Rep. 10:7443. doi: 10.1038/s41598-020-63619-y PubMed DOI PMC
Bertels J., De Heering A., Bourguignon M., Cleeremans A., Destrebecqz A. (2023). What determines the neural response to snakes in the infant brain? A systematic comparison of color and grayscale stimuli. Front. Psychol. 14:1027872. doi: 10.3389/fpsyg.2023.1027872, PMID: PubMed DOI PMC
Blumstein D. T. (2006). The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112, 209–217. doi: 10.1111/j.1439-0310.2006.01209.x DOI
Brosch T., Pourtois G., Sander D. (2010). The perception and categorisation of emotional stimuli: a review. Cogn. Emot. 24, 377–400. doi: 10.1080/02699930902975754 DOI
Chippaux J. P. (2011). Estimate of the burden of snakebites in sub-Saharan Africa: a meta-analytic approach. Toxicon 57, 586–599. doi: 10.1016/j.toxicon.2010.12.022 PubMed DOI
Clark J. D., Deheinzelin J., Schick K. D., Hart W. K., White T. D., Woldegabriel G., et al. . (1994). African Homo erectus: old radiometric ages and young oldowan assemblages in the middle Awash Valley, Ethiopia. Science 264, 1907–1910. doi: 10.1126/science.8009220 PubMed DOI
Coelho C. M., Purkis H. (2009). The origins of specific phobias: influential theories and current perspectives. Rev. Gen. Psychol. 13, 335–348. doi: 10.1037/a00177 DOI
Coelho C. M., Suttiwan P., Faiz A., Ferreira-Santos F., Zsido A. N. (2019). Are humans prepared to detect, fear, and avoid snakes? The mismatch between laboratory and ecological evidence. Front. Psychol. 10:2094. doi: 10.3389/fpsyg.2019.02094 PubMed DOI PMC
Conroy G. C., Weber G. W., Seidler H., Recheis W., Zur Nedden D., Mariam J. H. (2000). Endocranial capacity of the Bodo cranium determined from three-dimensional computed tomography. Am. J. Phys. Anthropol. 113, 111–118. doi: 10.1002/1096-8644(200009)113:1<111::AID-AJPA10>3.0.CO;2-X PubMed DOI
Coss R. G. (1968). The ethological command in art. Leonardo 1, 273–287. doi: 10.2307/1571871 DOI
Coss R. G. (1991). Context and animal behavior III: the relationship between early development and evolutionary persistence of ground squirrel antisnake behavior. Ecol. Psychol. 3, 277–315. doi: 10.1207/s15326969eco0304_1 DOI
Coss R. G. (1993). Evolutionary persistence of ground squirrel Antisnake behavior: reflections on Burton's commentary. Ecol. Psychol. 5, 171–194. doi: 10.1207/s15326969eco0502_4 DOI
Coss R. G. (1999). “Effects of relaxed natural selection on the evolution of behaviour” in Geographic variation in behavior: Perspectives on evolutionary mechanisms. eds. Foster S. A., Endler J. A. (New York: Oxford University Press; ), 180–208.
Coss R. G. (2003). “The role of evolved perceptual biases in art and design” in Evolutionary aesthetics. eds. Voland E., Grammer K. (Heidelberg: Springer-Verlag; )
Coss R. G., Cavanaugh C., Brennan W. (2019). Development of snake-directed antipredator behavior by wild-faced capuchin monkeys: III. The signaling properties of alarm-call tonality. Am. J. Primatol. 81:e22950. doi: 10.1002/ajp.22950 PubMed DOI
Coss R. G., Charles E. P. (2021). The saliency of snake scales and leopard rosettes to infants: its relevance to graphical patterns portrayed in prehistoric art. Front. Psychol. 12:763436. doi: 10.3389/fpsyg.2021.763436 PubMed DOI PMC
Coss R. G., McCowan B., Ramakrishnan U. (2007). Threat-related acoustical differences in alarm calls by wild bonnet macaques (Macaca radiata) elicited by python and leopard models. Ethology 113, 352–367. doi: 10.1111/j.1439-0310.2007.01336.x DOI
Crockford C., Wittig R. M., Mundry R., Zuberbühler K. (2012). Wild chimpanzees inform ignorant group members of danger. Curr. Biol. 22, 142–146. doi: 10.1016/j.cub.2011.11.053, PMID: PubMed DOI
Cui S. P., Luo X., Chen D. Q., Sun J. Z., Chu H. J., Li C. W., et al. . (2016). The adder (Vipera berus) in southern Altay Mountains: population characteristics, distribution, morphology and phylogenetic position. Peerj 4:e2342. doi: 10.7717/peerj.2342, PMID: PubMed DOI PMC
Dimberg U., Thunberg M. (1998). Rapid facial reactions to emotional facial expressions. Scand. J. Psychol. 39, 39–45. doi: 10.1111/1467-9450.00054 PubMed DOI
Dinh H. T., Nishimaru H., Le Q. V., Matsumoto J., Setogawa T., Maior R. S., et al. . (2021). Preferential neuronal responses to snakes in the monkey medial prefrontal cortex support an evolutionary origin for Ophidiophobia. Front. Behav. Neurosci. 15:653250. doi: 10.3389/fnbeh.2021.653250, PMID: PubMed DOI PMC
Ditmars R. L. (1931). Snakes of the world. New York: Macmillan.
