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Multiple paedomorphic lineages of soft-substrate burrowing invertebrates: parallels in the origin of Xenocratena and Xenoturbella


Autoři: Alexander Martynov aff001;  Kennet Lundin aff002;  Bernard Picton aff004;  Karin Fletcher aff006;  Klas Malmberg aff003;  Tatiana Korshunova aff001
Působiště autorů: Zoological Museum, Moscow State University, Moscow, Russia aff001;  Gothenburg Natural History Museum, Gothenburg, Sweden aff002;  Gothenburg Global Biodiversity Centre, Gothenburg, Sweden aff003;  National Museums Northern Ireland, Holywood, Northern Ireland, United Kingdom aff004;  Queen’s University, Belfast, Northern Ireland, United Kingdom aff005;  Milltech Marine, Port Orchard, Washington, United States of America aff006;  Gothenburg Global Biodiversity Centre, Aquatilis, Gothenburg, Sweden aff007;  Koltzov Institute of Developmental Biology RAS, Moscow, Russia aff008
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227173

Souhrn

Paedomorphosis is an important evolutionary force. It has previously been suggested that a soft-substrate sediment-dwelling (infaunal) environment facilitates paedomorphic evolution in marine invertebrates. However, until recently this proposal was never rigorously tested with robust phylogeny and broad taxon selection. Here, for the first time, we present a molecular phylogeny for a majority of the 21 families of one of the largest nudibranch subgroups (Aeolidacea) and show that the externally highly simplified vermiform nudibranch family, Pseudovermidae, with clearly defined paedomorphic traits and inhabiting a soft-substrata environment, is a sister group to the complex nudibranch family, Cumanotidae. We also report the rediscovery of one of the most enigmatic nudibranchs–Xenocratena suecica–on the Swedish and Norwegian coasts 70 years after it was first found. Xenocratena was described from the same location and environment in the Swedish Gullmar fjord as one of the most enigmatic vermiform organisms, Xenoturbella bocki, which represents either an original simple bilaterian body plan or secondary simplification of a more complex organisation. Our results show that Xenocratena suecica reveals an onset of parallel paedomorphic evolution so we have proposed the new family, Xenocratenidae fam. n., to accommodate the molecular and morphological disparities we discovered. The paedomorphic origin of another aeolidacean family, Embletoniidae, is also demonstrated for the first time. Thus, by presenting three independent lineages from non-closely related aeolidacean families, Xenocratenidae fam. n., Cumanotidae and Embletoniidae, we confirm with phylogenetic data that a soft-substrata burrowing-related environment strongly favours paedomorphic evolution. We suggest criteria to distinguish ancestral and derived characters in the context of modifications of ontogenetic cycles. Applying an evolutionary model of the soft substrate-driven multiple paedomorphic origin of several families of nudibranch molluscs we propose that it is plausible to extend this model to other marine invertebrates and suggest that the ancestral organisation of the enigmatic metazoan, Xenoturbella, might correspond to the larval part of a complex ancestral bilaterian ontogenetic cycle with sedentary/semi-sedentary adult stages and planula-like larval stages.

Klíčová slova:

Animal phylogenetics – Evolutionary processes – Molluscs – Phylogenetic analysis – Phylogenetics – Teeth – Burrowing – Echinoderms


Zdroje

1. Bhullar BA, Marugán-Lobón J, Racimo F, Bever GS, Rowe TB, Norell MA et al. Birds have paedomorphic dinosaur skulls. Nature. 2012; 487: 223–226. https://doi.org/10.1038/nature11146 22722850

2. Somel M, Franz H, Yan Z, Lorenc A, Guo S, Giger T et al. Transcriptional neoteny in the human brain. PNAS. 2009; 106: 5743–5748. https://doi.org/10.1073/pnas.0900544106 19307592

