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Comparative and Evolutionary Aspects of the Digestive System and Its Enteric Nervous System Control

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The Enteric Nervous System II

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1383))

Abstract

All life forms must gain nutrients from the environment and from single cell organisms to mammals a digestive system is present. Components of the digestive system that are recognized in mammals can be seen in the sea squirt that has had its current form for around 500my. Nevertheless, in mammals, the organ system that is most varied is the digestive system, its architecture being related to the dietary niche of each species. Forms include those of foregut or hindgut fermenters, single or multicompartment stomachs and short or capacious large intestines. Dietary niches include nectarivores, folivores, carnivores, etc. The human is exceptional in that, through food preparation (>80% of human consumption is prepared food in modern societies), humans can utilize a wider range of foods than other species. They are cucinivores, food preparers. In direct descendants of simple organisms, such as sponges, there is no ENS, but as the digestive tract becomes more complex, it requires integrated control of the movement and assimilation of its content. This is achieved by the nervous system, notably the enteric nervous system (ENS) and an array of gut hormones. An ENS is first observed in the phylum cnidaria, exemplified by hydra. But hydra has no collections of neurons that could in any way be regarded as a central nervous system. All animals more complex than hydra have an ENS, but not all have a CNS. In mammals, the ENS is extensive and is necessary for control of movement, enteric secretions and local blood flow, and regulation of the gut immune system. In animals with a CNS, the ENS and CNS have reciprocal connections. From hydra to human, an ENS is essential to life.

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References

  1. Ábrahám A (1940) Die Innervation des Darmkanals der Gastropoden. Cell Tissue Res 30:273–296

    Google Scholar 

  2. Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199–221

    Article  Google Scholar 

  3. Alexandrowicz J-S (1928) Notes sur l’innervation du tube digestif des céphalopodes. Arch Zool Exp 67:69–90

    Google Scholar 

  4. Allen RD (1974) Food vacuole membrane growth with microtubule-associated membrane transport in Paramecium. J Cell Biol 63:904–922

    Article  CAS  Google Scholar 

  5. Arendt D, Denes AS, Jékely G, Tessmar-Raible K (2008) The evolution of nervous system centralization. Philos Trans R Soc Lond B Biol Sci 363:1523–1528

    Article  Google Scholar 

  6. Bach A, Calsamiglia S, Stern MD (2005) Nitrogen metabolism in the rumen. J Dairy Sci 88:E9–E21

    Article  Google Scholar 

  7. Barker CJ, Gillett A, Polkinghorne A, Timms P (2013) Investigation of the koala (Phascolarctos cinereus) hindgut microbiome via 16S pyrosequencing. Vet Microbiol 167:554–564

    Article  CAS  Google Scholar 

  8. Bernalier-Donadille A (2010) Fermentative metabolism by the human gut microbiota. Gastroenterol Clin Biol 34:S16–S22

    Article  CAS  Google Scholar 

  9. Brouns F, Theuwissen E, Adam A, Bell M, Berger A, Mensink RP (2012) Cholesterol-lowering properties of different pectin types in mildly hyper-cholesterolemic men and women. Eur J Clin Nutr 66:591–599

    Article  CAS  Google Scholar 

  10. Clauss M, Hume ID, Hummel J (2010) Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4:979–992

    Article  CAS  Google Scholar 

  11. Colasanti M, Venturini G, Merante A, Musci G, Lauro GM (1997) Nitric oxide involvement in Hydra vulgaris very primitive olfactory-like system. J Neurosci 17:493–499

    Article  CAS  Google Scholar 

  12. Copeland L, Blazek J, Salman H, Tang MC (2009) Form and functionality of starch. Food Hydrocoll 23:1527–1534

    Article  CAS  Google Scholar 

  13. Copenhaver PF (2007) How to innervate a simple gut: familiar themes and unique aspects in the formation of the insect enteric nervous system. Dev Dyn 236:1841–1864

    Article  CAS  Google Scholar 

  14. Cordain L, Eaton SB, Sebastian A, Mann N, Lindeberg S, Watkins BA, O’Keefe JH, Brand-Miller J (2005) Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 81:341–354

    Article  CAS  Google Scholar 

  15. Dierenfeld ES, Hintz HF, Robertson JB (1982) Utilization of bamboo by the giant panda. J Nutr 112:636–641

    Article  CAS  Google Scholar 

  16. Doerffler-Melly J, Neuhuber WL (1988) Rectospinal neurons: evidence for a direct projection from the enteric to the central nervous system in the rat. Neurosci Lett 92:121–125