Dobson J. S. (2022). Evolution and diversification of the Anguimorphan lizard venom system. Herston: University of Queensland, p. 242.
Durvasula A., Sankararaman S. (2020). Recovering signals of ghost archaic introgression in African populations. Scie. Adv. 6:eaax5097. doi: 10.1126/sciadv.aax5097 PubMed DOI PMC
Effting M., Salemink E., Verschuere B., Beckers T. (2016). Implicit and explicit measures of spider fear and avoidance behavior: examination of the moderating role of working memory capacity. J. Behav. Ther. Exp. Psy. 50, 269–276. doi: 10.1016/j.jbtep.2015.10.003 PubMed DOI
Fekadu T. (2016). Envenoming snakebites in Eritrea: a preliminary study. J. Eritrean Stud. 7, 127–147.
Fry B. G., Casewell N. R., Wuster W., Vidal N., Young B., Jackson T. N. W. (2012). The structural and functional diversification of the Toxicofera reptile venom system. Toxicon 60, 434–448. doi: 10.1016/j.toxicon.2012.02.013, PMID: PubMed DOI
Fry B. G., Wroe S., Teeuwisse W., van Osch M. J. P., Moreno K., Ingle J., et al. . (2009). A central role for venom in predation by Varanus komodoensis (komodo dragon) and the extinct giant Varanus (Megalania) priscus. Proc. Natl. Acad. Sci. U. S. A. 106, 8969–8974. doi: 10.1073/pnas.0810883106, PMID: PubMed DOI PMC
Frynta D., Lišková S., Bultmann S., Burda H. (2010). Being attractive brings advantages: the case of parrot species in captivity. Plos One 5:e12568. doi: 10.1371/journal.pone.0012568 PubMed DOI PMC
Frynta D., Marešová J., Řeháková-Petrů M., Šklíba J., Šumbera R., Krása A. (2011). Cross-cultural agreement in perception of animal beauty: Boid snakes viewed by people from five continents. Hum. Ecol. 39, 829–834. doi: 10.1007/s10745-011-9447-2 DOI
Frynta D., Šimková O., Lišková S., Landová E. (2013). Mammalian collection on Noah's ark: the effects of beauty brain body size. Plos One 8:e63110. doi: 10.1371/journal.pone.0063110 PubMed DOI PMC
Fuss J., Spassov N., Begun D. R., Böhme M. (2017). Potential hominin affinities of Graecopithecus from the late Miocene of Europe. Plos One 12:e0177127. doi: 10.1371/journal.pone.0177127, PMID: PubMed DOI PMC
Gallotti R., Mussi M. (2017). Two Acheuleans, two humankinds: from 1.5 to 0.85 ma at Melka Kunture (upper awash, Ethiopian highlands). J. Anthropol. Sci. 95, 137–181. doi: 10.4436/jass.95001 PubMed DOI
Gamer M., Lemon J., Fellows I., Singh P. (2020). Various coefficients of interrater reliability and agreement. Package ‘irr’.
Gamer M., Lemon J., Singh P. (2012). Irr: Various coefficients of interrater reliability and agreement. R package.
Gibbons A. (2017). Oldest members of our species discovered in Morocco. Science 356, 993–994. doi: 10.1126/science.356.6342.993 PubMed DOI
Grassini S., Railo H., Valli K., Revonsuo A., Koivisto M. (2019). Visual features and perceptual context modulate attention towards evolutionarily relevant threatening stimuli: electrophysiological evidence. Emotion 19, 348–364. doi: 10.1037/emo0000434 PubMed DOI
Groucutt H. S., Petraglia M. D., Bailey G., Scerri E. M. L., Parton A., Clark-Balzan L., et al. . (2015). Rethinking the dispersal of Homo sapiens out of Africa. Evol. Anthropol. 24, 149–164. doi: 10.1002/evan.21455, PMID: PubMed DOI PMC
Haak W., Lazaridis I., Patterson N., Rohland N., Mallick S., Llamas B., et al. . (2015). Massive migration from the steppe was a source for indo-European languages in Europe. Nature 522, 207–211. doi: 10.1038/nature14317 PubMed DOI PMC
Habib A. G., Kuznik A., Hamza M., Abdullahi M. I., Chedi B. A., Chippaux J. P., et al. . (2015). Snakebite is under appreciated: appraisal of burden from West Africa. Plos Neglect. Trop. D. 9:e0004088. doi: 10.1371/journal.pntd.0004088 PubMed DOI PMC
Halilu S., Iliyasu G., Hamza M., Chippaux J. P., Kuznik A., Habib A. G. (2019). Snakebite burden in sub-Saharan Africa: estimates from 41 countries. Toxicon 159, 1–4. doi: 10.1016/j.toxicon.2018.12.002 PubMed DOI
Harnad S. (2017). “To cognize is to categorize: cognition is categorization” in Handbook of categorization in cognitive science. eds. Cohen H., Lefebvre C. (Amsterdam: Elsevier; ), 21–54.