3. Bocak L, Kundata R, Fernandez CA, Vogler AP. The discovery of Iberobaeniidae (Coleoptera: Elateroidea): a new family of beetles from Spain, with immatures detected by environmental DNA sequencing. Proc R Soc Lond. 2016; B 283: 20152350. https://doi.org/10.1098/rspb.2015.2350 27147093

4. Martynov A, Ishida Y, Irimura S, Tajiri R, O'Hara T, Fujita T. When ontogeny matters: A new Japanese species of brittle star illustrates the importance of considering both adult and juvenile characters in taxonomic practice. PLOS ONE. 2015; 15: e0139463. https://doi.org/10.1371/journal.pone.0139463 PMC4625035

5. Andrade SC, Novo M, Kawauchi GY, Worsaae K, Pleijel F, Giribet G et al. Articulating “Archiannelids”: phylogenomics and annelid relationships, with emphasis on meiofaunal taxa. Mol Biol Evol. 2015; 32: 2860–2875. https://doi.org/10.1093/molbev/msv157 26205969

6. Westheide W. Progenesis as a principle in meiofauna evolution. J Nat Hist. 1987; 21: 843–854. https://doi.org/10.1080/00222938700770501

7. Boaden PJS. Meiofauna and the origins of the Metazoa. Zool J Linn Soc. 1989; 96: 217–227. https://doi.org/10.1111/j.1096-3642.1989.tb02257.x

8. Nakano H. What is Xenoturbella? Zool Lett. 2015; 1: 22. https://doi.org/10.1186/s40851-015-0018-z

9. Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, et al. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature. 2011; 470: 255–258. https://doi.org/10.1038/nature09676 21307940

10. Rouse GW, Wilson NG, Carvajal JI, Vrijenhoek RC. New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature. 2016; 530: 94–97. https://doi.org/10.1038/nature16545 26842060

11. Cannon JT, Vellutini BC, Smith J, Ronquist F, Jondelius U, Hejnol A. Xenacoelomorpha is the sister group to Nephrozoa. Nature. 2016; 530: 89–93. https://doi.org/10.1038/nature16520 26842059

12. Delsuc F, Philippe H, Tsagkogeorga G, Simion P, Tilak MK, Turon X et al. A phylogenomic framework and timescale for comparative studies of tunicates. BMC Biology. 2018; 16: 39. https://doi.org/10.1186/s12915-018-0499-2 29653534

13. Kano Y, Brenzinger B, Nützel A, Wilson NG, Schrödl M. Ringiculid bubble snails recovered as the sister group to sea slugs (Nudipleura). Sci. Rep. 2016; 6: 30908. https://doi.org/10.1038%2Fsrep30908 27498754

14. Wägele H, Klussmann-Kolb A, Verbeek E, Schrödl M. Flashback and foreshadowing—a review of the taxon Opisthobranchia. Org Div Evol. 14; 2014: 133–149. https://doi.org/10.1007/s13127-013-0151-5

15. Katz PS. Evolution of central pattern generators and rhythmic behaviours. Phil Trans R Soc B. 2016; 371: 20150057. https://doi.org/10.1098%2Frstb.2015.0057 26598733

16. Nuzzo G, Ciavatta ML, Kiss R, Mathieu V, Leclercqz H, Manzo E et al. Chemistry of the Nudibranch Aldisa andersoni: structure and biological activity of phorbazole metabolites. Marine Drugs. 2012; 10: 1799–1811. https://doi.org/10.3390%2Fmd10081799 23015775

17. Martin R, Heß M, Schrödl M, Tomaschko KH. Cnidosac morphology in dendronotacean and aeolidacean nudibranch molluscs: from expulsion of nematocysts to use in defense? Mar. Biol. 2009; 156: 261–268. https://doi.org/10.1007/s00227-008-1080-2

18. Goodheart JS, Bleidißel S, Schillo D, Strong EE, Ayres DL, Preisfeld A. Comparative morphology and evolution of the cnidosac in Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia). Front Zool. 2018; 15: 43. https://doi.org/10.1186%2Fs12983-018-0289-2 30473719

