The Animals

  • Roberto Ligrone


The transition from Proterozoic to Phanerozoic (542 MYA) has been traditionally associated with the appearance of animals in the fossil record; paleontological evidence currently antedates this event to at least 565 MYA. Novel phylogenetic inference challenges traditional phylogeny by substituting the ctenophores for the sponges at the base of the animal tree, implying that fundamental innovations such as the intestine and neurons either evolved independently in the ctenophores and cnidarian/bilateria, or were present in a common ancestor and were lost in the sponges. In line with a “reductive” scenario, old and novel evidence suggests that the absence of a canonical mesoderm in the Cnidaria is a derived character. The evolution of an intestine enabled the animals to switch from phagotrophy, a form of predation necessarily restricted to unicellular prey, to macrotrophy, predation of multicellular organisms. Thus, the intestine was a fundamental innovation that paved the way to the evolution of most other animal traits. The diffusion of animals in Cambrian oceans enhanced organic carbon sequestration at the ocean bottom due to the sinking of carcasses and faeces, thus probably contributing to coeval rise in oxygen concentration. The diffusion of filter-feeding animals reduced the bacterial component of phytoplankton and favoured larger-celled eukaryotic phytoplankton, causing a shift from the stratified, turbid and partly anoxic Proterozoic ocean to a clear-water Palaeozoic ocean dominated by eukaryotic algae. Likewise, predation by animals was a powerful driver of macroalgal evolution and deeply influenced the evolutionary trajectory of land plants.


  1. Alberts B et al (2014) Molecular biology of the cell, VI edn. Garland Science, New YorkGoogle Scholar
  2. Amato KR (2013) Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci Med 1:10–29. CrossRefGoogle Scholar
  3. Benton MJ et al (2015) Constraints on the timescale of animal evolutionary history. Palaeontol Electron 18.1.1FC: 1–106.
  4. Bertrand S, Escriva H (2011) Evolutionary crossroads in developmental biology: amphioxus. Development 138:4819–4830PubMedCrossRefGoogle Scholar
  5. Brunet T, King N (2017) The origin of animal multicellularity and cell differentiation. Dev Cell 43:124–140PubMedPubMedCentralCrossRefGoogle Scholar
  6. Butterfield NJ (2009) Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7(1):1–7PubMedCrossRefGoogle Scholar
  7. Butterfield NJ (2011) Animals and the invention of the phanerozoic earth system. Trends Ecol Evol 26:81–87CrossRefGoogle Scholar
  8. Cavalier-Smith T (2017) Origin of animal multicellularity: precursors, causes, consequences – the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion. Philos Trans R Soc B 372:20150476. CrossRefGoogle Scholar
  9. Cerny R et al (2010) Evidence for the prepattern/cooption model of vertebrate jaw evolution. Proc Natl Acad Sci U S A 107:17262–17267PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chang ES et al (2015) Genomic insights into the evolutionary origin of Myxozoa within Cnidaria. Proc Natl Acad Sci U S A 112:14 912–14 917CrossRefGoogle Scholar
  11. Colbert EH, Morales M, Minkoff EC (2001) Colbert’s evolution of the Vertebrates: a history of the backboned animals through time, 5th edn. Wiley, New DelhiGoogle Scholar
  12. Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124:815–822PubMedCrossRefGoogle Scholar
  13. Cunningham JA et al (2017) The origin of animals: can molecular clocks and the fossil record be reconciled. Bioessays 39:1–12PubMedCrossRefGoogle Scholar
  14. Daeschler EB, Shubin NH, Jenkins FA (2006) A Devonian tetrapod-like fish and the evolution of the tetrapod body plan. Nature 440:757–763CrossRefGoogle Scholar
  15. Davenport ER et al (2017) The human microbiome in evolution. BMC Biol 15:127. PubMedPubMedCentralCrossRefGoogle Scholar
  16. Dawkins R (2004) The ancestor’s tale. A pilgrimage to the dawn of life. Weidenfeld & Nicolson, LondonGoogle Scholar