Hayakawa S., Kawai N., Masataka N. (2011). The influence of color on snake detection in visual search in human children. Sci. Rep. 1, 1–4. doi: 10.1038/srep00080 PubMed DOI PMC
He H. S., Kubo K., Kawai N. (2014). Spiders do not evoke greater early posterior negativity in the event-related potential as snakes. Neuroreport 25, 1049–1053. doi: 10.1097/wnr.0000000000000227 PubMed DOI
Headland T. N., Greene H. W. (2011). Hunter-gatherers and other primates as prey, predators, and competitors of snakes. Proc. Natl. Acad. Sci. U. S. A. 108, E1470–E1474. doi: 10.1073/pnas.1115116108, PMID: PubMed DOI PMC
Hernández Tienda C., Beltrán Francés V., Majolo B., Romero T., Illa Maulany R., Oka Ngakan P., et al. . (2021). Reaction to snakes in wild moor macaques (Macaca maura). Int. J. Primatol. 42, 528–532. doi: 10.1007/s10764-021-00230-6 PubMed DOI PMC
Hublin J. J., Ben-Ncer A., Bailey S. E., Freidline S. E., Neubauer S., Skinner M. M., et al. . (2017). New fossils from Jebel Irhoud, Morocco and the pan-African origin of Homo sapiens. Nature 546, 289–292. doi: 10.1038/nature22336 PubMed DOI
Hyde J., Ryan K. M., Waters A. M. (2019). Psychophysiological markers of fear and anxiety. Curr. Psych. Rep. 21, 1–10. doi: 10.1007/s11920-019-1036-x PubMed DOI
Isbell L. A. (2006). Snakes as agents of evolutionary change in primate brains. J. Hum. Evol. 51, 1–35. doi: 10.1016/j.jhevol.2005.12.012, PMID: PubMed DOI
Isbell L. A. (2009). The fruit, the tree, and the serpent: Why we see so well. Cambridge: Harvard University Press.
Isbell L. A., Etting S. F. (2017). Scales drive detection, attention, and memory of snakes in wild vervet monkeys (Chlorocebus pygerythrus). Primates 58, 121–129. doi: 10.1007/s10329-016-0562-y PubMed DOI
Ivanov M., Čerňanský A. (2017). Vipera berus (Linnaeus, 1758) remains from the late Pleistocene of Slovakia. Amphibia-Reptilia 38, 133–144. doi: 10.1163/15685381-00003095 DOI
Janovcová M., Rádlová S., Polák J., Sedláčková K., Peléšková S., Žampachová B., et al. . (2019). Human attitude toward reptiles: a relationship between fear, disgust, and aesthetic preferences. Animals 9:238. doi: 10.3390/ani9050238 PubMed DOI PMC
Kawai N. (2019). “The underlying neuronal circuits of fear learning and the Snake detection theory (SDT)” in The fear of snakes: Evolutionary and psychobiological perspectives on our innate fear. ed. Kawai N. (Singapore: Springer; )
Kawai N., He H. S. (2016). Breaking Snake camouflage: humans detect snakes more accurately than other animals under less discernible visual conditions. Plos One 11:e0164342. doi: 10.1371/journal.pone.0164342, PMID: PubMed DOI PMC
Kawai N., Qiu H. C. (2020). Humans detect snakes more accurately and quickly than other animals under natural visual scenes: a flicker paradigm study. Cogn. Emot. 34, 614–620. doi: 10.1080/02699931.2019.1657799, PMID: PubMed DOI
Kelly C. M. R., Barker N. P., Villet M. H., Broadley D. G. (2009). Phylogeny, biogeography and classification of the snake superfamily Elapoidea: a rapid radiation in the late Eocene. Cladistics 25, 38–63. doi: 10.1111/j.1096-0031.2008.00237.x, PMID: PubMed DOI
Kirscher U., El Atfy H., Gärtner A., Dallanave E., Munz P., Niedźwiedzki G., et al. . (2021). Age constraints for the Trachilos footprints from Crete. Sci. Rep. 11:19427. doi: 10.1038/s41598-021-98618-0, PMID: PubMed DOI PMC
Landová E., Bakhshaliyeva N., Janovcová M., Peléšková S., Suleymanova M., Polák J., et al. . (2018a). Association between fear and beauty evaluation of snakes: cross-cultural findings. Front. Psychol. 9:333. doi: 10.3389/fpsyg.2018.00333 PubMed DOI PMC