19. Korshunova TA, Martynov AV, Bakken T, Evertsen J, Fletcher K, Mudianta IW et al. Polyphyly of the traditional family Flabellinidae affects a major group of Nudibranchia: aeolidacean taxonomic reassessment with descriptions of several new families, genera, and species (Mollusca, Gastropoda). ZooKeys. 2017: 717: 1–139. https://doi.org/10.3897%2Fzookeys.717.21885 29391848

20. Goodheart JA, Bazinet AL, Valdés Á, Collins AG, Cummings MP. Prey preference follows phylogeny: evolutionary dietary patterns within the marine gastropod group Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia). BMC Evol. Biol. 2017; 17: 221. https://doi.org/10.1186/s12862-017-1066-0 29073890

21. Korshunova TA, Picton B, Furfaro G, Mariottini P, Pontes M, Prkić J, et al. Multilevel fine-scale diversity challenges the ‘cryptic species’ concept. Scientific Reports. 2019; 9: 6732. https://doi.org/10.1038/s41598-019-42297-5 31043629

22. Jörger KM, Stoschek T, Migotto AE, Haszprunar G, Neusser TP. 3D-microanatomy of the mesopsammic Pseudovermis salamandrops Marcus, 1953 from Brazil (Nudibranchia, Gastropoda). Mar Biodiv. 2014; 44: 327–341. https://doi.org/10.1007/s12526-014-0224-5

23. Odhner NH. Eine neue Nacktschnecke, Xenocratena suecica n. gen. n. sp., und ihre Verwandtschaft. Ark Zool. ser. 1. 1940; 32; 1–8.

24. Westblad E. Xenoturbella bocki n.g., n. sp. a peculiar, primitive turbellarian type. Ark Zool. ser. 2, 1949: 1: 11–29.

25. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res. 2002; 30: 3059–3066. https://doi.org/10.1093/nar/gkf436 12136088

26. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007; 56: 564–577. https://doi.org/10.1080/10635150701472164 17654362

27. Nylander JA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL. Bayesian phylogenetic analysis of combined data. Syst Biol. 2004; 53: 47–67. https://doi.org/10.1080/10635150490264699 14965900

28. Akaike H. A new look at the statistical model identification. IEEE Trans Automat Control. 1974; 19: 716–723. https://doi.org/10.1007/978-1-4612-1694-0_16

29. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012; 61: 539–542. https://doi.org/10.1093/sysbio/sys029 22357727

30. Stamatakis A, Hoover P, Rougemont JA. Rapid bootstrap algorithm for the RAxML web-servers. Syst. Biol. 2008; 75: 758–771. https://doi.org/10.1080/10635150802429642 18853362

31. Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis. Version 3.10. 2016. Available at http://mesquiteproject.org

32. McNamara KJ. A Guide to the nomenclature of heterochrony. J Paleontol. 1986; 60: 4–13. https://doi.org/10.1017/S0022336000021454

33. Bonett RM, Steffen MA, Robison GA. Heterochrony repolarized: a phylogenetic analysis of developmental timing in plethodontid salamanders. Evodevo. 2014; 5: 27. https://doi.org/10.1186/2041-9139-5-27 25243058

34. Martynov AV, Schrödl M. Phylogeny and evolution of corambid nudibranchs (Mollusca: Gastropoda). Zool J Linn Soc. 2011; 163: 585–604. https://doi.org/10.1111/j.1096-3642.2011.00720.x

35. Martynov A, Brenzinger B, Hooker Y, Schrödl M. 3D-anatomy of a new tropical Peruvian nudibranch gastropod species, Corambe mancorensis, and novel hypotheses on dorid gill ontogeny and evolution. J Molluscan Stud. 2011; 77: 129–141. https://doi.org/10.1093/mollus/eyq047

36. Martynov AV, Korshunova TA. A new deep-sea genus of the family Polyceridae (Nudibranchia) possesses a gill cavity, with implications for the cryptobranch condition and a ‘Periodic Table’ approach to taxonomy. J. Moll. Stud. 2015; 81: 365–379. https://doi.org/10.1093/mollus/eyv003

37. Martynov AV, Korshunova TA, Padula V, Picton B, Schrödl M. Was the common ancestor of dorids cryptobranchiate or phanerobranchiate? Re-reorganizing onchidoridid systematics. 5th International Workshop on opisthobranchs, Abel Salazar Institute of Biomedical Sciences University of Porto Porto, Portugal, Book of Abstracts; 2015. pp. 32–33.

