Early bursts of diversification defined the faunal colonization of land

Abstract

The colonization of land was one of the major events in Earth history, leading to the expansion of life and laying the foundations for the modern biosphere. We examined trace fossils, the record of the activities of past life, to understand how animals diversify both behaviourally and ecologically when colonizing new habitats. The faunal invasion of land was preceded by excursions of benthic animals into very shallow, marginal marine environments during the latest Ediacaran period and culminated in widespread colonization of non-marine niches by the end of the Carboniferous period. Trace fossil evidence for the colonization of new environments shows repeated early burst patterns of maximal ichnodisparity (the degree of difference among basic trace fossil architectural designs), ecospace occupation and level of ecosystem engineering prior to maximal ichnodiversity. Similarities across different environments in the types of behavioural programme employed (as represented by different trace fossils), modes of life present and the ways in which animals impacted their environments suggest constraints on behavioural and ecological diversification. The early burst patterns have the hallmark of novelty events. The underlying drivers of these events were probably the extrinsic limitation of available ecospace and intrinsic controls of genomic and developmental plasticity that enabled trace-maker morphological and behavioural novelty.

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Figure 1: Colonization of subaqueous coastal environments (estuaries and shallow subtidal flats) through the Ediacaran to Permian periods.
Figure 2: Colonization of transitional coastal environments (coastal plains and tidal flats) through the Ediacaran to Permian periods.
Figure 3: Colonization of transitional alluvial environments (floodplains and abandoned channels) through the Ediacaran to Permian periods.
Figure 4: Number of global ichnogenera per global architectural design occupying different tiers through time in different environments.

References

  1. 1

    Maynard Smith, J . & Szathmáry, E. The Major Transitions in Evolution (WH Freeman, 1995).

    Google Scholar 

  2. 2

    Battistuzzi, F. U., Feijao, A. & Hedges, S. B. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4, 44 (2004).

    PubMed  PubMed Central  Google Scholar 

  3. 3

    Davies, N. S., Liu, A. G., Gibling, M. R. & Miller, R. F. Resolving MISS conceptions and misconceptions: a geological approach to sedimentary surface textures generated by microbial and abiotic processes. Earth-Sci. Rev. 154, 210–246 (2016).

    Google Scholar 

  4. 4

    Horodyski, R. J. & Knauth, L. P. Life on land in the Precambrian. Science 263, 494–498 (1994).

    CAS  PubMed  Google Scholar 

  5. 5

    Strother, P. K., Battison, L., Brasier, M. D. & Wellman, C. H. Earth’s earliest non-marine eukaryotes. Nature 473, 505–509 (2011).

    CAS  PubMed  Google Scholar 

  6. 6

    Wellman, C. H. & Strother, P. K. The terrestrial biota prior to the origin of land plants (embryophytes): a review of the evidence. Palaeontology 58, 601–627 (2015).

    Google Scholar 

  7. 7

    Watanabe, Y., Martini, J. E. J. & Ohmoto, H. Geochemical evidence for terrestrial ecosystems 2.6 billion years ago. Nature 408, 574–578 (2000).

    CAS  PubMed  Google Scholar 

  8. 8

    Knauth, L. P. & Kennedy, M. J. The late Precambrian greening of the Earth. Nature 460, 728–732 (2009).

    CAS  PubMed  Google Scholar 

  9. 9

    Kennedy, M., Droser, M., Mayer, L. M., Pevear, D. & Mrofka, D. Late Precambrian oxygenation; inception of the clay mineral factory. Science 311, 1446–1449 (2006).

    CAS  PubMed  Google Scholar 

  10. 10

    McMahon, W. J., Davies, N. S. & Went, D. J. Negligible microbial matground influence on pre-vegetation river functioning: evidence from the Ediacaran–Lower Cambrian Series Rouge, France. Precambrian Res. 292, 13–34 (2017).

    CAS  Google Scholar 

  11. 11

    Horodyskyj, L. B., White, T. S. & Kump, L. R. Substantial biologically mediated phosphorus depletion from the surface of a Middle Cambrian paleosol. Geology 40, 503–506 (2012).

    CAS  Google Scholar 

  12. 12

    Rubinstein, C. V., Gerrienne, P., de la Puente, G. S., Astini, R. A. & Steemans, P. Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytol. 188, 365–369 (2010).

    CAS  PubMed  Google Scholar 

  13. 13

    Retallack, G. J. Ediacaran life on land. Nature 493, 89–92 (2013).

    PubMed  Google Scholar 

  14. 14

    Minter, N. J. et al. in The Trace-Fossil Record of Major Evolutionary Events Vol. 1 (eds Mángano, M. G. & Buatois, L. A. ) 157–204 (Springer, 2016).

    Google Scholar 

  15. 15

    Rota-Stabelli, O., Daley, A. C. & Pisani, D. Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr. Biol. 23, 392–398 (2013).

