Towards an Integrated Triad: Taxonomy, Morphology and Phylogeny

  • Olav GiereEmail author
Part of the SpringerBriefs in Biology book series (BRIEFSBIOL)


In the early days of meiobenthology (this term did not even exist), researchers were confronted with a plethora of new taxa and novel structures, from species to phylum. Thus, they focussed on taxonomic descriptions and morphological studies. But today, can these traditional domains still offer something ‘new under the sun’? Looking at the amazingly fruitful recent literature, this question is easily answered. Computer analyses help to construct molecular genetic patterns, not only of some specimens, oftentimes of whole populations or even the entire bulk of meiofauna contained in sample sets.


  1. Abebe E, Decraemer W, Ley PD (2008) Global diversity of nematodes (Nematoda) in freshwater. Hydrobiologia 595:67–78Google Scholar
  2. Avó AP, Daniell TJ, Neilson R et al (2017) DNA barcoding and morphological identification of benthic nematodes assemblages of estuarine intertidal sediment: advances in molecular tools for biodiversity assessment. Front Mar Sci 4:66.
  3. Bali´nski A, Sun Y, Dzik J (2013) Traces of marine nematodes from 470 million years old early Ordovician rocks in China. Nematology 15:567–574Google Scholar
  4. Bartsch I (2009) Checklist of marine and freshwater halacarid mite genera and species (Halacaridae: Acari) with notes on synonyms, habitats, distribution and descriptions of the taxa. Zootaxa 1998:3–170Google Scholar
  5. Bekkouche N, Worsaae K (2016) Nervous system and ciliary structures of Micrognathozoa (Gnathifera): evolutionary insight from an early branch in Spiralia. R Soc Open Sci 3(10):160289CrossRefGoogle Scholar
  6. Bhadury PMC, Austen DT, Bilton PJD et al (2007) Exploitation of archived marine nematodes—a hot lysis DNA extraction protocol for molecular studies. Zool Scr 36:93–98CrossRefGoogle Scholar
  7. Bleidorn C (2017) Sources of error and incongruence in phylogenomic analyses. Phylogenomics—An introduction. Springer, Berlin, pp 173–193CrossRefGoogle Scholar
  8. Borner J, Rehm P, Schill RO et al (2014) A transcriptome approach to ecdysozoan phylogeny. Mol Phylogen Evol 80:79–87CrossRefGoogle Scholar
  9. Brannock PM, Halanych KM (2015) Meiofaunal community analysis by high-throughput sequencing: comparison of extraction, quality filtering, and clustering methods. Mar Genomics 23:67–75CrossRefGoogle Scholar
  10. Brannock PM, Learman DR, Mahon AR et al (2018) Meiobenthic community composition and biodiversity along a 5500 km transect of Western Antarctica: a metabarcoding analysis. Mar Ecol Prog Ser 603:47–60. Scholar
  11. Brenzinger B, Haszprunar G, Schrödl M (2013) 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 10:37.
  12. Cannon JT, Vellutini BC, Smith J et al (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530:89–93CrossRefGoogle Scholar
  13. Chen Z, Chen X, Chuanming Z et al (2018) Late Ediacaran trackways produced by bilaterian animals with paired appendages. Sci Adv 4:eaao6691Google Scholar
  14. Costello MJ (2015) Biodiversity: the known, unknown, and rates of extinction. Curr Biol 25(9):R368–R371. Scholar
  15. Creer S, Fonseca VG, Porazinska DL et al (2015) Ultrasequencing of the meiofaunal biosphere: practice, pitfalls and promises. Mol Ecol 19(Suppl. 1):4–20Google Scholar
  16. Cunningham JA, Liu AG, Bengtson S, Donoghue PCJ (2017) The origin of animals: can molecular clocks and the fossil record be reconciled? BioEssays 39:1600120. Scholar
  17. De Bruijn FJ (ed) (2011) Handbook of molecular microbial ecology II. Metagenomics in different habitats. Wiley-Blackwell, Wiley & Sons Inc, Hoboken, New Jersey, 610 ppGoogle Scholar
  18. Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2(11):e329. Scholar
  19. Derycke S, De Ley P, De Ley IT et al (2010) Linking DNA sequences to morphology: cryptic diversity and population genetic structure in the marine nematode Thoracostoma trachygaster (Nematoda, Leptosomatidae). Zool Scr 39:276–289CrossRefGoogle Scholar
