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The Evolution of Group Living

  • Ashley Ward
  • Mike Webster
Chapter

Abstract

When and how did group living evolve? Direct evidence of ancient animals living in groups is hard to come by, and adage has it that behaviour does not fossilise. In fact this is not strictly true, and some paleontological remains have been seen as providing evidence of animals living in groups, albeit with varying degrees of controversy. The abundance of remains of Pleistocene carnivores such as the dire wolf (Canis dirus) and Smilodon (Smilodon fatalis) found in the La Brea Tar Pits in California, viewed in conjunction with what we know of the scavenging behaviour of contemporary African social carnivores, has led to some researchers to speculate that these species too were social (Carbone et al. 2009; Van Valkenburgh et al. 2009). Far earlier still, the Cretaceous-era trackways left by dozens of small theropod dinosaurs and a single larger animal in what is now Lark Quarry in Queensland, Australia, have been suggested by some workers to provide evidence of a stampeding herd, fleeing the approach of a predator (Thulborn and Wade 1979, Fig. 10.1). This interpretation has stirred debate, and more recent analyses conclude that the large dinosaur is most likely an herbivore and that the tracks attributed to the herd of smaller dinosaurs may actually have been laid down sequentially over a longer period of time as individuals forded a shallow or partially dried river crossing (Romilio and Salisbury 2011). While acknowledging the difficulty of inferring sociality from paleontological evidence, we can nevertheless speculate about group living in long extinct species. It is likely that animals living in past environments faced the same kinds of challenges as do contemporary ones, such as finding food, avoiding predators, effectively navigating and so on, and it is therefore not unreasonable to imagine that they met these challenges in many of the same ways, including by forming groups. This speculation is further bolstered by the observations that a diverse range of extant species spend at least some portions of their lives in groups and that among these lineages group living appears to have evolved multiple times, suggesting that group formation might be a common evolution response to particular selection pressures. Phylogenetic analysis allows researchers to map patterns of grouping behaviours onto the living members of clades and, by incorporating information about the evolutionary relationships between these extant species and their extinct ancestors, create statistical models which estimate the appearance and loss of this behaviour over evolutionary time.

Keywords

Brain Size Mushroom Body Group Living Cooperative Breeding Sand Lance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JA, Andersson M, Andre JB, van Baalen M, Balloux F, Balshine S, Barton N, Beukeboom LW, Biernaskie JM, Bilde T, Borgia G, Breed M, Brown S, Bshary R, Buckling A, Burley NT, Burton-Chellew MN, Cant MA, Chapuisat M, Charnov EL, Clutton-Brock T, Cockburn A, Cole BJ, Colegrave N, Cosmides L, Couzin ID, Coyne JA, Creel S, Crespi B, Curry RL, Dall SR, Day T, Dickinson JL, Dugatkin LA, El Mouden C, Emlen ST, Evans J, Ferriere R, Field J, Foitzik S, Foster K, Foster WA, Fox CW, Gadau J, Gandon S, Gardner A, Gardner MG, Getty T, Goodisman MA, Grafen A, Grosberg R, Grozinger CM, Gouyon PH, Gwynne D, Harvey PH, Hatchwell BJ, Heinze J, Helantera H, Helms KR, Hill K, Jiricny N, Johnstone RA, Kacelnik A, Kiers ET, Kokko H, Komdeur J, Korb J, Kronauer D, Kümmerli R, Lehmann L, Linksvayer TA, Lion S, Lyon B, Marshall JA, McElreath R, Michalakis Y, Michod RE, Mock D, Monnin T, Montgomerie R, Moore AJ, Mueller UG, Noë R, Okasha S, Pamilo P, Parker GA, Pedersen JS, Pen I, Pfennig D, Queller DC, Rankin DJ, Reece SE, Reeve HK, Reuter M, Roberts G, Robson SK, Roze D, Rousset F, Rueppell O, Sachs JL, Santorelli L, Schmid-Hempel P, Schwarz MP, Scott-Phillips T, Shellmann-Sherman J, Sherman PW, Shuker DM, Smith J, Spagna JC, Strassmann B, Suarez AV, Sundström L, Taborsky M, Taylor P, Thompson G, Tooby J, Tsutsui ND, Tsuji K, Turillazzi S, Ubeda F, Vargo EL, Voelkl B, Wenseleers T, West SA, West-Eberhard MJ, Westneat DF, Wiernasz DC, Wild G, Wrangham R, Young AJ, Zeh DW, Zeh JA, Zink A (2011) Inclusive fitness theory and eusociality. Nature 471(7339):E1–E4CrossRefPubMedGoogle Scholar