38. Korshunova TA, Fletcher K, Picton B, Lundin K, Sho K et al. The Emperor Cadlina, hidden diversity and gill cavity evolution: new insights for the taxonomy and phylogeny of dorid nudibranchs (Mollusca: Gastropoda). Zool. J. Linn. Soc. (accepted).

39. Koehler R. Echinodermes recueillis par l’Investigator” dans l’Ocean Indien. I. Les Ophiures de mer profonde. Ann Sci Nat Zool Ser 8. 1897; 4: 277–372.

40. Martynov AV, Ishida Y, Irimura S, Tajiri R, O’Hara T, Fujita T. When ontogeny matters: a new Japanese species of brittle star illustrates the importance of considering both adult and juvenile characters in taxonomic practice. PLOS ONE. 2015; 10: e0139463. doi: 10.1371/journal.pone.0139463 26509273

41. Stöhr S, Martynov AV. Paedomorphosis as an evolutionary driving force: insights from deep-sea brittle stars. PLOS ONE. 2016; 11: e0164562. https://doi.org/10.1371/journal.pone.0164562 27806039

42. O'Hara TD, Hugall AF, Thuy B, Stöhr S, Martynov AV. Restructuring higher taxonomy using broad-scale phylogenomics: The living Ophiuroidea. Mol Phylogenet Evol. 2017; 107: 415–430. doi: 10.1016/j.ympev.2016.12.006 27940329

43. Marshall NB. Progenetic tendencies in deep-sea fishes. In: Potts GW, Wootton RJ, editors. Fish Reproduction: Strategies and Tactics. London; Orlando: Fisheries Society of the British Isles; Academic Press; 1984. pp. 91–101.

44. Korshunova TA, Lundin K, Malmberg K, Picton B, Martynov AV. First true brackish-water nudibranch mollusc provides new insights for phylogeny and biogeography and reveals paedomorphosis-driven evolution. PLOS ONE. 2018; 13: e0192177. https://doi.org/10.1371/journal.pone.0192177 29538398

45. Garstang M. The morphology of the Tunicata, and its bearing on the phylogeny of the Chordata. Quart J Micr Sci. 1928; 72: 52–187.

46. McKinney ML, McNamara KJ. The evolution of ontogeny. Plenum Pres; 1991, 437 p.

47. Kollman J. Das Ueberwintern von europeischen Frosch- und Tritonlarven und die Umwandlung des mexikanischen Axolotl. Verh. Naturfor. Gesell. Basel 1885; 7: 387–398.

48. Giard D. La castration parasitaire et son influence sur les caracteres exterieurs du sexe male ches les crustaces decapodes. Bull. Sci, Dep. du Nord 1887; 18: 1–28.

49. Yushin VV, Malakhov V.V. The origin of nematode sperm: progenesis at the cellular level. Rus. J. Mar. Biol 2014; 40: 71–81. https://doi.org/10.1134/S1063074014020114

50. Worsaae K, Giribet G, Martíne A. The role of progenesis in the diversification of the interstitial annelid lineage Psammodrilidae. Invert. Syst. 2018; 32: 774–793 https://doi.org/10.1071/IS17063

51. Gould SJ. Ontogeny and Phylogeny. Cambridge: Belknap Press; 1977.

52. Godfrey LR, Sutherland MR. Paradox of peramorphic paedomorphosis: heterochrony and human evolution. Am J Phys Anthropol. 1996; 99: 17–42. 10.1002/ajpa.1330990102 8928718