Landová E., Janovcová M., Štolhoferová I., Rádlová S., Frýdlová P., Sedláčková K., et al. . (2021). Specificity of spiders among fear- and disgust-eliciting arthropods: spiders are special, but phobics not so much. Plos One 16:e0257726. doi: 10.1371/journal.pone.0257726 PubMed DOI PMC
Landová E., Marešová J., Šimková O., Cikánová V., Frynta D. (2012). Human responses to live snakes and their photographs: evaluation of beauty and fear of the king snakes. J. Environ. Psychol. 32, 69–77. doi: 10.1016/j.jenvp.2011.10.005 DOI
Landová E., Musilová V., Polák J., Sedláčková K., Frynta D. (2016). Antipredatory reaction of the leopard gecko Eublepharis macularius to snake predators. Curr. Zool. 62, 439–450. doi: 10.1093/cz/zow050 PubMed DOI PMC
Landová E., Peléšková S., Sedláčková K., Janovcová M., Polák J., Rádlová S., et al. . (2020). Venomous snakes elicit stronger fear than nonvenomous ones: psychophysiological response to snake images. Plos One 15:e0236999. doi: 10.1371/journal.pone.0236999 PubMed DOI PMC
Landová E., Polákova P., Rádlová S., Janovcová M., Bobek M., Frynta D. (2018b). Beauty ranking of mammalian species kept in the Prague zoo: does beauty of animals increase the respondents' willingness to protect them? Sci. Nat. 105, 1–14. doi: 10.1007/s00114-018-1596-3 PubMed DOI
Landová E., Rádlová S., Pidnebesna A., Tomeček D., Janovcová M., Peléšková Š., et al. . (2023). Toward a reliable detection of arachnophobia: subjective, behavioral, and neurophysiological measures of fear response. Front. Psych. 14:1196785. doi: 10.3389/fpsyt.2023.1196785 PubMed DOI PMC
Langergraber K. E., Prüfer K., Rowney C., Boesch C., Crockford C., Fawcett K., et al. . (2012). Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc. Natl. Acad. Sci. U.S.A. 109, 15716–15721. doi: 10.1073/pnas.1211740109, PMID: PubMed DOI PMC
Langeslag S. J. E., van Strien J. W. (2018). Early visual processing of snakes and angry faces: an ERP study. Brain Res. 1678, 297–303. doi: 10.1016/j.brainres.2017.10.031 PubMed DOI
Lanza B. (1990). Amphibians and reptiles of the Somali Democratic Republic: check list and biogeography. Biogeographia – J. Integr. Biogeogr 14, 407–465.
Lazaridis I., Nadel D., Rollefson G., Merrett D. C., Rohland N., Mallick S., et al. . (2016). Genomic insights into the origin of farming in the ancient near east. Nature 536, 419–424. doi: 10.1038/nature19310, PMID: PubMed DOI PMC
Lazaridis I., Patterson N., Mittnik A., Renaud G., Mallick S., Kirsanow K., et al. . (2014). Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413. doi: 10.1038/nature13673 PubMed DOI PMC
LeDoux J. E. (2000). Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155–184. doi: 10.1146/annurev.neuro.23.1.155 PubMed DOI
LeDoux J. E. (2012). Evolution of human emotion: a view through fear. Prog. Brain Res. 195:431442. doi: 10.1016/B978-0-444-53860-4.00021-0 PubMed DOI PMC
Lišková S., Frynta D. (2013). What determines bird beauty in human eyes? Anthrozoös 26, 27–41. doi: 10.2752/175303713x13534238631399 DOI
Lišková S., Landová E., Frynta D. (2015). Human preferences for colorful birds: vivid colors or pattern? Evol. Psychol. 13, 339–359. doi: 10.1177/14747049150130020 PubMed DOI
LoBue V. (2014). Deconstructing the snake: the relative roles of perception, cognition, and emotion on threat detection. Emotion 14, 701–711. doi: 10.1037/a0035898 PubMed DOI
LoBue V., DeLoache J. S. (2008). Detecting the snake in the grass: attention to fear-relevant stimuli by adults and young children. Psychol. Sci. 19, 284–289. doi: 10.1111/j.1467-9280.2008.02081.x PubMed DOI
LoBue V., DeLoache J. S. (2010). Superior detection of threat relevant stimuli in infancy. Develop. Sci. 13, 221–228. doi: 10.1111/j.1467-7687.2009.00872.x PubMed DOI