  2. Allen J, Weinrich M, Hoppitt W, Rendell L (2013) Network-based diffusion analysis reveals cultural transmission of lobtail feeding in humpback whales. Science 340(6131):485–488CrossRefPubMedGoogle Scholar
  3. Aplin LM, Farine DR, Morand‐Ferron J, Cole EF, Cockburn A, Sheldon BC (2013) Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecol Lett 16(11):1365–1372CrossRefPubMedGoogle Scholar
  4. Aplin LM, Farine DR, Mann RP, Sheldon BC (2014) Individual-level personality influences social foraging and collective behaviour in wild birds. Pro Roy Soc B Biol Sci 281(1789):20141016CrossRefGoogle Scholar
  5. Aplin LM, Farine DR, Morand-Ferron J, Cockburn A, Thornton A, Sheldon BC (2015) Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518(7540):538–541CrossRefPubMedPubMedCentralGoogle Scholar
  6. Beauchamp G (2002) Higher-level evolution of intraspecific flock-feeding in birds. Behav Ecol Sociobiol 51(5):480–487CrossRefGoogle Scholar
  7. Beauchamp G (2013) Social foragers adopt a riskier foraging mode in the centre of their groups. Biol Lett 9(6). doi: 10.1098/rsbl.2013.0528
  8. Beja-Pereira A, Luikart G, England PR, Bradley DG, Jann OC, Bertorelle G, Chamberlain AT, Nunes TP, Metodiev S, Ferrand N, Erhardt G (2003) Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nature Gene 35(4):311–313CrossRefGoogle Scholar
  9. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77(4):771–783CrossRefPubMedPubMedCentralGoogle Scholar
  10. Boomsma JJ (2007) Kin selection versus sexual selection: why the ends do not meet. Curr Biol 17(16):R673–R683CrossRefPubMedGoogle Scholar
  11. Boomsma JJ, Beekman M, Cornwallis CK, Griffin AS, Holman L, Hughes WO, Keller L, Oldroyd BP, Ratnieks FL (2011) Only full-sibling families evolved eusociality. Nature 471(7339):E4–E5CrossRefPubMedGoogle Scholar
  12. Botham MS, Hayward RK, Morrell LJ, Croft DP, Ward JR, Ramnarine I, Krause J (2008) Risk-sensitive antipredator behavior in the Trinidadian guppy, Poecilia reticulata. Ecology 89(11):3174–3185CrossRefGoogle Scholar
  13. Brashares JS, Garland T, Arcese P (2000) Phylogenetic analysis of coadaptation in behavior, diet, and body size in the African antelope. Behav Ecol 11(4):452–463CrossRefGoogle Scholar
  14. Brown CR, Brown MB (2000) Heritable basis for choice of group size in a colonial bird. Proc Natl Acad Sci 97(26):14825–14830CrossRefPubMedPubMedCentralGoogle Scholar
  15. Carbone C, Maddox T, Funston PJ, Mills MG, Grether GF, Van Valkenburgh B (2009) Parallels between playbacks and Pleistocene tar seeps suggest sociality in an extinct sabretooth cat, Smilodon. Biol Lett 5(1):81–85CrossRefPubMedPubMedCentralGoogle Scholar
  16. Carere C, Drent PJ, Privitera L, Koolhaas JM, Groothuis TG (2005) Personalities in great tits, Parus major: stability and consistency. Anim Behav 70(4):795–805CrossRefGoogle Scholar
  17. Carvalho GR, Shaw PW, Hauser L, Seghers BH, Magurran AE (1996) Artificial introductions, evolutionary change and population differentiation in Trinidadian guppies (Poecilia reticulata: Poeciliidae). Biol J Linn Soc 57(3):219–234CrossRefGoogle Scholar
  18. Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296(5565):69–72CrossRefPubMedGoogle Scholar
  19. Clutton‐Brock T, Janson C (2012) Primate socioecology at the crossroads: past, present, and future. Evol Anthropol 21(4):136–150CrossRefPubMedGoogle Scholar
  20. Cornwallis CK, West SA, Davis KE, Griffin AS (2010) Promiscuity and the evolutionary transition to complex societies. Nature 466(7309):969–972CrossRefPubMedGoogle Scholar
