DIVERSE AND COMPLEX DEVELOPMENTAL MECHANISMS OF EARLY EDIACARAN EMBRYO-LIKE FOSSILS FROM THE WENG’AN BIOTA, SOUTHWEST CHINA

1. Diverse and complex developmental mechanisms of early
Ediacaran embryo-like fossils from the Weng’an biota,
Southwest China
ZJ. Yin1,2* , W.C. Sun1,2,3, P.J. Liu4, J.Y. Chen1, D.J. Bottjer5, J.H. Li6, M.Y.Zhu1,2
1 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of
Sciences, Nanjing 210008, China;
2 Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China;
3 University of Science and Technology of China, Hefei 230026, China;
4 Institute of Geology, Chinese Academy of Geological Sciences, Beijing 100037, China;
5 Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089, USA;
6 Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Innovation Academy for Earth Science,
Chinese Academy of Sciences, Beijing 100029, China;
7 College of Earth Sciences, University of Chinese Academy of Sciences, Beijing 100049, China.
*E-mail: zjyin@nigpas.ac.cn

2. 2
Weng’an biota: an important taphonomic window (~609 Ma)
Phosphatized microfossil assemblage from the Ediacaran Doushantuo Formation, Southwest China

3. 3
Animal Tree
Why Weng’an biota?
Cunningham et al., 2017
Weng’an biota

4. Embryo-like fossils: Ediacaran developmental biology

5. 1
Metazoan
embryos
Xiao et al., 1998, Nature
Chen et al., 2006, Science
Yin L et al., 2007, Nature
Chen et al., 2009, PNAS
Yin Z et al., 2016, Geology
2
Stem-group
metazaons
Hagadorn et al., 2006, Science
Chen L et al., 2014，Nature
4
Giant sulfur
bacteria
Bailey et al., 2007, Nature
5
Multicellular
algae
Butterfield, 2011, Science
Chen L et al., 2014, Nature
3
Non-metazoan
holozoans
Huldtgren et al., 2011, Science
Embryo-like fossils: Ediacaran developmental biology

6. 6
1 2
Huldtgren et al., 2011
Simply constructed with few
phylogenetic signals
Affinities of embryo-like fossils: under debate
Difficult to reconstruct their life
cycles
Huldtgren et al., 2011

7. 7
Affinities of embryo-like fossils: under debate
Megasphaera
Helicoforamina
Spiralicellula
Caveasphaera
Tianshushania
…..
Different developmental stages of the same organism VS different organisms

8. 8
Cell division patterns: proxy of diversity
Diverse cleavage patterns of living animal embryos
Radial cleavage
Spiral cleavage
Bilateral cleavage
Rotational cleavage
Discodial cleavage
Superficial cleavage
…
Gilbert, 2009

9. 9
Cleavage pattern (1): synchronous & equal cell division
The spatial arrangements of the
cells are stable, predicable, and
similar to that of spiral cleavage…
L-Q: development process of living Spongilla lacustris (demosponge) (after Saller and Weissenfels, 1985)

10. 10
A-D：a 7-celled specimen
• Cell 7 is twice larger than the
others
• Tow nuclei in the large cell-7
• One nucleus in each small cell
Cleavage pattern (2): asynchronous & equal cell division

11. 11
E-L：Specimens with bilateral
arrangement of cells
• 7-celled specimens
• Large, middle and small cells
Yin et al., unpublished
Cleavage pattern (3): asynchronous & unequal cell division

12. 12
A-S: Weng’an embryo-like fossils
• Cell number=1, 2, 3, 4, 5…
• Always has a large cell on one pole
• Small cell form a cap covering the
large cell
• The size of the large cell decreased
from early to late stages
T1-T8: Early cleavage process of
Asplanchna ebbesbornii (Rotifer) (after
Tannreuther, 1920)
Cleavage pattern (4): asynchronous & unequal cell division
Yin et al., unpublished

13. 13
Cleavage pattern (4): asynchronous & unequal cell division
A-D: fossils; E-G: extant rotifer embryos

14. 14
Cleavage pattern (4): asynchronous & unequal cell division

15. 15
Cleavage pattern (5): putative discodial cell division
Yin et al., 2016, Geology

16. 16
Yolk Cell
Cell-1
Cell-2
Cell-3
Cell-4
Cell-5
Cell-6
Cell-7
Cell-8
Cell-9
Cell-10
Cell-11
Cell-12
IN Spaces
62.3%
Epiboly gastrulation of frogs
Weng’an embryo-like fossils
Cell volume
Internal structures
Possible gastrulation stages?
Cleavage pattern (5): putative discoidal cell division
Yin et al., 2016, Geology

17. Polar lobe formation in extant marine snail
Early development of living marine clam
A living mollusc embryo (clam)
Early development of embryo-like fossils with PL
(pl=polar lobe,)
Weng’an embryo-like fossils
Cleavage pattern (6): putative polar lobe formation
Chen et al., 2006, Science; Yin et al., 2013, Precambrian Research

18. Cleavage patterns: phylogenetic implications?
Protists: ichthyosporeans
Gilbert, 2009; Marshall & Berbee, 2011, 2013; Mendoza et al., 2002

19. Cleavage patterns: phylogenetic implications?
Sebé-Pedrós et al., 2017, Nature Genetics Review
• Some embryo-like fossil could be non-
metazoan holozoans, but they are not
necessarily to be protits.
• Temporal cell differentiation to spatial cell
differentiation

20. 20
Later developmental stages of spherical Megasphaera, undergoing germination or propagule release
Huldtgren et al., 2011, Science
Elongate embryo-like fossils: germination & propagule release?

21. 21
Huldtgren et al., 2011, Science
Elongate embryo-like fossils: germination & propagule release?
Yin et al., unpublished

22. 22
Elongate embryo-like fossils: cleavage stages
Yin et al., unpublished

23. 23
Elongate embryo-like fossils: cleavage stages
Yin et al., unpublished

24. 24

25. 25
Elongate embryo-like fossils: late stages
Yin et al., unpublished

26. 26
Elongate embryo-like fossils: stem-group metazoans?
1. They developed inside multi-layered, thick envelops
2. They are not late stages of spherical Megasphaera
3. They likely developed from single cell to very late stages with cellular differentiation
and cell cluster separation via palintomic cleavage
4. Life cycle is still not complete

27. Cleavage patterns: phylogenetic implications?
Sebé-Pedrós et al., 2017, Nature Genetics Review
• Temporal cell differentiation to spatial cell
differentiation
• Some embryo-like fossil could be non-
metazoan holozoans, but they are not
necessarily to be protits.

28. 28
1. Some embryo-like fossils could be animal’s protistan relatives
2. Some embryo-like fossils are likely stem-group animals
3. Cleavage patterns and developmental process suggest that the diversity of the Weng’an
embryo-like fossils are higher than previous thought
4. More fossil evidence needed to constrain their phylogenetic affinities
Tentative conclusions

29. 29
Acknowledgements
May, 2011, Eric’s office, Caltech

30. 30
Field work in Weng’an, Guizhou, Southwest China,
September, 2016

31. Acknowledgements
Funding:
Chinese Academy of Sciences
Natural Science Foundation of China
Royal Society Newton Advanced Fellowship
Philip C.J. Donoghue (Bristol University)
John Cunningham (Bristol University)
Douglas Erwin (Smithsonian National Museum of Natural History)
Shuhai Xiao (Virginia Tech)
Eric Davidson (Caltech)
….