  20. First MR, Hollibaugh JT (2010) Diel depth distributions of microbenthos in tidal creek sediments: high resolution mapping in fluorescently labeled embedded cores. Hydrobiologia 655:149–158CrossRefGoogle Scholar
  21. Fonseca VG, Carvalho GR, Sung W et al (2010) Second-generation environmental sequencing unmasks marine metazoan biodiversity. Nat Commun 1:98.
  22. Fonseca VG, Packer M, Carvalho GR et al (2011) Isolation of marine meiofauna from sandy sediments: from decanting to DNA extraction. Nat Protoc Exch.
  23. Fonseca VG, Sinniger F, Gaspar JM et al (2017) Revealing higher than expected meiofaunal diversity in Antarctic sediments: a metabarcoding approach. Sci Rep 7:6094. Scholar
  24. Fontaneto D, De Smet WH, Melone G (2007) Identification key to the genera of marine rotifers worldwide. Meiofauna Mar 16:75–99Google Scholar
  25. Fontaneto D, Flot J-F, Tang CQ (2015) Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar Biodivers 45:433–451CrossRefGoogle Scholar
  26. Galassi DMP, Huys R, Reid JW (2009) Diversity, ecology and evolution of groundwater copepods. Freshw Biol 54:691–708CrossRefGoogle Scholar
  27. Gąsiorowski L, Bekkouche N, Worsaae K (2017) Morphology and evolution of the nervous system in Gnathostomulida (Gnathifera, Spiralia). Org Divers Evol 17:447.
  28. Geiger M, Borsch J, Burkhardt U (2016) How to tackle the molecular species inventory for an industrialized nation—lessons from the first phase of the German Barcode of Life initiative (GBOL (2012–2015). Genome 59:1–10CrossRefGoogle Scholar
  29. Grosemans T, Morris K, Thomas WK et al (2016) Mitogenomics reveals high synteny and long evolutionary histories of sympatric cryptic nematode species. Ecol Evol 6:1854–1870. Scholar
  30. Han J, Conway Morris S, Ou Q et al (2017) Meiofaunal deuterostomes from the basal Cambria of Shaanxi (China). Nature 542:228–231CrossRefGoogle Scholar
  31. Harper LR, Buxton AS, Rees HC et al (2019) Prospects and challenges of environmental DNA (eDNA) monitoring in freshwater ponds. Hydrobiologia 826:25–41. Scholar
  32. Harvey THP, Butterfield NJ (2017) Exceptionally preserved Cambrian loriciferans and the early animal invasion of the meiobenthos. Nat Ecol Evol 1:0022.
  33. ISIMCO (2016) Draft book of abstracts. In: 16th international meiofauna conference, Heraklion, Greece, 3–8 July 2016, 182 ppGoogle Scholar
  34. Jiang H, Kilburn MR, Decelle J, Musat N (2016) NanoSIMS chemical imaging combined with correlative microscopy for biological sample analysis. Curr Opin Biotechnol 41:130–135CrossRefGoogle Scholar
  35. Karanovic T, Kim K (2014) New insights into polyphyly of the harpacticoid genus Delavalia (Crustacea, Copepoda) through morphological and molecular study of an unprecedented diversity of sympatric species in a small South Korean bay. Zootaxa 3783:1–96. Scholar
  36. Kerbl A, Martin-Durán JM, Worsaae K, Hejnol A (2016) Molecular regionalization in the compact brain of the meiofauna annelid Dinophilus gyrociliatus (Dinophilidae). EvoDevo 7:20CrossRefGoogle Scholar
  37. Kitahashi T, Watanabe HK, Tsuchiya M et al (2018) A new method for acquiring images of meiobenthic images using the FlowCAM. MethodsX 5:1330–1335. Scholar
  38. Laumer CE, Bekkouche N, Kerbl A et al (2015) Spiralian phylogeny informs the evolution of microscopic lineages. Curr Biol 25:2000–2006CrossRefGoogle Scholar
  39. Lindgren JF, Hassellöv I-M, Dahllöf I (2013) Analyzing changes in sediment meiofauna communities using the image analysis software ZooImage. J Exp Mar Biol Ecol 440:74–80CrossRefGoogle Scholar
  40. Maurin LC, Himmel D, Mansot JL et al (2010) Raman microspectrometry as a powerful tool for a quick screening of thiotrophy: an application on mangrove swamp meiofauna of Guadeloupe (FWI). Mar Environ Res 69:382–389CrossRefGoogle Scholar
  41. Mayer G, Martin C, Rüdiger J et al (2013) Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods. BMC Evol Biol 13:230.
  42. Neves R, Bailly X, Leasi F et al (2013) A complete three-dimensional reconstruction of the myoanatomy of Loricifera: comparative morphology of an adult and a Higgins larva stage. Front Zool 10:1–21CrossRefGoogle Scholar