  21. Cote J, Fogarty S, Sih A (2012) Individual sociability and choosiness between shoal types. Anim Behav 83(6):1469–1476CrossRefGoogle Scholar
  22. Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, PrincetonCrossRefGoogle Scholar
  23. Croft DP, Krause J, Darden SK, Ramnarine IW, Faria JJ, James R (2009b) Behavioural trait assortment in a social network: patterns and implications. Behav Ecol Sociobiol 63(10):1495–1503CrossRefGoogle Scholar
  24. Crook JH, Gartlan JS (1966) Evolution of primate societies. Nature 210(5042):1200CrossRefPubMedGoogle Scholar
  25. Di Fiore A, Rendall D (1994) Evolution of social organization: a reappraisal for primates by using phylogenetic methods. Proc Natl Acad Sci 91(21):9941–9945CrossRefPubMedPubMedCentralGoogle Scholar
  26. Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc Royal Soc London Series B Biol Sci 271(1541):847–852CrossRefGoogle Scholar
  27. Dunbar RI (1991) Functional significance of social grooming in primates. Folia Primatol 57(3):121–131CrossRefGoogle Scholar
  28. Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6:178–190CrossRefGoogle Scholar
  29. Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347CrossRefPubMedGoogle Scholar
  30. Dzieweczynski TL, Crovo JA (2011) Shyness and boldness differences across contexts in juvenile three spined stickleback Gasterosteus aculeatus from an anadromous population. J Fish Biol 79(3):776–788CrossRefPubMedGoogle Scholar
  31. Estes R (1991) The behavior guide to African mammals, vol 64. University of California Press, BerkeleyGoogle Scholar
  32. Feeney WE, Medina I, Somveille M, Heinsohn R, Hall ML, Mulder RA, Stein JA, Kilner RM, Langmore NE (2013) Brood parasitism and the evolution of cooperative breeding in birds. Science 342(6165):1506–1508CrossRefPubMedGoogle Scholar
  33. Greenwood AK, Wark AR, Yoshida K, Peichel CL (2013) Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks. Curr Biol 23(19):1884–1888CrossRefPubMedGoogle Scholar
  34. Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302(5645):634–636CrossRefPubMedGoogle Scholar
  35. Hendry AP, Peichel CL, Matthews B, Boughman JW, Nosil P (2013) Stickleback research: the now and the next. Evolu Ecology Res 15(2):111–141Google Scholar
  36. Hughes WO, Oldroyd BP, Beekman M, Ratnieks FL (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320(5880):1213–1216CrossRefPubMedGoogle Scholar
  37. Huizinga M, Ghalambor CK, Reznick DN (2009) The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies, Poecilia reticulata. J Evol Biol 22(9):1860–1866CrossRefPubMedGoogle Scholar
  38. Ioannou CC, Guttal V, Couzin ID (2012) Predatory fish select for coordinated collective motion in virtual prey. Science 337(6099):1212–1215CrossRefPubMedGoogle Scholar
  39. Jarman P (1974) The social organisation of antelope in relation to their ecology. Behaviour 48(1):215–267CrossRefGoogle Scholar
  40. Jolly A (1985) The evolution of primate behavior. Am Sci 73:230–239Google Scholar
  41. Kingdon J (1982) Bovids. East African mammals: an atlas of evolution in AfricaGoogle Scholar
  42. Laland KN, Galef BG (2009) The question of animal culture. Harvard University Press, Cambridge/LondonGoogle Scholar
  43. Laland KN, Hoppitt W (2003) Do animals have culture? Evol Anth Iss News Rev 12(3):150–159CrossRefGoogle Scholar
  44. Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21(10):542–547CrossRefPubMedGoogle Scholar
  45. Laland KN, Odling-Smee J, Myles S (2010) How culture shaped the human genome: bringing genetics and the human sciences together. Nat Rev Genet 11(2):137–148CrossRefPubMedGoogle Scholar
  46. Lefebvre L, Palameta B, Hatch KK (1996) Is group-living associated with social learning? A comparative test of a gregarious and a territorial columbid. Behaviour 133(3):241–261CrossRefGoogle Scholar
  47. Liao X, Rong S, Queller DC (2015) Relatedness, conflict, and the evolution of eusociality. PLoS Biol 13(3):e1002098CrossRefPubMedPubMedCentralGoogle Scholar
  48. Magurran AE (1998) Population differentiation without speciation. Phil Tran Royal Soc B Biol Sci 353(1366):275–286CrossRefGoogle Scholar