  17. Donoghue PCJ, Keating JN (2014) Early vertebrate evolution. Palaeontology 57:879–893CrossRefGoogle Scholar
  18. dos Reis M et al (2015) Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales. Curr Biol 25:2939–2950PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dunn CW et al (2014) Animal phylogeny and its evolutionary implications. Annu Rev Ecol Evol Syst 45:371–395CrossRefGoogle Scholar
  20. Dunn CW, Leys SP, Haddock SHD (2015) The hidden biology of sponges and ctenophores. Trends Ecol Evol 30:282–591PubMedCrossRefGoogle Scholar
  21. Eitel M et al (2013) Global diversity of the Placozoa. PLoS ONE 8:e57131. PubMedPubMedCentralCrossRefGoogle Scholar
  22. Erwin DH (2015) Early metazoan life: divergence, environment and ecology. Philos Trans R Soc B 370:20150036. CrossRefGoogle Scholar
  23. Fahey B, Degnan BM (2010) Origin of animal epithelia: insights from the sponge genome. Evol Dev 12:601–617PubMedCrossRefGoogle Scholar
  24. Feuda R et al (2017) Improved modelling of compositional heterogeneity supports sponges as sister to all other animals. Curr Biol 27:3864–3870PubMedCrossRefGoogle Scholar
  25. Gaidos E et al (2007) The Precambrian emergence of animal life: a geobiological perspective. Geobiology 5:351–373CrossRefGoogle Scholar
  26. Garcia-Fernàndez J (2006) The genesis and evolution of homeobox gene clusters. Nat Rev Genet 6:881–891CrossRefGoogle Scholar
  27. Giribet G (2016) New animal phylogeny: future challenges for animal phylogeny in the age of phylogenomics. Org Divers Evol 16:419–426CrossRefGoogle Scholar
  28. Halanych KM (2016) How our view of animal phylogeny was reshaped by molecular approaches: lessons learned. Org Divers Evol. CrossRefGoogle Scholar
  29. Hedrick MS, Jones DR (1999) Control of gill ventilation and air breathing in the bowfin Amia. J Exp Biol 202:87–94PubMedGoogle Scholar
  30. Hejnol A, Martindale MQ (2008a) Acoel development supports a simple planula-like urbilaterian. Philos Trans R Soc B 363:1493–1501CrossRefGoogle Scholar
  31. Hejnol A, Martindale MQ (2008b) Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456:382–386PubMedCrossRefGoogle Scholar
  32. Hejnol A, Martindale MQ (2009) The mouth, the anus, and the blastopore – open questions about questionable openings. In: Telford MJ, Littlewood DTJ (eds) Animal evolution: genomes, fossils and trees. University Press, Oxford, pp 33–40. CrossRefGoogle Scholar
  33. Hejnol A, Martín-Durán JM (2015) Getting to the bottom of anal evolution. Zool Anz 256:61–74. CrossRefGoogle Scholar
  34. Holland LZ et al (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18:1100–1111PubMedPubMedCentralCrossRefGoogle Scholar
  35. Ikuta T (2011) Evolution of invertebrate deuterostomes and Hox/ParaHox genes. Genomics Proteomics Bioinformatics 9:77–96. PubMedPubMedCentralCrossRefGoogle Scholar
  36. Jakob W et al (2004) The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214:170–175PubMedCrossRefGoogle Scholar
  37. Janvier P (2004) Wandering nostrils. Nature 432:23–24PubMedCrossRefGoogle Scholar
  38. Kelava I, Rentzsch F, Technau U (2015) Evolution of eumetazoan nervous systems: insights from cnidarians. Philos Trans R Soc B 370:20150065. CrossRefGoogle Scholar
  39. King N et al (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788PubMedPubMedCentralCrossRefGoogle Scholar
  40. Laurin M, Girondot M, de Ricqlès A (2000) Early tetrapod evolution. Tree 15:118–123PubMedGoogle Scholar
  41. Leys SP, Eerkes-Medrano D (2005) Gastrulation in calcareous sponges: in search of Haeckel’s Gastraea. Integr Comp Biol 45:342–351PubMedCrossRefGoogle Scholar
  42. Leys SP, Riesgo A (2011) Epithelia, an evolutionary novelty of metazoans. J Exp Zool 314B:438–447. CrossRefGoogle Scholar
  43. Leys SP, Nichols SA, Adams EDM (2008) Epithelia and integration in sponges. Integr Comp Biol 49:167–177CrossRefGoogle Scholar
  44. Long JA, Gordon MS (2004) The greatest step in vertebrate history: a paleobiological review of the fish-tetrapod transition. Physiol Biochem Zool 77:700–719PubMedCrossRefGoogle Scholar
