Skip to main content
SpringerLink
Log in

The oldest known larva and its implications for the plesiomorphy of metazoan development

已知最古老的幼虫以及它们对后生动物发育祖征的启示

  • Article
  • Earth Sciences
  • Published:
Science Bulletin

Abstract

There has been a century-long debate in evolutionary developmental biology about whether the ancestral metazoan was a larva or an adult. Two competing hypotheses have been proposed: the “terminal addition” theory, which assumes the primitiveness of larvae, and the “intercalation” theory, which assumes the primitiveness of adults. A consensus has not yet been reached, but the “terminal addition” theory appears to be more widely accepted. However, in contrast to the majority of larvae among living metazoans, all currently known fossil invertebrate embryos such as Markuelia and Olivooides are direct developers. Here, we describe Eolarva kuanchuanpuensis gen. et sp. nov., the oldest known larva, from the early Cambrian (~535 Ma) of South China. Eolarva kuanchuanpuensis lacks a mouth or any other type of feeding apparatus, which is non-feeding or lecithotrophic. It possesses a distinct body plan and might represent a cnidarian-grade animal. This is the first fossil evidence indicating that indirect development is the plesiomorphy of metazoan development.

摘要

绝大多数现生海洋无脊椎动物的个体发育都有幼虫阶段,因而,生物学家认为间接发育是后生动物发育的原始特征。然而,由于已知的化石胚胎都是直接发育的,古生物学家认为直接发育才是后生动物发育的原始特征。本文报道了距今5.35亿年的化石幼虫——宽川铺始祖幼虫。此幼虫缺乏摄食器官,是不摄食或蛋黄营养型的。它展示了独特的体构,可能代表刺胞级的动物。据此,本文首次提供了间接发育是后生动物发育原始特征的化石证据。

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Haeckel E (1874) Die Gastrea-Theorie, die phylogenetische clasification des thierreichs und die homologie der keimblatter. Jena Z Naturw 8:1–55

    Google Scholar 

  2. Jägersten G (1972) The Evolution of Metazoan Life Cycle. Academic Press, London

    Google Scholar 

  3. Nielsen C (2013) Life cycle evolution: Was the eumetazoan ancestor a holopelagic, planktotrophic gastraea? BMC Evol Biol 13:171

    Article  Google Scholar 

  4. Peterson KJ (2005) Macroevolutionary interplay between planktic larvae and benthic predators. Geology 33:929–932

    Article  Google Scholar 

  5. Dong X-P, Bengtson S, Gostling NJ et al (2010) The anatomy, taphonomy, taxonomy and systematic affinity of Markuelia: Early Cambrian to Early Ordovician scalidophorans. Palaeontology 53:1291–1314

    Article  Google Scholar 

  6. Bengtson S, Yue Z (1997) Fossilized metazoan embryos from the earliest Cambrian. Science 277:1645–1648

    Article  Google Scholar 

  7. Conway Morris S (1998) Eggs and embryos from the Cambrian. BioEssays 20:676–682

    Article  Google Scholar 

  8. Chen F, Dong X-P (2008) The internal structure of early Cambrian fossil embryo Olivooides revealed in the light of Synchrotron X-ray tomographic microscopy. Chin Sci Bull 53:3860–3865

    Article  Google Scholar 

  9. Steiner M, Li G, Qian Y et al (2004) Lower Cambrian small shelly fossils of northern Sichuan and southern Shaanxi (China), and their biostratigraphic importance. Geobios 37:259–275

    Article  Google Scholar 

  10. Peng S, Babcock LE, Cooper RA (2012) The Cambrian Period. In: Gradstein FM, Ogg JG, Schmitz M et al (eds) Geological Time Scale 2012. Elsevier, Oxford, pp 437–488

    Chapter  Google Scholar 

  11. Steiner M, Qian Y, Li G et al (2014) The developmental cycles of early Cambrian Olivooidae fam. nov. (?Cycloneuralia) from the Yangtze Platform (China). Palaeogeogr Palaeoclimatol Palaeoecol 398:97–124

    Article  Google Scholar 

  12. Ou Q, Xiao S, Han J et al (2015) A vanished history of skeletonization in Cambrian comb jellies. Sci Adv. doi:10.1126/sciadv.1500092

    Google Scholar 

  13. Müller KJ, Hinz-Schallreuter I (1993) Palaeoscolecid worms from the Middle Cambrian of Australia. Palaeontology 36:549–592

    Google Scholar 

  14. Harvey THP, Dong X-P, Donoghue PCJ (2010) Are palaeoscolecids ancestral ecdysozoans? Evol Dev 12:177–200

    Article  Google Scholar 

  15. Duan B, Dong X-P, Donoghue PCJ (2012) New palaeoscolecid worms from the Furongian (upper Cambrian) of Hunan, South China: Is Markuelia an embryonic palaeoscolecid? Palaeontology 55:613–622

    Article  Google Scholar 

  16. Dong X-P, Cunningham JA, Bengtson S et al (2013) Embryos, polyps and medusae of the early Cambrian scyphozoan Olivooides. Proc R Soc B (Biol Sci). doi:10.1098/rspb.2013.0071

    Google Scholar 

  17. Liu Y, Li Y, Shao T et al (2014) Quadrapyrgites from the lower Cambrian of South China: growth pattern, post-embryonic development, and affinity. Chin Sci Bull 59:4086–4095