  49. Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, OxfordCrossRefGoogle Scholar
  50. Magurran AE, Seghers BH, Carvalho GR, Shaw PW (1992) Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad: evidence for the evolution of anti-predator behaviour in the wild. Proc Royal Soc London Series B Biol Sci 248(1322):117–122CrossRefGoogle Scholar
  51. Magurran AE, Seghers BH, Shaw PW, Carvalho GR (1995) The behavioral diversity and evolution of guppy, Poecilia reticulata, populations in Trinidad. Adv Study Behav 24:155–202CrossRefGoogle Scholar
  52. Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc Royal Soc London B Biol Sci 255(1344):223–229CrossRefGoogle Scholar
  53. Nowak MA, Allen B (2015) Inclusive fitness theorizing invokes phenomena that are not relevant for the evolution of eusociality. PLoS Biolo 13:e1002134CrossRefGoogle Scholar
  54. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466(7310):1057–1062CrossRefPubMedPubMedCentralGoogle Scholar
  55. O’Donnell S, Bulova SJ, DeLeon S, Khodak P, Miller S, Sulger E (2015) Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae). Proc Roy Soc B. doi: 10.1098/rspb.2015.0791 Google Scholar
  56. Olson RS, Hintze A, Dyer FC, Knoester DB, Adami C (2013) Predator confusion is sufficient to evolve swarming behaviour. J R Soc Interface 10(85):20130305CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ostlund-Nilsson S, Mayer I, Huntingford FA (eds) (2006) Biology of the three-spined stickleback. CRC Press, Boca RatonGoogle Scholar
  58. Perez-Barberia FJ, Shultz S, Dunbar RIM (2007) Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61:2811–2821CrossRefPubMedGoogle Scholar
  59. Pike TW, Samanta M, Lindström J, Royle NJ (2008) Behavioural phenotype affects social interactions in an animal network. Proce Royal Soc B Biol Sci 275(1650):2515–2520CrossRefGoogle Scholar
  60. Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175CrossRefGoogle Scholar
  61. Reader SM, Laland KN (eds) (2003) Animal innovation, vol 10. Oxford University Press, OxfordGoogle Scholar
  62. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82(2):291–318CrossRefPubMedGoogle Scholar
  63. Reznick DA, Bryga H, Endler JA (1990) Experimentally induced life-history evolution in a natural population. Nature 346:357–359CrossRefGoogle Scholar
  64. Roche EA, Brown CR, Brown MB (2011) Heritable choice of colony size in cliff swallows: does experience trump genetics in older birds? Anim Behav 82(6):1275–1285CrossRefPubMedPubMedCentralGoogle Scholar
  65. Romilio A, Salisbury SW (2011) A reassessment of large theropod dinosaur tracks from the mid-Cretaceous (late Albian–Cenomanian) Winton Formation of Lark Quarry, central-western Queensland, Australia: a case for mistaken identity. Cretaceous Res 32(2):135–142CrossRefGoogle Scholar
  66. Rosengaus RB, Guldin MR, Traniello JF (1998a) Inhibitory effect of termite fecal pellets on fungal spore germination. J Chem Ecol 24(10):1697–1706CrossRefGoogle Scholar
  67. Rosengaus RB, Maxmen AB, Coates LE, Traniello JF (1998b) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav Ecol Sociobiol 44(2):125–134CrossRefGoogle Scholar
  68. Rosengaus RB, Lefebvre ML, Traniello JF (2000a) Inhibition of fungal spore germination by Nasutitermes: evidence for a possible antiseptic role of soldier defensive secretions. J Chem Ecol 26(1):21–39CrossRefGoogle Scholar
  69. Rosengaus RB, Traniello JFA, Lefebvre ML, Carlock DM (2000b) The social transmission of disease between adult male and female reproductives of the dampwood termite Zootermopsis angusticollis. Ethol Ecol Evol 12(4):419–433CrossRefGoogle Scholar
  70. Schino G (2001) Grooming, competition and social rank among female primates: a meta-analysis. Anim Behav 62(2):265–271CrossRefGoogle Scholar
  71. Serrano D, Tella JL (2007) The role of despotism and heritability in determining settlement patterns in the colonial lesser kestrel. Am Nat 169(2):E53–E67CrossRefPubMedGoogle Scholar
