Enigmatic macrofossils of late Ediacaran age (580–541 million years ago) provide the oldest known record of diverse complex organisms on Earth, lying between the microbially dominated ecosystems of the Proterozoic and the Cambrian emergence of the modern biosphere1. Among the oldest and most enigmatic of these macrofossils are the Rangeomorpha, a group characterized by modular, self-similar branching and a sessile benthic habit2,3,4. Localized occurrences of large in situ fossilized rangeomorph populations allow fundamental aspects of their biology to be resolved using spatial point process techniques5. Here we use such techniques to identify recurrent clustering patterns in the rangeomorph Fractofusus, revealing a complex life history of multigenerational, stolon-like asexual reproduction, interspersed with dispersal by waterborne propagules. Ecologically, such a habit would have allowed both for the rapid colonization of a localized area and for transport to new, previously uncolonized areas. The capacity of Fractofusus to derive adult morphology by two distinct reproductive modes documents the sophistication of its underlying developmental biology.
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Liu, A. G, Kenchington C. G. & Mitchell, E. G. Remarkable insights into the paleoecology of the Avalonian Ediacaran biota. Gondwana Res. 27, 1355–1380 (2015)
Gehling, J. G. & Narbonne, G. M. Spindle-shaped Ediacara fossils from the Mistaken Point assemblage, Avalon Zone, Newfoundland. Can. J. Earth Sci. 44, 367–387 (2007)
Narbonne, G. M. Modular construction of early Ediacaran complex life forms. Science 305, 1141–1144 (2004)
Hoyal Cuthill, J. F. & Conway Morris, S. Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic body plan. Proc. Natl Acad. Sci. USA 111, 13122–13126 (2014)
Illian, J., Penttinen, A., Stoyan, H. & Stoyan, D. Statistical Analysis and Modelling of Spatial Point Patterns Vol. 70 (John Wiley, 2008)
Wood, D. A., Dalrymple, R. W., Narbonne, G. M., Gehling, J. G. & Clapham, M. E. Paleoenvironmental analysis of the late Neoproterozoic Mistaken Point and Trepassey formations, southeastern Newfoundland. Can. J. Earth Sci. 40, 1375–1391 (2003)
Darroch, S. A. F., Laflamme, M. & Clapham, M. E. Population structure of the oldest known macroscopic communities from Mistaken Point, Newfoundland. Paleobiology 39, 591–608 (2013)
Wiegand, T., Gunatilleke, S., Gunatilleke, N. & Okuda, T. Analyzing the spatial structure of a Sri Lankan tree species with multiple scales of clustering. Ecology 88, 3088–3102 (2007)
Landing, E., Narbonne, G. M., Myrow, P., eds. Trace fossils, small shelly fossils and the Precambrian–Cambrian boundary. Bull. NY State Mus. 463, 1–81 (1988)
Clapham, M. E., Narbonne, G. M. & Gehling, J. G. Paleoecology of the oldest known animal communities: Ediacaran assemblages at Mistaken Point, Newfoundland. Paleobiology 29, 527–544 (2003)
Hofmann, H. J., O’Brien, S. J. & King, A. F. Ediacaran biota on Bonavista Peninsula, Newfoundland. Can. J. Paleontol. 82, 1–36 (2008)
Benus, A. P. Sedimentological context of a deep-water Ediacaran fauna (Mistaken Point Formation, Avalon zone, eastern Newfoundland). Bull. NY State Mus. 463, 8–9 (1988)
Narbonne, G. M., Laflamme, M., Trusler, P. W., Dalrymple, R. W. & Greentree, C. Deep-water Ediacaran fossils from northwestern Canada: Taphonomy, ecology, and evolution. J. Paleontol. 88, 207–223 (2014)