    Article  Google Scholar 

  18. Li P, Hua H, Zhang L et al (2007) Lower Cambrian phosphatized Punctatus from southern Shaanxi and their ontogeny sequence. Chin Sci Bull 52:2820–2828

    Article  Google Scholar 

  19. Shao T, Liu Y, Wang Q et al (2015) New material of the oldest known scalidophoran animal Eopriapulites sphinx. Palaeoworld. doi:10.1016/j.palwor.2015.1007.1003

    Google Scholar 

  20. Raff RA (2008) Origins of the other metazoan body plans: The evolution of larval forms. Phil Trans R Soc B 363:1473–1479

    Article  Google Scholar 

  21. Nielsen C (2012) Animal evolution: Interrelationships of the living phyla. Oxford University Press, Oxford

    Google Scholar 

  22. Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev Camb Philos Soc 25:1–45

    Article  Google Scholar 

  23. Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: Evolution of developmental regulatory mechanisms. Science 270:1319–1325

    Article  Google Scholar 

  24. Peterson KJ, Cameron RA, Davidson EH (1997) Set-aside cells in maximal indirect development: Evolutionary and developmental significance. BioEssays 19:623–631

    Article  Google Scholar 

  25. Blackstone NW, Ellison AM (2000) Maximal indirect development, set-aside cells, and levels of selection. J Exp Zool 288:99–104

    Article  Google Scholar 

  26. Nielsen C (2008) Six major steps in animal evolution: Are we derived sponge larvae? Evol Dev 10:241–257

    Article  Google Scholar 

  27. Nielsen C (2015) Larval nervous systems: True larval and precocious adult. J Exp Biol 218:629–636

    Article  Google Scholar 

  28. Brusca RC, Brusca GJ (2003) Invertebrates. Sinauer Associates, Inc. Publishers, Sunderland

    Google Scholar 

  29. Nielsen C (1985) Animal phylogeny in the light of the trochaea theory. Biol J Linn Soc 25:243–299

    Article  Google Scholar 

  30. Strathmann RR, Jahn TL, Fonseca JC (1972) Suspension feeding by marine invertebrate larvae: Clearance of particles by ciliated bands of a rotifer, pluteus, and trochophore. Biol Bull 142:505–519

    Article  Google Scholar 

  31. Wolpert L (1999) From egg to adult to larva. Evol Dev 1:3–4

    Article  Google Scholar 

  32. Nielsen C, Nørrevang A (1985) The trochaea theory: An example of life cycle phylogeny. In: Conway Morris S, George JD, Gibson R et al (eds) The origins and relationships of lower invertebrates—(The Systematics Association, special volume No 28). Oxford University Press, Oxford, pp 28–41

    Google Scholar 

  33. Sly BJ, Snoke MS, Raff RA (2003) Who came first—Larvae or adults? Origins of bilaterian metazoan larvae. Int J Dev Biol 47:623–632

    Google Scholar 

  34. Valentine JW, Collins AG (2000) The significance of moulting in Ecdysozoan evolution. Evol Dev 2:152–156

    Article  Google Scholar 

  35. Degnan SM, Degnan BM (2006) The origin of the pelagobenthic metazoan life cycle: What’s sex got to do with it? Integr Comp Biol 46:683–690

    Article  Google Scholar 

  36. Minelli A (2009) Perspectives in Animal Phylogeny & Evolution. Oxford University Press Inc., New York

    Google Scholar 

  37. Maas A, Waloszek D, Haug JT et al (2009) Loricate larvae (Scalidophora) from the Middle Cambrian of Australia. Mem Assoc Aust Palaeontol 37:281–302

    Google Scholar 

  38. Maas A, Waloszek D, Haug JT et al (2007) A possible larval roundworm from the Cambrian “Orsten” and its bearing on the phylogeny of Cycloneuralia. Mem Assoc Aust Palaeontol 34:499–519

    Google Scholar 

  39. Wills MA, Gerber S, Ruta M et al (2012) The disparity of priapulid, archaeopriapulid and palaeoscolecid worms in the light of new data. J Evol Biol 25:2056–2076

    Article  Google Scholar 

  40. Han J, Kubota S, Li G et al (2015) Divergent evolution of medusozoan symmetric patterns: Evidence from the microanatomy of Cambrian tetramerous cubozoans from South China. Gondwana Res. doi:10.1016/j.gr.2015.1001.1003

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (41372015, 41102003, J1210006), the State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (103102, 20132107), and the Research Fund for the Doctoral Program of High Education (20060001059). We thank Shuhai Xiao for discussion and suggestions, Dinghua Yang for technical help, and two anonymous reviewers for their constructive comments.

Author information

Authors and Affiliations

  1. Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences (Nanjing Institute of Geology and Palaeontology), Nanjing, 210008, China

    Huaqiao Zhang

  2. School of Earth and Space Sciences, Peking University, Beijing, 100871, China

    Xi-Ping Dong

Authors
  1. Huaqiao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xi-Ping Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xi-Ping Dong.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Dong, XP. The oldest known larva and its implications for the plesiomorphy of metazoan development. Sci. Bull. 60, 1947–1953 (2015). https://doi.org/10.1007/s11434-015-0886-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11434-015-0886-9

Keywords

关键词

Search

Navigation