  72. Shultz S, Opie C, Atkinson QD (2011) Stepwise evolution of stable sociality in primates. Nature 479(7372):219–222CrossRefPubMedGoogle Scholar
  73. Sih A, Bell AM, Johnson JC, Ziemba RE (2004a) Behavioral syndromes: an integrative overview. Q Rev Biol 79(3):241–277CrossRefPubMedGoogle Scholar
  74. Sih A, Bell A, Johnson JC (2004b) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19(7):372–378CrossRefPubMedGoogle Scholar
  75. Strassmann JE, Page RE Jr, Robinson GE, Seeley TD (2011) Kin selection and eusociality. Nature 471(7339):E5–E6CrossRefPubMedGoogle Scholar
  76. Thulborn RA, Wade M (1979) Dinosaur stampede in the Cretaceous of Queensland. Lethaia 12(3):275–279CrossRefGoogle Scholar
  77. Traniello JF, Rosengaus RB, Savoie K (2002) The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc Natl Acad Sci 99(10):6838–6842CrossRefPubMedPubMedCentralGoogle Scholar
  78. van Oers K, Drent PJ, De Goede P, Van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc Royal Soc London Series B Biolo Sci 271(1534):65–73CrossRefGoogle Scholar
  79. Van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87(1):120–144CrossRefGoogle Scholar
  80. Van Valkenburgh B, Maddox T, Funston PJ, Mills MG, Grether GF, Carbone C (2009) Sociality in Rancho La Brea Smilodon: arguments favour ‘evidence’ over ‘coincidence’. Biol Lett 5(4):563–564CrossRefPubMedCentralGoogle Scholar
  81. Vitone ND, Altizer S, Nunn CL (2004) Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evolu Ecolo Res 6(2):183–199Google Scholar
  82. Wang ET, Kodama G, Baldi P, Moyzis RK (2006) Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc Natl Acad Sci U S A 103(1):135–140CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wark AR, Greenwood AK, Taylor EM, Yoshida K, Peichel CL (2011) Heritable differences in schooling behavior among threespine stickleback populations revealed by a novel assay. PLoS One 6(3):e18316CrossRefPubMedPubMedCentralGoogle Scholar
  84. Wark AR, Mills MG, Dang LH, Chan YF, Jones FC, Brady SD, Absher DM, Grimwood J, Schmutz J, Myers RM, Kingsley DM, Peichel CL (2012) Genetic architecture of variation in the lateral line sensory system of three spine sticklebacks. G3 (Bethesda) 2(9):1047–1056CrossRefGoogle Scholar
  85. Warner RR (1988) Traditionality of mating-site preferences in a coral reef fish. Nature 335(6192):719–721CrossRefGoogle Scholar
  86. Way GP, Kiesel AL, Ruhl N, Snekser JL, McRobert SP (2015) Sex differences in a shoaling-boldness behavioral syndrome, but no link with aggression. Behav Pro 113:7–12CrossRefGoogle Scholar
  87. Webster MM, Laland KN (2015) Space-use and sociability are not related to public-information use in ninespine sticklebacks. Behav Ecol Sociobiol 69(6):895–907CrossRefGoogle Scholar
  88. Westneat DF, Stewart IR (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396CrossRefGoogle Scholar
  89. Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  90. Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CE, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399(6737):682–685CrossRefPubMedGoogle Scholar
  91. Wilson EO, Hölldobler B (2005) Eusociality: origin and consequences. Proc Natl Acad Sci U S A 102(38):13367–13371CrossRefPubMedPubMedCentralGoogle Scholar
  92. Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75(3):262–300CrossRefGoogle Scholar
  93. Wright D, Rimmer LB, Pritchard VL, Butlin RK, Krause J (2003) Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). J Fish Biol 63(s1):258–259CrossRefGoogle Scholar
  94. Wright D, Nakamichi R, Krause J, Butlin RK (2006) QTL analysis of behavioral and morphological differentiation between wild and laboratory zebrafish (Danio rerio). Behav Genet 36(2):271–284CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Ashley Ward
    • 1
  • Mike Webster
    • 2
  1. 1.School of Life and Environmental SciencesThe University of SydneySydneyAustralia
  2. 2.School of BiologyUniversity of St AndrewsSt AndrewsUK

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