    Article  CAS  Google Scholar 

  17. Eng CM, Lieberman DE, Zink KD, Peters MA (2013) Bite force and occlusal stress production in hominin evolution. Am J Phys Anthropol 151:544–557

    Article  Google Scholar 

  18. Fischer A, Canning BJ, Undem BJ, Kummer W (1998) Evidence for an esophageal origin of VIP-IR and NO synthase-IR nerves innervating the guinea pig trachealis: a retrograde neuronal tracing and immunohistochemical analysis. J Comp Neurol 394:326–334

    Article  CAS  Google Scholar 

  19. Furness JB (2006) The enteric nervous system. Blackwell, Oxford

    Google Scholar 

  20. Furness JB, Bravo DM (2015) Humans as cucinivores: comparisons with other species. J Comp Physiol B 185:825–834

    Article  Google Scholar 

  21. Furness JB, Callaghan B, Rivera LR, Cho HJ (2014) The enteric nervous system and gastrointestinal innervation: integrated local and central control. Adv Exp Med Biol 817:39–71

    Article  Google Scholar 

  22. Furness JB, Cottrell JJ, Bravo DM (2015) Comparative physiology of digestion. J Anim Sci 93:485–491

    Article  CAS  Google Scholar 

  23. Furness JB, Fakhry J, Gajewski J, Boyle EK, Fothergill L (2019) The digestive system in evolutionary medicine. In: Brüne M, Schiefenhövel W (eds) Oxford handbook of evolutionary medicine. Oxford University Press, pp 531–562

    Google Scholar 

  24. Furness JB, Rivera LR, Cho H-J, Bravo DM, Callaghan B (2013) The gut as a sensory organ. Nat Rev Gastroenterol Hepatol 10:729–740

    Article  CAS  Google Scholar 

  25. Furness JB, Stebbing MJ (2018) The first brain: species comparisons and evolutionary implications for the enteric and central nervous systems. Neurogastroenterol Motil 30:e13234

    Article  Google Scholar 

  26. García-Arrarás JE, Rojas-Soto M, Jiménez LB, Díaz-Miranda L (2001) The enteric nervous system of echinoderms: unexpected complexity revealed by neurochemical analysis. J Exp Biol 204:865–873

    Article  Google Scholar 

  27. Giez C, Klimovich A, Bosch TC (2021) Neurons interact with the microbiome: an evolutionary-informed perspective. e-Neuroforum. https://doi.org/10.1515/nf-2021-0003

  28. Gershon MD (1999) The enteric nervous system: a second brain. Hosp Pract 34:31–32

    Article  CAS  Google Scholar 

  29. Gordon JL, LeBlanc SJ, Duffield TF (2013) Ketosis treatment in lactating dairy cattle. Vet Clin North Am Food Anim Pract 29:433–445

    Article  Google Scholar 

  30. Gribble FM, Reimann F, Roberts GP (2018) Gastrointestinal hormones. In: Said HM (ed) Physiology of the gastrointestinal tract 6edn. Academic Press, New York, pp 31–70

    Google Scholar 

  31. Grimmelikhuijzen CJP, Dierickx K, Boer GJ (1982) Oxytocin/vasopressin-like immunoreactivity is present in the nervous system of hydra. Neuroscience 7:3191–3199

    Article  CAS  Google Scholar 

  32. Grimmelikhuijzen CJP, Spencer AN, Carré D (1986) Organization of the nervous system of physonectid siphonophores. Cell Tissue Res 246:463–479

    Article  Google Scholar 

  33. Holland LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu J-K (2013) Evolution of bilaterian central nervous systems: a single origin? EvoDevo 4:27

    Article  Google Scholar 

  34. Holst MC, Kelly JB, Powley TL (1997) Vagal preganglionic projections to the enteric nervous system characterized with phaseolus vulgaris-leucoagglutinin. J Comp Neurol 381:81–100

    Article  CAS  Google Scholar 

  35. Hu Y, Wu Q, Ma S, Ma T, Shan L, Wang X, Nie Y, Ning Z, Yan L, Xiu Y, Wei F (2017) Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. Proc Natl Acad Sci 114:1081–1086

    Article  CAS  Google Scholar 

  36. Ierusalimsky VN, Balaban PM (2006) Immunoreactivity to molluskan neuropeptides in the central and stomatogastric nervous systems of the earthworm, lumbricus terrestris L. Cell Tissue Res 325:555–565