53. Bufill E, Agustí J, Blesa R. Human neoteny revisited: The case of synaptic plasticity. Am J Hum Biol. 2011; 23: 729–739. doi: 10.1002/ajhb.21225 21957070

54. McNamara KJ. Heterochrony: the evolution of development. Evo Edu Outreach 2012; 5: 203–218 https://doi/10.1007/s12052-012-0420-3

55. Smirnov SV. Paedomorphosis as a mechanism of evolutionary transformation, in: Modern Evolutionary Morphology, Vorobjeva E. I. and Vronskiy E. I. (eds.), 1991; Kiev: Naukova Dumka, pp. 88–104.

56. Rundell RJ, Leander BS. Masters of miniaturization: convergent evolution among interstitial eukaryotes. Bioessays. 2010; 32: 430–437. 10.1002/bies.200900116 20414901

57. Denoël M, Joly P. Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata). Proc R Soc Lond. 2000; 267: 1481–1485. https://doi.org/10.1098/rspb.2000.1168

58. Reilly SM, Wiley EO, Meinhardt DJ. An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biol J Linn Soc 1997; 60: 119–143. https://doi.org/10.1006/bijl.1996.0092

59. Alberch P, Gould SJ, Oster GF, Wake DB. Size and shape in ontogeny and phylogeny. Paleobiology 1979; 5: 296–317. https://doi.org/10.1017/S0094837300006588

60. Martynov AV. Ontogenetic systematics: The synthesis of taxonomy, phylogenetics, and evolutionary developmental biology. Paleontol J. 2012; 46: 833–864. 10.1134/S0031030112080072

61. Minelli A. EvoDevo and its significance for animal evolution and phylogeny. In: Wanninger A, editor. Evolutionary Developmental Biology of Invertebrates 1. Springer Vienna; 2015. pp. 1–23. Available: http://link.springer.com/chapter/10.1007/978-3-7091-1862-7_1

62. Sevastopulo GD, Lane NG. Ontogeny and phylogeny of disparid crinoids. In Paul CRC, Smith AB (eds.), Echinoderm phylogeny and evolutionary biology. 1988; Oxford University Press, Oxford, pp. 245–253.

63. Klingenberg CP. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol. Rev. 1998; 73: 79–112. https://doi.org/10.1017/S000632319800512X 9569772

64. McNamara KJ, McKinney ML. Heterochony, disparity, and macroevolution. Paleobiology 2005; 31: 17–26. https://doi.org/10.1666/0094-8373(2005)031

65. Shkil FN, Kapitanova DV, Borisov VB, Abdissa B, Smirnov SV. Thyroid hormone in skeletal development of cyprinids: effects and morphological consequences. J. Appl. Ichthyol. 2012; 28: 398–405. https://doi.org/10.1111/j.1439-0426.2012.01992.x

66. Rozhnov SV, Mirantsev GV. Structural aberrations in the cup in cladid crinoids from the Carboniferous of the Moscow region. Paleont. J. 2014; 12: 1243–1257. https://doi.org/10.1134/S0031030114120090

67. Smirnov AV. Paedomorphosis and heterochrony in the origin and evolution of the class Holothuroidea. Paleont. J. 2015; 49: 1597–1615. https://doi.org/10.1134/S003103011514018X

68. Luque J, Feldmann RM, Vernygora O, Schweitzer CE, Cameron CB, Kerr KA et al. Exceptional preservation of mid-Cretaceous marine arthropods and the evolution of novel forms via heterochrony. Sci. Advan. 2019; 5: eaav3875. 10.1126/sciadv.aav3875

69. Bonett RM, Blair AL. Evidence for complex life cycle constraints on salamander body form diversification. Proc Natl Acad Sci U S A. 2017; 114: 9936–9941. 10.1073/pnas.1703877114 28851828

70. Denoël M, Ficetola GF. Heterochrony in a complex world: disentangling environmental processes of facultative paedomorphosis in an amphibian. J Anim Ecol. 2014; 83: 606–615. 10.1111/1365-2656.12173 24180255

71. Wägele H, Willan RC. Phylogeny of the Nudibranchia. Zool. J. Linn. Soc. 2000 130: 83–181.

72. Martynov AV. From “tree-thinking” to “cycle-thinking”: ontogenetic systematics of nudibranch molluscs. Thalassas 2011; 27: 193–224.