  43. Park JK, Rho HS, Kristensen RM et al (2006) First molecular data on the phylum Loricifera—an investigation into the phylogeny of Ecdysozoa with emphasis on the positions of Loricifera and Priapulida. Zool Sci 23:943–954CrossRefGoogle Scholar
  44. Parry LA, Boggiani PC, Condon DJ et al (2017) Ichnological evidence for meiofaunal bilaterians from the terminal Ediacaran and earliest Cambrian of Brazil. Nature Ecol Evol 1:1455–1464.
  45. Pereira TJ, Fonseca G, Mundo-Ocampo M et al (2010) Diversity of free-living marine nematodes (Enoplida) from Baja California assessed by integrative taxonomy. Mar Biol 157:1665–1678.
  46. Perry ES, Miller WR, Lindsay S (2015) Looking at tardigrades in a new light: using epifluorescence to interpret structure. J Microsc 257(2):117–122CrossRefGoogle Scholar
  47. Purschke G, Jördens J (2007) Male genital organs in the eulittoral meiofaunal polychaete Stygocapitella subterranea (Annelida, Parergodrilidae): ultrastructure, functional and phylogenetic significance. Zoomorphology 126:283–297CrossRefGoogle Scholar
  48. Rossel S, Martinez Arbizu PM (2018a) Automatic specimen identification of harpacticoids (Crustacea: Copepoda) using random forest and MALDI-TOF mass spectra, including a post hoc test for false positive discovery. Methods Ecol Evol 2018:1–14. Scholar
  49. Rossel S, Martinez Arbizu PM (2018b) Effects of sample fixation on specimen identification in biodiversity assemblies based on proteomic data (MALDI-TOF). Front Mar Sci 5:149. Scholar
  50. Rota-Stabelli O, Daley AC, Pisani D (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for Ecdysozoan evolution. Curr Biol 23:392–398CrossRefGoogle Scholar
  51. Savic AG, Preus S, Rebecchi L, Guidetti R (2016) New multivariate image analysis method for detection of differences in chemical and structural composition of chitin structures in tardigrade feeding apparatuses. Zoomorphology 135:43–50CrossRefGoogle Scholar
  52. Siveter DJ, Tanaka G, Farrell UC et al (2014) Exceptionally preserved 450-million-year-old Ordovician ostracods with brood care. Curr Biol 24:801–806CrossRefGoogle Scholar
  53. Struck TH, Golombek A, Weigert A et al (2015) The evolution of annelids reveals two adaptive routes to the interstitial realm. Curr Biol 25:1933–1999CrossRefGoogle Scholar
  54. Tang CQ, Leasi F, Obertegger U et al (2012) The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. PNAS 109:16208–16212CrossRefGoogle Scholar
  55. Thomas JA, Welch JJ, Lanfear R, Bromham L (2010) A generation time effect on the rate of molecular evolution in invertebrates. Mol Biol Evol 27:1173–1180CrossRefGoogle Scholar
  56. Van Megen H, Van Den Elsen S, Holterman M et al (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–950CrossRefGoogle Scholar
  57. Wang Y, Huang WE, Cui L, Wagner M (2016) Single cell stable isotope probing in microbiology using Raman microspectroscopy. Curr Opin Biotechnol 41:34–42CrossRefGoogle Scholar
  58. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Phil Trans R Soc Lond B 314:1–340CrossRefGoogle Scholar
  59. Witek A, Herlyn H, Ebersberger I et al (2009) Support for the monophyletic origin of Gnathifera from phylogenomics. Mol Phylogen Evol 53:1037–1041CrossRefGoogle Scholar
  60. Worsaae K, Giribet G, Martínez A (2018) The role of progenesis in the diversification of the interstitial annelid lineage Psammodrilidae. Inv Sys 32:774Google Scholar
  61. Xu J, Wang Y-S, Yin J, Lin J (2011) New series of corers for taking undisturbed vertical samples of soft bottom sediments. Mar Environ Res 71:312–316CrossRefGoogle Scholar
  62. Yang J, Ortega-Hernández J, Butterfield NJ et al (2016) Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda. Proc Nat Acad Sci 113:2988–2993Google Scholar
  63. Zhang H, Xiao S (2017) Three-dimensionally phosphatized meiofaunal bivalved arthropods from the Upper Cambrian of Western Hunan, South China. Neues Jb Geol Paläont—Abhdl 285:39–52Google Scholar

Copyright information

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Universität Hamburg (Emeritus)HamburgGermany

Personalised recommendations