LoBue V., DeLoache J. S. (2011). What's so special about slithering serpents? Children and adults rapidly detect snakes based on their simple features. Vis. Cogn. 19, 129–143. doi: 10.1080/13506285.2010.522216 DOI
LoBue V., Rakison D. H. (2013). What we fear most: a developmental advantage for threat-relevant stimuli. Develop. Rev. 33, 285–303. doi: 10.1016/j.dr.2013.07.005 DOI
Marešová J., Krása A., Frynta D. (2009a). We all appreciate the same animals: cross-cultural comparison of human aesthetic preferences for Snake species in Papua New Guinea and Europe. Ethology 115, 297–300. doi: 10.1111/j.1439-0310.2009.01620.x DOI
Marešová J., Landová E., Frynta D. (2009b). What makes some species of milk snakes more attractive to humans than others? Theory Biosci. 128, 227–235. doi: 10.1007/s12064-009-0075-y PubMed DOI
McDougall I., Brown F. H., Fleagle J. G. (2005). Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433, 733–736. doi: 10.1038/nature03258 PubMed DOI
Meno W., Coss R. G., Perry S. (2013a). Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: I Snake-species discrimination. Am. J. Primatol. 75, 281–291. doi: 10.1002/ajp.22106 PubMed DOI
Meno W., Coss R. G., Perry S. (2013b). Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: II. Influence of the social environment. Am. J. Primatol. 75, 292–300. doi: 10.1002/ajp.22109 PubMed DOI
Meriau K., Wartenburger I., Kazzer P., Prehn K., Lammers C. H., van der Meer E., et al. . (2006). A neural network reflecting individual differences in cognitive processing of emotions during perceptual decision making. NeuroImage 33, 1016–1027. doi: 10.1016/j.neuroimage.2006.07.031, PMID: PubMed DOI
Mizsei E., Jablonski D., Roussos S. A., Dimaki M., Ioannidis Y., Nilson G., et al. . (2017). Nuclear markers support the mitochondrial phylogeny of Vipera ursinii-renardi complex (Squamata: Viperidae) and species status for the Greek meadow viper. Zootaxa 4227, 75–88. doi: 10.11646/zootaxa.4227.1.4 PubMed DOI
Moorjani P., Amorim C. E. G., Arndt P. F., Przeworski M. (2016). Variation in the molecular clock of primates. Proc. Natl. Acad. Sci. U.S.A. 113, 10607–10612. doi: 10.1073/pnas.1600374113, PMID: PubMed DOI PMC
Morris R., Morris D. (1965). Men and snakes. London: Hutchison.
Nhachi C. F., Kasilo O. M. (1994). Snake poisoning in rural Zimbabwe–a prospective study. J. Appl. Toxicol. 14, 191–193. doi: 10.1002/jat.2550140308 PubMed DOI
Nicula B. I. (2020). Cracking the Snake detection theory: the subcortical visual pathway as a major player in cultural transformations. World J. Neurosci. 10, 166–190.
Nilson G., Andrén C. (2001). The meadow and steppe vipers of Europe and Asia the Vipera (Acridophaga) ursinii complex. Acta Zool. Acad. Sci. Hungaricae 47, 87–267.
Öhman A., Flykt A., Esteves F. (2001). Emotion drives attention: detecting the snake in the grass. J. Exp. Psychol. 130, 466–478. doi: 10.1037/0096-3445.130.3.466, PMID: PubMed DOI
Öhman A., Mineka S. (2001). Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 108, 483–522. doi: 10.1037//0033-295x.108.3.483 PubMed DOI
Öhman A., Mineka S. (2003). The malicious serpent: snakes as a prototypical stimulus for an evolved module of fear. Curr. Dir. Psychol. Sci. 12, 5–9. doi: 10.1111/1467-8721.01211 DOI
Okon-Singer H., Alyagon U., Kofman O., Tzelgov J., Henik A. (2011). Fear-related pictures deteriorate the performance of university students with high fear of snakes or spiders. Stress 14, 185–193. doi: 10.3109/10253890.2010.527401 PubMed DOI
Oksanen J., Blanchet F. G., Friendly M., Kindt R., Legendre P., McGlinn D., et al. . (2020). Vegan: Community ecology package. R package.