Brasier, M. D., Antcliffe, J. B. & Liu, A. G. The architecture of Ediacaran fronds. Palaeontology 55, 1105–1124 (2012)
Diggle, P. Statistical Analysis of Spatial Point Patterns 2nd edn (Arnold, 2003)
Baddeley, A. & Turner, R. Practical maximum pseudolikelihood for spatial point patterns. Aust. NZ J. Stat. 42, 283–322 (2000)
Chiu, S. N., Stoyan, D., Kendall, W. S. & Mecke, J. Stochastic Geometry and its Applications 3rd edn (John Wiley, 2013)
Lin, Y., Chang, L., Yang, K., Wang, H. & Sun, I. Point patterns of tree distribution determined by habitat heterogeneity and dispersal limitation. Oecologia 165, 175–184 (2011)
Droser, M. L. & Gehling, J. G. Synchronous aggregate growth in an abundant new Ediacaran tubular organism. Science 319, 1660–1662 (2008)
Gaylord, B., Reed, D. C., Raimondi, P. T. & Washburn, L. Macroalgal spore dispersal in coastal environments: mechanistic insights revealed by theory and experiment. Ecol. Monogr. 76, 481–502 (2006)
Shanks, A. L. Pelagic larval duration and dispersal distance revisited. Biol. Bull. 216, 373–385 (2009)
Gaylord, B., Reed, D., Raimondi, P., Washburn, L. & McLean, S. A physically based model of macroalgal spore dispersal in the wave and current-dominated nearshore. Ecology 83, 1239–1251 (2002)
Araki, K., Shimatani, K. & Ohara, M. Dynamics of distribution and performance of ramets constructing genets: a demographic–genetic study in a clonal plant, Convallaria keiskei. Ann. Bot. (Lond.) 104, 71–79 (2009)
Narbonne, G. M. & Gehling, J. G. Life after snowball: the oldest complex Ediacaran fossils. Geology 31, 27–30 (2003)
Peterson, K. J., Waggoner, B. & Hagadorn, J. W. A fungal analog for Newfoundland Ediacaran fossils? Integr. Comp. Biol. 43, 127–136 (2003)
Fedonkin, M. A. in Vendskaya Sistema 1, istoriko-geologicheskoe i paleontologicheskoe obosnovanie paleontologiya Vol. 1 (eds Sokolov, B. S. & Ivanovskiy, A. B. ) 70–106 (Nauka, 1985)
Penny, A. M. et al. Ediacaran metazoan reefs from the Nama Group, Namibia. Science 344, 1504–1506 (2014)
Yuan, X. et al. The Lantian biota: a new window onto the origin and early evolution of multicellular organisms. Chin. Sci. Bull. 58, 701–707 (2013)
Hua, H., Chen, Z., Yuan, X., Zhang, L. & Xiao, S. Skeletogenesis and asexual reproduction in the earliest biomineralizing animal Cloudina. Geology 33, 277–280 (2005)
Chen, L., Xiao, S., Pang, K., Zhou, C. & Yuan, X. Cell differentiation and germ–soma separation in Ediacaran animal embryo-like fossils. Nature 516, 238–241 (2014)
Clapham, M. E. in Quantifying the Evolution of Early Life (eds Laflamme, M., Schiffbauer, J. D. & Dornbos, S. Q. ) 3–21 (Springer, 2011)
Shen, B., Dong, L., Xiao, S. & Kowalewski, M. The Avalon explosion: evolution of Ediacara morphospace. Science 319, 81–84 (2008)
Liu, A. G., McIlroy, D., Antcliffe, J. B. & Brasier, M. D. Effaced preservation in the Ediacara biota and its implications for the early macrofossil record. Palaeontology 54, 607–630 (2011)
Narbonne, G. M., Laflamme, M., Greentree, C. & Trusler, P. Reconstructing a lost world: Ediacaran rangeomorphs from Spaniard’s Bay, Newfoundland. J. Paleontol. 83, 503–523 (2009)
Brasier, M. D. & Antcliffe, J. B. Evolutionary relationships within the Avalonian Ediacara biota: new insights from laser analysis. J. Geol. Soc. Lond. 166, 363–384 (2009)
R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2013)
Baddeley, A. & Turner, R. Spatstat: an R package for analyzing spatial point patterns. J. Stat. Softw. 12, 1–42 (2005)