  45. Mah JL et al (2014) Choanoflagellate and choanocyte collar-flagellar systems and the assumption of homology. Evol Dev 16:25–37PubMedCrossRefGoogle Scholar
  46. Maldonado M (2004) Choanoflagellates, choanocytes, and animal multicellularity. Invertebr Biol 123:1–22CrossRefGoogle Scholar
  47. Marshall CR, Valentine JW (2010) The importance of preadapted genomes in the origin of the animal body plans and the Cambrian explosion. Evolution 64:1189–1201PubMedGoogle Scholar
  48. Martìn-Durán JM et al (2016) The developmental basis for the recurrent evolution of deuterostomy and protostomy. Nat Ecol Evol 1:1–10. CrossRefGoogle Scholar
  49. Mills DB, Canfield DE (2016) A trophic framework for animal origins. Geobiology 15:197–210. PubMedCrossRefGoogle Scholar
  50. Mills DB et al (2014) Oxygen requirements of the earliest animals. Proc Natl Acad Sci U S A 111:4168–4172PubMedPubMedCentralCrossRefGoogle Scholar
  51. Mills DB et al (2018) The last common ancestor of animals lacked the HIF pathway and respired in low oxygen environments. Elife 7:e31176PubMedPubMedCentralCrossRefGoogle Scholar
  52. Moreno E et al (2009) Tracking the origins of the bilaterian Hox patterning system: insights from the acoel flatworm Symsagittifera roscoffensis. Evol Dev 11:574–581PubMedCrossRefGoogle Scholar
  53. Moroz LL et al (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510:109–114PubMedPubMedCentralCrossRefGoogle Scholar
  54. Nakanishi N, Sogabe S, Degnan BM (2014) Evolutionary origin of gastrulation: insights from sponge development. BMC Biol 12:26. PubMedPubMedCentralCrossRefGoogle Scholar
  55. Paps J (2018) What makes an animal? The molecular quest for the origin of the animal kingdom. Integr Comp Biol 58:654–665PubMedCrossRefGoogle Scholar
  56. Paps J, Holland PWH (2018) Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty. Nat Commun 9:1730. PubMedPubMedCentralCrossRefGoogle Scholar
  57. Paps J et al (2013) Molecular phylogeny of Unikonts: new insights into the position of Apusomonads and Ancyromonads and the internal relationships of Opisthokonts. Protist 164:2–12PubMedCrossRefGoogle Scholar
  58. Perry SF, Sander M (2004) Reconstructing the evolution of the respiratory apparatus in tetrapods. Respir Physiol Neurobiol 144:125–139PubMedCrossRefGoogle Scholar
  59. Peterson KJ et al (2008) The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philos Trans R Soc B 36:1435–1443CrossRefGoogle Scholar
  60. Philippe H et al (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712PubMedCrossRefGoogle Scholar
  61. Pick KS et al (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27:1983–1987PubMedPubMedCentralCrossRefGoogle Scholar
  62. Pierce S, Clack JA, Hutchinson JR (2012) Three-dimensional limb joint mobility in the early tetrapod Ichthyostega. Nature 486:523–526PubMedCrossRefGoogle Scholar
  63. Pisani D et al (2015) Genomic data do not support comb jellies as the sister group to all other animals. Proc Natl Acad Sci U S A 112:15402–15407PubMedPubMedCentralCrossRefGoogle Scholar
  64. Reinhard CT et al (2016) Earth’s oxygen cycle and the evolution of animal life. Proc Natl Acad Sci U S A 113:8933–8938PubMedPubMedCentralCrossRefGoogle Scholar
  65. Ruiz-Trillo I et al (2008) A phylogenomic investigation into the origin of Metazoa. Mol Biol Evol 25:664–672PubMedCrossRefGoogle Scholar
  66. Ryan JF, Chiodin M (2015) Where is my mind? How sponges and placozoans may have lost neural cell types. Philos Trans R Soc B 370:20150059. CrossRefGoogle Scholar
  67. Ryan JF et al (2010) The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. EvoDevo 1:9. PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ryan JF et al (2013) The genome of the ctenophore Mnemiopsis leidyi and Its implications for cell type evolution. Science 342:1242592. PubMedPubMedCentralCrossRefGoogle Scholar
  69. Sagane Y et al (2010) Functional specialization of cellulose synthase genes of prokaryotic origin in chordate larvaceans. Development 137:1483–1492PubMedCrossRefGoogle Scholar