73. Pabst EA, Kocot KM Phylogenomics confirms monophyly of Nudipleura (Gastropoda: Heterobranchia). J. Moll. Studies 2018; 84: 259–265.

74. Picton BE. Cumanotus beaumonti (Eliot, 1906), a nudibranch adapted for life in a shallow sandy habitat? Malacologia 1991; 32: 219–222.

75. Boaden PJS. Littoral interstitial species from Anglesey representing three families new to Britain. Nature 1961; 191: 512. https://doi.org/10.1038/191512a0

76. Martynov AV. Archaic Tergipedidae of the Arctic and Antarctic: Murmania antiqua gen. et sp. n. from the Barents Sea and a revision of the genus Guyvalvoria Vayssière with descriptions of two new species. Ruthenica 2006; 16: 73–88.

77. Vinther J, Parry L, Briggs DEG, Van Roy P. Ancestral morphology of crown-group molluscs revealed by a new Ordovician stem aculiferan. Nature 2017: 542: 471–474. doi: 10.1038/nature21055 28166536

78. MolluscaBase (2018). Xenocratena Odhner, 1940. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=742746

79. Korshunova TA, Martynov AV, Picton BE. Ontogeny as an important part of integrative taxonomy in tergipedid aeolidaceans (Gastropoda: Nudibranchia) with a description of a new genus and species from the Barents Sea. Zootaxa. 2017; 4324: 1–22. https://doi.org/10.11646/zootaxa.0000.0.0

80. Flammensbeck CK, Haszprunar G, Korshunova TA, Martynov AV, Neusser TP, Jörger KM. Pseudovermis paradoxus 2.0—3D microanatomy and ultrastructure of a vermiform, meiofaunal nudibranch (Gastropoda, Heterobranchia). Org Divers Evol. 2019; 19: 41. https://doi.org/10.1007/s13127-018-0386-2

81. Bonett RM, Phillips JG, Ledbetter NM, Martin SD, Lehman L. Rapid phenotypic evolution following shifts in life cycle complexity. Proc R Soc. 2018; B285: 20172304. https://doi.org/10.1098/rspb.2017.2304 29343600

82. Miller MC, Willan RC. Redescription of Embletonia gracile Risbec, 1928 (Nudibranchia: Embletoniidae): relocation to suborder Dendronotacea with taxonomic and phylogenetic implications. J Moll Stud. 1991; 58: 1–12. https://doi.org/10.1093/mollus/58.1.1

83. Brenzinger B, Haszprunar G, Schrödl M. At the limits of a successful body plan– 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod. Front Zool. 2013; 10: 37. https://doi.org/10.1186/1742-9994-10-37 23809165

84. Laumer CE, Bekkouche N, Kerbl A, Goetz F, Neves RC, Sørensen MV et al. Spiralian phylogeny informs the evolution of microscopic lineages. Curr Biol. 2015; 25: 1–7. https://doi.org/10.1016/j.cub.2015.06.068

85. Worsaae K, Sterrer W, Kaul-Strehlow S, Hay-Schmidt A, Giribet G. An anatomical description of a miniaturized acorn worm (Hemichordata, Enteropneusta) with asexual reproduction by paratomy. PLOS ONE 2012; 7: e48529. https://doi.org/10.1371/journal.pone.0048529 23144898

86. Haszprunar G. Review of data for a morphological look on Xenacoelomorpha (Bilateria incertae sedis). Org Div Evol. 2016; 16: 363–389. https://doi.org/10.1007/s13127-015-0249-z