Berman, M. Testing for spatial association between a point process and another stochastic process. Appl. Stat. 35, 54–62 (1986)
Baddeley, A., Rubak, E. & Møller, J. Score, pseudo-score and residual diagnostics for spatial point process models. Stat. Sci. 26, 613–646 (2011)
Wiegand, T. & Moloney, K. Rings, circles, and null-models for point pattern analysis in ecology. Oikos 104, 209–229 (2004)
Wiegand, T., Kissling, W., Cipriotti, P. & Aguiar, M. Extending point pattern analysis for objects of finite size and irregular shape. J. Ecol. 94, 825–837 (2006)
Wiegand, T., Moloney, K., Naves, J. & Knauer, F. Finding the missing link between landscape structure and population dynamics: a spatially explicit perspective. Am. Nat. 154, 605–627 (1999)
Loosmore, N. B. & Ford, E. D. Statistical inference using the G or K point pattern spatial statistics. Ecology 87, 1925–1931 (2006)
Wiegand, T. & Moloney, K. A. Handbook of Spatial Point-Pattern Analysis in Ecology (CRC, 2013)
Levin, S. A. in Ecological Time Series Vol. 2 (eds Powell, T. M. & Steele, J. H. ) 277–326 (Springer, 1995)
McIntire, E. J. & Fajardo, A. Beyond description: the active and effective way to infer processes from spatial patterns. Ecology 90, 46–56 (2009)
Fragoso, J. M., Silvius, K. M. & Correa, J. A. Long-distance seed dispersal by tapirs increases seed survival and aggregates tropical trees. Ecology 84, 1998–2006 (2003)
Russo, S. E. & Augspurger, C. K. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol. Lett. 7, 1058–1067 (2004)
Besag, J. Spatial interaction and the statistical analysis of lattice systems. J. R. Stat. Soc. B 36, 192–236 (1974)
Thomas, M. A generalization of Poisson’s binomial limit for use in ecology. Biometrika 36, 18–25 (1949)
Grabarnik, P., Myllymäki, M. & Stoyan, D. Correct testing of mark independence for marked point patterns. Ecol. Model. 222, 3888–3894 (2011)
Fraley, C. & Raftery, A. E. MCLUST version 3: an R package for normal mixture modeling and model-based clustering (Department of Statistics, Washington University, 2006)
Fraley, C. & Raftery, A. E. Bayesian regularization for normal mixture estimation and model-based clustering. J. Classific. 24, 155–188 (2007)
Pélissier, R. & Goreaud, F. A practical approach to the study of spatial structure in simple cases of heterogeneous vegetation. J. Veg. Sci. 12, 99–108 (2001)
Stoyan, D., Kendall, W. S. & Mecke, J. Stochastic Geometry and its Applications 2nd edn (Springer, 1995)
The Parks and Natural Areas Division, Department of Environment and Conservation, Government of Newfoundland and Labrador, provided permits to conduct research within the Mistaken Point Ecological Reserve in 2010, while the Department of Tourism, Culture and Recreation provided permits for palaeontological research on the Bonavista Peninsula in 2012. Access to both of the aforementioned fossil localities is by scientific research permit only. Contact the relevant Department listed above for further information. This work has been supported by the Natural Environment Research Council (grant numbers NE/I005927/1 to C.G.K., NE/J5000045/1 to J.J.M., NE/L011409/1 to A.G.L. and NE/G523539/1 to E.G.M.), and a Henslow Junior Research Fellowship from the Cambridge Philosophical Society to A.G.L. We thank M. Laflamme for discussions on this manuscript.
The authors declare no competing financial interests.