    Article  CAS  Google Scholar 

  37. Ito S, Kurokawa M (2007) Coordinated peripheral neuronal activities among the different regions of the digestive tract in Aplysia. Zool Sci 24:714–722

    Article  Google Scholar 

  38. Jin C, Ciochon RL, Dong W, Hunt RM, Liu J, Jaeger M, Zhu Q (2007) The first skull of the earliest giant panda. Proc Natl Acad Sci U S A 104:10932–10937

    Article  CAS  Google Scholar 

  39. Kass-Simon G, Pierobon P (2007) Cnidarian chemical neurotransmission, an updated overview. Comp Biochem Physiol 146:9–25

    Article  CAS  Google Scholar 

  40. Kaul-Strehlow S, Urata M, Minokawa T, Stach T, Wanninger A (2015) Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords. Org Divers Evol 15:405–422

    Article  Google Scholar 

  41. Kelly KA (1980) Gastric emptying of liquids and solids: roles of proximal and distal stomach. Am J Phys 239:G71–G76

    CAS  Google Scholar 

  42. Kennedy AL, Mawe GM (1998) Duodenal sensory neurons project to sphincter of Oddi ganglia in guinea pig. J Neurosci 18:8065–8073

    Article  CAS  Google Scholar 

  43. Kirchgessner AL, Gershon MD (1990) Innervation of the pancreas by neurons in the gut. J Neurosci 10:1626–1642

    Article  CAS  Google Scholar 

  44. Klemm N, Hustert R, Cantera R, Nässel DR (1986) Neurons reactive to antibodies against serotonin in the stomatogastric nervous system and in the alimentary canal of locust and crickets (Orthoptera, Insecta). Neuroscience 17:247–261

    Article  CAS  Google Scholar 

  45. Leonard WR, Snodgrass JJ, Robertson ML (2007) Effects of brain evolution on human nutrition and metabolism. Annu Rev Nutr 27:311–327

    Article  CAS  Google Scholar 

  46. Martinez-Pereira MA, Franceschi RDC, Antunes GDF, Coelho BP, Achaval M, Zancan DM (2013) General morphology and innervation of the midgut and hindgut of Megalobulimus abbreviatus (Gastropoda, Pulmonata). Zool Sci 30:319–330

    Article  Google Scholar 

  47. Martinez-Pereira MA, Franceschi RDC, Coelho BP, Zancan DM (2017) The stomatogastric and enteric nervous system of the pulmonate snail Megalobulimus abbreviatus: a neurochemical analysis. Zool Sci 34:300–311

    Article  CAS  Google Scholar 

  48. Milton K (2003) The critical role played by animal source foods in human (Homo) evolution. J Nutr 133:3886S–3892S

    Article  CAS  Google Scholar 

  49. Milton K, Demment MW (1988) Digestion and passage kinetics of chimpanzees fed high and low fiber diets and comparison with human data. J Nutr 118:1082–1088

    Article  CAS  Google Scholar 

  50. Nässel DR, Eckert M, Muren JE, Penzlin H (1998) Species-specific action and distribution of tachykinin-related peptides in the foregut of the cockroaches Leucophaea maderae and Periplaneta americana. J Exp Biol 201:1615–1626

    Article  Google Scholar 

  51. Neuhuber WL, Appelt M, Polak JM, Baier Kustermann W, Abelli L, Ferri GL (1993) Rectospinal neurons: cell bodies, pathways, immunocytochemistry and ultrastructure. Neuroscience 56:367–378

    Article  CAS  Google Scholar 

  52. Nie Y, Zhang Z, Raubenheimer D, Elser JJ, Wei W, Wei F (2015) Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry. Funct Ecol 29:26–34

    Article  Google Scholar 

  53. Okamoto T, Kurokawa M (2010) The role of the peripheral enteric nervous system in the control of gut motility in the snail Lymnaea stagnalis. Zool Sci 27:602–610

    Article  Google Scholar 

  54. Padbury RTA, Furness JB, Baker RA, Toouli J, Messenger JP (1993) Projections of nerve cells from the duodenum to the sphincter of Oddi and gallbladder of the Australian possum. Gastroenterology 104:130–136

    Article  CAS  Google Scholar 

  55. Podewils LJ, Mintz ED, Nataro JP, Parashar UD (2004) Acute, infectious diarrhea among children in eveloping countries. Semin Pediatr Infect Dis 15:155–168