87. Nakano H, Lundin K, Bourlat SJ, Telford MJ, Funch P, Nyengaard JR, et al. Xenoturbella bocki exhibits direct development with similarities to Acoelomorpha. Nat Comm. 2013; 4: 1537. https://doi.org/10.1038%2Fncomms2556 23443565

88. Ruiz-Trillo I, Paps J. Acoelomorpha: earliest branching bilaterians or deuterostomes? Org Div Evol. 2016; 16: 391–399. https://doi.org/10.1007/s13127-015-0239-1

89. Brauchle M, Bilican A, Eyer C, Bailly X, Martínez P, Ladurner P et al. Xenacoelomorpha survey reveals that all 11 animal homeobox gene classes were present in the first bilaterians. Genome Biol Evol. 2018; 10: 2205–2217. https://doi.org/10.1093/gbe/evy170 30102357

90. Philippe H, Poustka AJ, Chiodin M, Hoff KJ, Dessimoz C, Tomiczek B et al. Mitigating anticipated effects of systematic errors supports sister-group relationship between Xenacoelomorpha and Ambulacraria. Curr Biol. 2019; 29: 1–9. https://doi.org/10.1016/j.cub.2019.04.009

91. Buckland‑Nicks J, Lundin K, Wallberg A. The sperm of Xenacoelomorpha revisited: implications for the evolution of early bilaterians. Zoomorphology 2019; 138: 13–27. https://doi.org/10.1007/s00435-018-0425-8

92. Andrikou C, Thiel D, Ruiz-Santiesteban JA, Hejnol A. Active mode of excretion across digestive tissues predates the origin of excretory organs. PLOS Biol; 2019; 17: e3000408. https://doi.org/10.1371/journal.pbio.3000408 31356592

93. Van Iten H, Marques AC, de Moraes Leme J, Forancelli Pacheco MLAet al. Origin and early diversification of the phylum Cnidaria Verrill: major developments in the analysis of the taxon’s Proterozoic–Cambrian history. Palaeontology 2014; 57: 677–960. https://doi.org/10.1111/pala.12116

94. Kayal E, Bentlage B, Pankey MS, Ohdera AH, Medina M, Plachetzki DC et al. Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits. BMC Evol. Biol. 2018; 18: 68 https://doi.org/10.1186/s12862-018-1142-0

95. Leininger S, Adamski M, Bergum B, Guder C, Liu J, Laplante M et al. Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans. Nature Communications 2014; 5: 3905. doi: https://doi.org/10.1038/ncomms4905 24844197

96. Nielsen C. Six major steps in animal evolution: are we derived sponge larvae? Evol. Dev. V. 2008; 10: 241–257. https://doi.org/10.1111/j.1525-142X.2008.00231.x 18315817

97. Simion P, Philippe H, Baurain D, Jager M, Richter DJ, Di Franco A et al. A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Current Biology 2017; 27: 1–10. https://doi/10.1016/j.cub.2017.02.031

98. Borisenko I, Adamski M, Ereskovsky A, Adamska M. Surprisingly rich repertoire of Wnt genes in the demosponge Halisarca dujardini. BMC Evol Biol. 2016; 16: 123. https://doi/10.1186/s12862-016-0700-6 27287511

99. Renard E, Leys SP, Wörheide G, Borchiellini C. Understanding animal evolution: the added value of sponge transcriptomics and genomics: the disconnect between gene content and body plan evolution. Bioessays 2018; 40: e1700237. 10.1002/bies.201700237 30070368

100. Zhao Y, Vinther J, Parry LA, Wei F, Green E, Pisani D et al. Cambrian sessile, suspension feeding stem-group ctenophores and evolution of the comb jelly body plan. Curr Biol. 2019; 29: 1112–1125. https://doi.org/10.1016/j.cub.2019.02.036 30905603

101. Rieger RM. The biphasic life cycle–a central theme of metazoan evolution. Amer Zool. 1994; 34: 484–491.

102. Martynov AV. Ontogeny, systematics, and phylogenetics: perspectives of future synthesis and a new model of the evolution of Bilateria. Biol. Bull. 2012; 39: 393–401. https://doi.org/10.1134/S106235901205010X