Extended data figures and tables
Extended Data Figure 1 Map and simplified stratigraphic column showing the position of studied bedding planes with bedding plane maps of Fractofusus.
a, Newfoundland, eastern Canada. Dashed area indicates region of interest in b. b, The Avalon and Bonavista Peninsulas, eastern Newfoundland. Locations of the bedding planes are indicated. c, Stratigraphic column (not to scale) compiled of information from the Avalon and Bonavista Peninsulas; lithological units in each region are treated as correlative in this study, but work is continuing to determine the validity of this assumption. The ‘E’ surface at Mistaken Point has been dated to 565 ± 3 Ma (ref. 12). There are currently no available radiometric dates from the Bonavista Peninsula. d–f, Maps of Fractofusus positions on the ‘D’ surface (d), the ‘E’ surface (e) and the H14 surface (f). In e the largest specimens are in light blue, medium specimens in mid-blue and smallest specimens in dark blue.
a, b, Plots of the lengths versus widths of discs from the ‘D’ surface, Mistaken Point (a), and the ‘E’ surface, Mistaken Point (b). The gradient of the line defines the retrodeformation factor, which for the ‘D’ surface is 1.35 ± 0.11 (R2 = 0.92) and for the ‘E’ surface is 1.71 ± 0.08 (R2 = 0.75). c, Fractofusus PCF on the ‘E’ surface with (solid line) and without (dashed line) retrodeformation. The grey shaded area depicts the boundary of 99 Monte Carlo simulations for the model which provided the best-fit model to the retrodeformed data, which has a good fit on the non-retrodeformed data (pd = 0.60).
a, Size–frequency distributions for Fractofusus, (n = 1,214); b, the results of the Bayesian information criterion52,53 (univariate data). Squares and triangles correspond to models assuming equal and unequal variance, respectively. High values of the Bayesian information criterion correspond to a good model fit, so the best-fit model is a three-component equal variance model using log-normalized length data. c–e, Rose diagrams plotting the directional orientation of the different size-classes of Fractofusus on the H14 surface showing large size-class (<11.0 cm, n = 350) (c), intermediate size-class (5.5–11.0 cm, n = 310) (d) and small size-class (<5.5 cm, n = 554) (e). The angles of the Fractofusus central axis are relative to north (0°). There is no strong orientation preference for any of the size-classes.
For all plots, the x axis is the inter-point distance between organisms (in metres). a, Mark correlation function5, where 1 corresponds to a lack of correlation of size, such that Fractofusus size is independent and identically distributed. A value of <1 corresponds to a positive dependency (in contrast to PCF) and >1 corresponds to a negative dependency. Small Fractofusus on the H14 surface (<0.3 cm) are more likely to be found near each other than expected by random. b, The ‘E’ surface PCF (solid line) showing the model that fits the data best, a double Thomas cluster model (dotted line, pd = 0.56), and the simulation envelope for 99 Monte Carlo simulations (grey shaded area). c, d, PCF for the best-fit models for the bivariate size-classes of Fractofusus on the H14 surface showing LCMs for small with medium size-classes (pd = 0.74) (c) and LCMs for medium with large size-classes (pd = 0.66) (d). e, The PCF of the largest size-class of H14 (solid line), showing the CSR Monte Carlo simulation envelope in grey, with the ‘D’ surface PCF (dotted line, pd = 0.56). f, Nearest neighbour distances (solid line, pd = 0.01) with CSR Monte Carlo simulation envelope in grey.
Extended Data Figure 5 Artistic reconstruction of Fractofusus on the H14 surface, Bonavista Peninsula.
The bottom right features a large Fractofusus around which there are five to eight medium specimens clustered. Each of the medium specimens also has small specimens clustered around them. The small specimens therefore form an independent double cluster pattern, namely clusters of clusters. Artwork by C.G.K.
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Mitchell, E., Kenchington, C., Liu, A. et al. Reconstructing the reproductive mode of an Ediacaran macro-organism. Nature 524, 343–346 (2015). https://doi.org/10.1038/nature14646
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