  70. Satoh N, Rokhsar D, Nishikawa T (2014) Chordate evolution and the three-phylum system. Proc R Soc B 281:20141729. PubMedCrossRefGoogle Scholar
  71. Schierwater B (2005) My favorite animal, Trichoplax adhaerens. BioEssays 27:1294–1302PubMedCrossRefGoogle Scholar
  72. Schierwater B et al (2009a) Concatenated analysis sheds light on early metazoan evolution and fuels a modern “urmetazoon” hypothesis. PLoS Biol 7:e1000020. PubMedCentralCrossRefGoogle Scholar
  73. Schierwater B et al (2009b) The Diploblast-Bilateria Sister hypothesis. Commun Integr Biol 2:403–405PubMedPubMedCentralCrossRefGoogle Scholar
  74. Schubert M et al (2006) Amphioxus and tunicates as evolutionary model systems. Trends Ecol Evol 21:269–277PubMedCrossRefGoogle Scholar
  75. Sebé-Pedrós A, Degnan BM, Ruiz-Trillo I (2017) The origin of Metazoa: a unicellular perspective. Nature 18:498–512Google Scholar
  76. Shalchian-Tabrizi K et al (2008) Multigene phylogeny of Choanozoa and the origin of animals. PLoS ONE 3:e2098. PubMedPubMedCentralCrossRefGoogle Scholar
  77. Shedlock AM, Edwards SV (2009) Amniotes (Amniota). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, OxfordGoogle Scholar
  78. Shimeld SM, Donoghue PCJ (2012) Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139:2091–2099PubMedCrossRefGoogle Scholar
  79. Simion P et al (2017) A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol 27:958–967PubMedCrossRefGoogle Scholar
  80. Sommer F, Bäckhed F (2013) The gut microbiota – masters of host development and physiology. Nature 11:227–238Google Scholar
  81. Srivastava M et al (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955–960PubMedCrossRefGoogle Scholar
  82. Srivastava M et al (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726PubMedPubMedCentralCrossRefGoogle Scholar
  83. Steenkamp ET, Wright J, Baldauf SL (2006) The protistan origins of animals and fungi. Mol Biol Evol 23:93–106PubMedCrossRefGoogle Scholar
  84. Strasser B et al (2014) Evolutionary origin and diversification of epidermal barrier proteins in amniotes. Mol Biol Evol 31:3194–3205PubMedPubMedCentralCrossRefGoogle Scholar
  85. Swartz B (2012) A marine stem-tetrapod from the Devonian of Western North America. PLoS ONE 7(3):e33683. PubMedPubMedCentralCrossRefGoogle Scholar
  86. Telford MJ (2006) Animal phylogeny. Curr Biol 16:R981–R985PubMedCrossRefGoogle Scholar
  87. Triques ML, Christoffersen ML (2009) Exaptations in the conquest of land by Tetrapoda. Gaia Scientia 3:69–74Google Scholar
  88. Tyler S (2003) Epithelium – the primary building block for metazoan complexity. Integr Comp Biol 43:55–63PubMedCrossRefGoogle Scholar
  89. Whelan NV et al (2015) Error, signal, and the placement of Ctenophora sister to all other animals. Proc Natl Acad Sci U S A 112:5773–5778PubMedPubMedCentralCrossRefGoogle Scholar
  90. Whelan NV et al (2017) Ctenophore relationships and their placement as the sister group to all other animals. Nat Ecol Evol 1:1737–1746. PubMedPubMedCentralCrossRefGoogle Scholar
  91. Wijesenaa N, Simmonsa DK, Martindalea MQ (2017) Antagonistic BMP–cWNT signaling in the cnidarian Nematostella vectensis reveals insight into the evolution of mesoderm. Proc Natl Acad Sci U S A 114:E5608–E5615. CrossRefGoogle Scholar
  92. Wray JA (2015) Molecular clocks and the early evolution of metazoan nervous systems. Philos Trans R Soc B 370:20150046. CrossRefGoogle Scholar
  93. Wu P et al (2004) Evo-Devo of amniote integuments and appendages. Int J Dev Biol 48:249–270PubMedPubMedCentralCrossRefGoogle Scholar
  94. Xiao S, Laflamme M (2008) On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. Trends Ecol Evol 24:31–40PubMedCrossRefGoogle Scholar
  95. Yeoman CJ et al (2011) Towards an evolutionary model of animal-associated microbiomes. Entropy 13:570–594CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Roberto Ligrone
    • 1
  1. 1.Department of Environmental, Biological and Pharmaceutical Sciences and TechnologiesUniversity of Campania “Luigi Vanvitelli”CasertaItaly

Personalised recommendations