Olalde I., Brace S., Allentoft M. E., Armit I., Kristiansen K., Booth T., et al. . (2018). The beaker phenomenon and the genomic transformation of Northwest Europe. Nature 555, 190–196. doi: 10.1038/nature25738 PubMed DOI PMC
Onyishi I. E., Nwonyi S. K., Pazda A., Prokop P. (2021). Attitudes and behaviour toward snakes on the part of Igbo people in southeastern Nigeria. Sci. Total Environ. 763:143045. doi: 10.1016/j.scitotenv.2020.143045 PubMed DOI
Owings D. H., Coss R. G., McKernon D., Rowe M. P., Arrowood P. C. (2001). Snake-directed antipredator behavior of rock squirrels (Spermophilus variegatus): population difference and snake-species discrimination. Behaviour 138, 575–595. doi: 10.1163/156853901316924485 DOI
Pandey D. P., Pandey G. S., Devkota K., Goode M. (2016). Public perceptions of snakes and snakebite management: implications for conservation and human health in southern Nepal. J. Ethnobiol. Ethnomed. 12, 22–25. doi: 10.1186/s13002-016-0092-0, PMID: PubMed DOI PMC
Papac L., Ernee M., Dobes M., Langova M., Rohrlach A. B., Aron F., et al. . (2021). Dynamic changes in genomic and social structures in third millennium BCE Central Europe. Sci. Adv. 7:eabi6941. doi: 10.1126/sciadv.abi6941, PMID: PubMed DOI PMC
Penkunas M. J., Coss R. G. (2013a). Rapid detection of visually provocative animals by preschool children and adults. J. Exp. Child Psychol. 114, 522–536. doi: 10.1016/j.jecp.2012.10.001 PubMed DOI
Penkunas M. J., Coss R. G. (2013b). A comparison of rural and urban Indian children's visual detection of threatening and nonthreatening animals. Develop. Sci. 16, 463–475. doi: 10.1111/desc.12043, PMID: PubMed DOI
Pessoa L., Adolphs R. (2010). Emotion processing and the amygdala: from a'low road'to'many roads' of evaluating biological significance. Nat. Rev. Neurosci. 11, 773–782. doi: 10.1038/nrn2920 PubMed DOI PMC
Pohlert T. (2014). The pairwise multiple comparison of mean ranks package (PMCMR). R Package
Pook C. E., Joger U., Stumpel N., Wuster W. (2009). When continents collide: phylogeny, historical biogeography and systematics of the medically important viper genus Echis (Squamata: Serpentes: Viperidae). Mol. Phylogenet. Evol. 53, 792–807. doi: 10.1016/j.ympev.2009.08.002 PubMed DOI
Portillo F., Branch W. R., Conradie W., Roedel M. O., Penner J., Barej M. F., et al. . (2018). Phylogeny and biogeography of the African burrowing snake subfamily Aparallactinae (Squamata: Lamprophiidae). Mol. Phylogenet. Evol. 127, 288–303. doi: 10.1016/j.ympev.2018.03.019, PMID: PubMed DOI
Portillo F., Stanley E. L., Branch W. R., Conradie W., Roedel M. O., Penner J., et al. . (2019). Evolutionary history of burrowing asps (Lamprophiidae: Atractaspidinae) with emphasis on fang evolution and prey selection. Plos One 14:e0214889. doi: 10.1371/journal.pone.0214889, PMID: PubMed DOI PMC
Profico A., Di Vincenzo F., Gagliardi L., Piperno M., Manzi G. (2016). Filling the gap. Human cranial remains from Gombore II (Melka Kunture, Ethiopia; ca. 850 ka) and the origin of Homo heidelbergensis. J. Anthropol. Sci. 94, 41–63. doi: 10.4436/jass.94019 PubMed DOI
Prokop P., Fančovičová J., Kučerová A. (2018). Aposematic colouration does not explain fear of snakes in humans. J. Ethol. 36, 35–41. doi: 10.1007/s10164-017-0533-9 DOI
Prokop P., Özel M., Uşak M. (2009). Cross-cultural comparison of student attitudes toward snakes. Society & Animals 17, 224–240. doi: 10.1163/156853009X445398 DOI
Prüfer K., Posth C., Yu H., Stoessel A., Spyrou M. A., Deviese T., et al. . (2021). A genome sequence from a modern human skull over 45,000 years old from Zlatý kůň in Czechia. Nat. Ecol. Evol. 5, 820–825. doi: 10.1038/s41559-021-01443-x, PMID: PubMed DOI PMC
R Development Core Team (2012). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing
Rádlová S., Janovcová M., Sedláčková K., Polák J., Nácar D., Peléšková S., et al. . (2019). Snakes represent emotionally salient stimuli that may evoke both fear and disgust. Front. Psychol. 10:1085. doi: 10.3389/fpsyg.2019.01085 PubMed DOI PMC
Rádlová S., Polák J., Janovcová M., Sedláčková K., Peléšková S., Landová E., et al. . (2020). Emotional reaction to fear- and disgust-evoking snakes: sensitivity and propensity in Snake-fearful respondents. Front. Psychol. 11:31. doi: 10.3389/fpsyg.2020.00031 PubMed DOI PMC