    Article  Google Scholar 

  56. Raven HC (1936) Notes on the anatomy of the viscera of the giant panda (Ailuropoda melanoleuca). Am Mus Novit 877:1–23

    Google Scholar 

  57. Raz-Bahat M, Douek J, Moiseeva E, Peters EC, Rinkevich B (2017) The digestive system of the stony coral Stylophora pistillata. Cell Tissue Res 368:311–323

    Article  CAS  Google Scholar 

  58. Renard E, Gazave E, Fierro-Constain L, Schenkelaars Q, Ereskovsky A, Vacelet J, Borchiellini C (2013) Porifera (sponges): recent knowledge and new perspectives. eLS. https://doi.org/10.1002/9780470015902.a0001582.pub2

  59. Shimizu H, Koizumi O, Fujisawa T (2004) Three digestive movements in Hydra regulated by the diffuse nerve net in the body column. J Comp Physiol 190:623–630

    Article  Google Scholar 

  60. Shimizu H, Takaku Y, Zhang X, Fujisawa T (2007) The aboral pore of hydra: evidence that the digestive tract of hydra is a tube not a sac. Dev Genes Evol 217:563–568

    Article  Google Scholar 

  61. Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. Cambridge University Press, Cambridge, New York

    Google Scholar 

  62. Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:303–427

    Article  Google Scholar 

  63. Szurszewski JH, Ermilov LG, Miller SM (2002) Prevertebral ganglia and intestinofugal afferent neurones. Gut 51:i6–i10

    Article  Google Scholar 

  64. van Boekel M, Fogliano V, Pellegrini N, Stanton C, Scholz G, Lalljie S, Somoza V, Knorr D, Rao Jasti P, Eisenbrand G (2010) A review on the beneficial aspects of food processing. Mol Nutr Food Res 54:1215–1247

    Article  Google Scholar 

  65. Watanabe H, Fujisawa T, Holstein TW (2009) Cnidarians and the evolutionary origin of the nervous system. Develop Growth Differ 51:167–183

    Article  CAS  Google Scholar 

  66. Watanabe H, Tokuda G (2001) Animal cellulases. Cell Mol Life Sci 58:1167–1178

    Article  CAS  Google Scholar 

  67. Weaver TD (2012) Did a discrete event 200,000—100,000 years ago produce modern humans? J Hum Evol 63:121–126

    Article  Google Scholar 

  68. Westfall JA, Elliott SR, MohanKumar PS, Carlin RW (2000) Immunocytochemical evidence for biogenic amines and immunogold labeling of serotonergic synapses in tentacles of Aiptasia pallida (Cnidaria, Anthozoa). Invertebr Biol 119:370–378

    Article  Google Scholar 

  69. Wrangham R, Conklin-Brittain N (2003) Cooking as a biological trait. Comp Biochem Physiol A Mol Integr Physiol 136:35–46

    Article  Google Scholar 

  70. Yao CK, Muir JG, Gibson PR (2016) Review article: insights into colonic protein fermentation, its modulation and potential health implications. Aliment Pharmacol Ther 43:181–196

    Article  CAS  Google Scholar 

  71. Zhao H, Yang J-R, Xu H, Zhang J (2010) Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo. Mol Biol Evol 27:2669–2673

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Digestive Physiology and Nutrition Laboratories, Florey Institute of Neuroscience and Mental Health, Parkville, VIC, Australia

    John B. Furness

  2. Department of Anatomy & Physiology, University of Melbourne, Parkville, VIC, Australia

    John B. Furness

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  1. John B. Furness
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Correspondence to John B. Furness .

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Editors and Affiliations

  1. College of Medicine & Public Health Flinders Medical Centre, Adelaide, SA, Australia

    Nick J. Spencer

  2. College of Medicine & Public Health Flinders Medical Centre, Adelaide, SA, Australia

    Marcello Costa

  3. South Australian Health & Medical Research Institute, Adelaide, SA, Australia

    Stuart M. Brierley

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Furness, J.B. (2022). Comparative and Evolutionary Aspects of the Digestive System and Its Enteric Nervous System Control. In: Spencer, N.J., Costa, M., Brierley, S.M. (eds) The Enteric Nervous System II. Advances in Experimental Medicine and Biology, vol 1383. Springer, Cham. https://doi.org/10.1007/978-3-031-05843-1_16

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