103. Topper TT, Guo J, Clausen S, Skovsted CB, Zhang Z. A stem group echinoderm from the basal Cambrian of China and the origins of Ambulacraria. Nat. Comm. 2019; 10:1366 https://doi.org/10.1038/s41467-019-09059-3

104. Smith AB, Zamora S. 2013. Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan. Proc R Soc B 2013; 280: 20131197. https://doi.org/10.1098/rspb.2013.1197

105. Smith AB, Zamora S, Javier Á. The oldest echinoderm faunas from Gondwana show that echinoderm body plan diversification was rapid. Nat. Comm. 2013; 4:1385 https://doi.org/10.1038/ncomms2391

106. Rahman IA, Waters JA, Sumrall CD, Astolfo A. Early post-metamorphic, Carboniferous blastoid reveals the evolution and development of the digestive system in echinoderms. Biol. Lett. 2015; 11: 20150776. https://doi.org/10.1098/rsbl.2015.0776

107. Tassia MG, Cannon JT, Konikoff CE, Shenkar N, Halanych KM, Swalla BJ. The global diversity of Hemichordata. PLoS ONE 2016; 11: e0162564. 10.1371/journal.pone.0162564 27701429

108. Tagawa K. Hemichordate models. Curr Opin Genet Dev. 2016; 39: 71–78. https://doi/10.1016/j.gde.2016.05.023 27328429

109. Cameron CB, Garey JR, Swalla BJ. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. P Natl Acad Sci USA. 2000; 97(9): 4469–4474. https://doi.org/10.1073/pnas.97.9.4469 10781046.

110. Kainz F, Ewen-Campen B, Akam M, Extavour CG. Notch/Delta signalling is not required for segment generation in the basally branching insect Gryllus bimaculatus. Development 2011; 138: 5015–5026. https://doi.org/10.1242/dev.073395 22028033

111. Janssen R, Budd GE Gene expression analysis reveals that Delta/Notch signalling is not involved in onychophoran segmentation. Dev Genes Evol 2016; 226: 69–77 doi: 10.1007/s00427-016-0529-4 26935716

112. Fritzenwanker JH, Uhlinger KR, Gerhart J, Silva E, Lowe CJ. Untangling posterior growth and segmentation by analyzing mechanisms of axis elongation in hemichordates. Proc Natl Acad Sci U S A. 2019;116: 8403–8408. doi: 10.1073/pnas.1817496116 30967509

113. Balavoine G. Are platyhelminthes coelomates without a coelom? An argument based on the evolution of Hox genes. Amer. Zool. 1998; 38: 843–858. https://doi.org/10.1093/icb/38.6.843

114. Cavalier-Smith T. Origin of animal multicellularity: precursors, causes, consequences—the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion. Phil. Trans. R. Soc. B 2017; 372: 20150476. https://doi.org/10.1098/rstb.2015.0476 27994119

115. Budd GE, Jensen S. The origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution. Biol Rev. 2017; 92: 446–473. doi: 10.1111/brv.12239 26588818

116. Marlétaz F, Peijnenburg KT, Goto T, Satoh N, Rokhsar DS. A new spiralian phylogeny places the enigmatic arrow worms among Gnathiferans. Curr Biol. 2019; 29: 312–318. https://doi.org/10.1016/j.cub.2018.11.042 30639106

117. Laumer CE, Fernández R, Lemer S, Combosch D, Kocot KM, Riesgo A et al. Revisiting metazoan phylogeny with genomic sampling of all phyla. Proc Biol Sci. 2019; 286: 20190831. https://doi.org/10.1098/rspb.2019.0831 31288696

118. Kristensen RM. Darwin’s dilemma dissolved. Nat Ecol Evol. 2017; 1: 0076. https://doi.org/10.1038/s41559-017-0076 28812717


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