Ramakrishnan U., Coss R. G., Schank J., Dharawat A., Kim S. (2005). Snake species discrimination by wild bonnet macaques (Macaca radiata). Ethology 111, 337–356. doi: 10.1111/j.1439-0310.2004.01063.x DOI
Rasband W. S. (2016). ImageJ U.S.. Bethesda, MD: National Institutes of Health
Ribeiro-Júnior M. A., Ferrari S. F., Lima J. R. F., da Silva C. R., Lima J. D. (2016). Predation of a squirrel monkey (Saimiri sciureus) by an Amazon tree boa (Corallus hortulanus): even small boids may be a potential threat to small-bodied platyrrhines. Primates 57, 317–322. doi: 10.1007/s10329-016-0545-z PubMed DOI
Richter D., Grun R., Joannes-Boyau R., Steele T. E., Amani F., Rue M., et al. . (2017). The age of the hominin fossils from Jebel Irhoud, Morocco, and the origins of the middle stone age. Nature 546, 293–296. doi: 10.1038/nature22335 PubMed DOI
Rightmire G. P. (2009). Middle and later Pleistocene hominins in Africa and Southwest Asia. Proc. Natl. Acad. Sci. U.S.A. 106, 16046–16050. doi: 10.1073/pnas.0903930106, PMID: PubMed DOI PMC
Rito T., Richards M. B., Fernandes V., Alshamali F., Cerny V., Pereira L., et al. . (2013). The first modern human dispersals across Africa. Plos One 8:e80031. doi: 10.1371/journal.pone.0080031 PubMed DOI PMC
Rito T., Vieira D., Silva M., Conde-Sousa E., Pereira L., Mellars P., et al. . (2019). A dispersal of Homo sapiens from southern to eastern Africa immediately preceded the out-of-Africa migration. Sci. Rep. 9:4728. doi: 10.1038/s41598-019-41176-3, PMID: PubMed DOI PMC
Scerri E. M. L., Drake N. A., Jennings R., Groucutt H. S. (2014). Earliest evidence for the structure of Homo sapiens populations in Africa. Quat. Sci. Rev. 101, 207–216. doi: 10.1016/j.quascirev.2014.07.019 DOI
Senut B., Pickford M., Gommery D., Mein P., Cheboi K., Coppens Y. (2001). First hominid from the Miocene (Lukeino formation, Kenya). C. R. Acad. Sci. Ser. IIA Earth Planet. Sci. 332, 137–144. doi: 10.1016/s1251-8050(01)01529-4 DOI
Shine R., Harlow P. S., Keogh J. S., and Boeadi (1998). The influence of sex and body size on food habits of a giant tropical snake, Python reticulatus. Funct. Ecol. 12, 248–258. doi: 10.1046/j.1365-2435.1998.00179.x DOI
Simons E. L., Seiffert E. R., Ryan T. M., Attia Y. (2007). A remarkable female cranium of the early Oligocene anthropoid Aegyptopithecus zeuxis (Catarrhini, Propliopithecidae). Proc. Natl. Acad. Sci. U.S.A. 104, 8731–8736. doi: 10.1073/pnas.0703129104, PMID: PubMed DOI PMC
Šmíd J., Gocmen B., Crochet P. A., Trape J. F., Mazuch T., Uvizl M., et al. . (2019). Ancient diversification, biogeography, and the role of climatic niche evolution in the Old World cat snakes (Colubridae, Telescopus). Mol. Phylogenet. Evol. 134, 35–49. doi: 10.1016/j.ympev.2019.01.015, PMID: PubMed DOI
Šmíd J., Tolley K. A. (2019). Calibrating the tree of vipers under the fossilized birth-death model. Sci. Rep. 9:5510. doi: 10.1038/s41598-019-41290-2 PubMed DOI PMC
Smith S. M. (1977). Coral-snake pattern recognition and stimulus generalisation by naive great kiskadees (Aves: Tyrannidae). Nature 265, 535–536. doi: 10.1038/265535a0 DOI
Smith S. M. (1980). Responses of naive temperate birds to warning coloration. Am. Midl. Nat. 103, 346–352. doi: 10.2307/2424633 DOI
Soares S. C., Lindstrom B., Esteves F., Ohman A. (2014). The hidden Snake in the grass: superior detection of snakes in challenging attentional conditions. Plos One 9:e114724. doi: 10.1371/journal.pone.0114724 PubMed DOI PMC
Springer M. S., Meredith R. W., Gatesy J., Emerling C. A., Park J., Rabosky D. L., et al. . (2012). Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species Supermatrix. Plos One 7:e49521. doi: 10.1371/journal.pone.0049521, PMID: PubMed DOI PMC
Staňková H., Janovcová M., Peléšková Š., Sedláčková K., Landová E., Frynta D. (2021). The ultimate list of the most frightening and disgusting animals: negative emotions elicited by animals in central European respondents. Animals 11:747. doi: 10.3390/ani11030747, PMID: PubMed DOI PMC
StatsSoft Inc (2010). Statistica (data analysis software system). Version 9, 1.
Stringer C. (2016). The origin and evolution of Homo sapiens. Philos. T. Roy. Soc. B 371:20150237. doi: 10.1098/rstb.2015.0237 PubMed DOI PMC
Szyndlar Z. (1991). A review of Neogene and quaternary snakes of central and eastern Europe. Part 11: Natricinae, Elapidae Viperidae. Estudios Geológicos 47, 237–266.
Tao D., He Z., Lin Y., Liu C., Tao Q. (2021). Where does fear originate in the brain? A coordinate-based meta-analysis of explicit and implicit fear processing. NeuroImage 227:117686. doi: 10.1016/j.neuroimage.2020.117686 PubMed DOI
Towers S. R., Coss R. G. (1990). Confronting snakes in the burrow: Snake-species discrimination and antisnake tactics of two California ground squirrel populations. Ethology 84, 177–192. doi: 10.1111/j.1439-0310.1990.tb00796.x DOI
Urciuoli A., Zanolli C., Beaudet A., Pina M., Almecija S., Moya-Sola S., et al. . (2021). A comparative analysis of the vestibular apparatus in Epipliopithecus vindobonensis: phylogenetic implications. J. Hum. Evol. 151:102930. doi: 10.1016/j.jhevol.2020.102930 PubMed DOI
Ursenbacher S., Carlsson M., Helfer V., Tegelstrom H., Fumagalli L. (2006). Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data. Mol. Ecol. 15, 3425–3437. doi: 10.1111/j.1365-294X.2006.03031.x, PMID: PubMed DOI
Valenta J. (2010). Venomous snakes – Envenoming, therapy. New York: Nova Science Publishers, Inc.
Van Le Q., Isbell L. A., Matsumoto J., Le V. Q., Hori E., Tran A. H., et al. . (2014). Monkey pulvinar neurons fire differentially to snake postures. Plos One 9:e114258. doi: 10.1371/journal.pone.0114258 PubMed DOI PMC
Van Le Q., Isbell L. A., Matsumoto J., Nguyen M., Hori E., Maior R. S., et al. . (2013). Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. Proc. Natl. Acad. Sci. U.S. A. 110, 19000–19005. doi: 10.1073/pnas.1312648110 PubMed DOI PMC
van Schaik C. P., Mitrasetia T. (1990). Changes in the behavior of wild long-tailed macaques (Macaca fascicularis) after encounters with a model python. Folia Primatol. 55, 104–108. doi: 10.1159/000156506 PubMed DOI
Van Strien J. W., Christiaans G., Franken I. H. A., Huijding J. (2016). Curvilinear shapes and the snake detection hypothesis: an ERP study. Psychophysiology 53, 252–257. doi: 10.1111/psyp.12564 PubMed DOI
Van Strien J. W., Isbell L. A. (2017). Snake scales, partial exposure, and the Snake detection theory: a human event-related potentials study. Sci. Rep. 7:46331. doi: 10.1038/srep46331, PMID: PubMed DOI PMC
Weiss L., Brandl P., Frynta D. (2015). Fear reactions to snakes in naïve mouse lemurs and pig-tailed macaques. Primates 56, 279–284. doi: 10.1007/s10329-015-0473-3, PMID: PubMed DOI
Westeen E. P., Durso A. M., Grundler M. C., Rabosky D. L., Rabosky A. R. D. (2020). What makes a fang? Phylogenetic and ecological controls on tooth evolution in rear-fanged snakes. BMC Evol. Biol. 20:80. doi: 10.1186/s12862-020-01645-0, PMID: PubMed DOI PMC
White T. D., Asfaw B., DeGusta D., Gilbert H., Richards G. D., Suwa G., et al. . (2003). Pleistocene Homo sapiens from middle awash, Ethiopia. Nature 423, 742–747. doi: 10.1038/nature01669 PubMed DOI
Wieser M. J., Brosch T. (2012). Faces in context: a review and systematization of contextual influences on affective face processing. Front. Psychol. 3:471. doi: 10.3389/fpsyg.2012.00471, PMID: PubMed DOI PMC
Wilcox C. D., Dove S. B., Doss-McDavid W., Greer D. B. (2002). UTHSCSA ImageTool©. San Antonio, TX: University of Texas Health Science Center
Yorek N. (2009). The only good snake is a dead snake: secondary school students' attitudes toward snakes. Biotechnol. Biotec. Eq. 23, 31–35. doi: 10.1080/13102818.2009.10818358 DOI
Zaher H., Murphy R. W., Arredondo J. C., Graboski R., Machado P. R., Mahlow K., et al. . (2019). Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). Plos One 14:e0216148. doi: 10.1371/journal.pone.0216148 PubMed DOI PMC
Why Are Some Snakes More Terrifying and What Is Behind the Fear?
Hooding cobras can get ahead of other snakes in the ability to evoke human fear
Imprint of ancestral and modern threats in human mind - experience of fear, disgust, and anger
Human emotional evaluation of ancestral and modern threats: fear, disgust, and anger