    CAS  PubMed  Google Scholar 

  16. 16

    Lozano-Fernandez, J. et al. A molecular palaeobiological exploration of arthropod terrestrialization. Phil. Trans. R. Soc. B 317, 20150133 (2016).

    Google Scholar 

  17. 17

    Fernández, R., Edgecombe, G. D. & Giribet, G. Exploring phylogenetic relationships within Myriapoda and the effects of matrix composition and occupancy on phylogenomic reconstruction. Syst. Biol. 65, 871–889 (2016).

    PubMed  PubMed Central  Google Scholar 

  18. 18

    Misof, B. et al. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767 (2014).

    CAS  PubMed  Google Scholar 

  19. 19

    Buatois, L. A. & Mángano, M. G. Ecospace utilization, paleoenvironmental trends, and the evolution of early nonmarine biotas. Geology 21, 595–598 (1993).

    Google Scholar 

  20. 20

    MacNaughton, R. B. et al. First steps on land: arthropod trackways in Cambrian–Ordovician eolian sandstone, southeastern Ontario, Canada. Geology 30, 391–394 (2002).

    Google Scholar 

  21. 21

    Miller, M. F. & Labandeira, C. C. Slow crawl across the salinity divide: delayed colonization of freshwater ecosystems by invertebrates. GSA Today 12, 4–10 (2002).

    Google Scholar 

  22. 22

    Braddy, S. J. Ichnological evidence for the arthropod invasion of land. Foss. Strat. 51, 136–140 (2004).

    Google Scholar 

  23. 23

    Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as ecosystem engineers. Oikos 69, 373–386 (1994).

    Google Scholar 

  24. 24

    Erwin, D. H. Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol. Evol. 23, 304–310 (2008).

    PubMed  Google Scholar 

  25. 25

    Foote, M. Discordance and concordance between morphological and taxonomic diversity. Paleobiology 19, 185–204 (1993).

    Google Scholar 

  26. 26

    Erwin, D. H. Disparity: morphological pattern and developmental context. Palaeontology 50, 57–73 (2007).

    Google Scholar 

  27. 27

    Benton, M. J. Exploring macroevolution using modern and fossil data. Proc. R. Soc. B 282, 20150569 (2015).

    PubMed  Google Scholar 

  28. 28

    Buatois, L. A., Mángano, M. G., Olea, R. A. & Wilson, M. A. Decoupled evolution of soft and hard substrate communities during the Cambrian Explosion and Great Ordovician Biodiversification Event. Proc. Natl Acad. Sci. USA 113, 6945–6948 (2016).

    CAS  PubMed  Google Scholar 

  29. 29

    Minter, N. J ., Buatois, L. A & Mángano, M. G . in The Trace-Fossil Record of Major Evolutionary Events Vol. 1 (eds Mángano, M. G. & Buatois, L. A. ) 1–26 (Springer, 2016).

    Google Scholar 

  30. 30

    Benton, M. J. Palaeodiversity and formation counts: redundancy or bias? Palaeontology 58, 1003–1029 (2015).

    Google Scholar 

  31. 31

    Johnson, E. W., Briggs, D. E. G., Suthren, R. J., Wright, J. L. & Tunnicliff, S. P. Non-marine arthropod traces from the subaerial Ordovician Borrowdale Volcanic Group, English Lake District. Geol. Mag. 131, 395–406 (1994).

    Google Scholar 

  32. 32

    Labandeira, C. C. Invasion of the continents: cyanobacterial crusts to tree-inhabiting arthropods. Trends Ecol. Evol. 20, 253–262 (2005).

    PubMed  Google Scholar 

  33. 33

    Morrissey, L. B., Braddy, S. J., Dodd, C., Higgs, K. T. & Williams, B. P. J. Trace fossils and palaeoenvironments of the Middle Devonian Caherbla Group, Dingle Peninsula, southwest Ireland. Geol. J. 47, 1–29 (2012).

    Google Scholar 

  34. 34

    Walker, E. F. Arthropod ichnofauna of the Old Red Sandstone at Dunure and Montrose, Scotland. Earth Env. Sci. T. R. So. 76, 287–297 (1985).

    Google Scholar 

  35. 35

    Mángano, M. G., Buatois, L. A., Astini, R. & Rindsberg, A. K. Trilobites in Early Cambrian tidal flats and the landward expansion of the Cambrian explosion. Geology 42, 143–146 (2014).

    Google Scholar 

  36. 36

    Davies, N. S., Sansom, I. J., Albanesi, G. L. & Cespedes, R. Ichnology, palaeoecology and taphonomy of an Ordovician vertebrate habitat: the Anzaldo Formation, central Bolivia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 249, 18–35 (2007).

    Google Scholar 

  37. 37

    Shear, W. A. & Kukalová-Peck, J. The ecology of Paleozoic terrestrial arthropods: the fossil evidence. Can. J. Zool. 68, 1807‒1834 (1990).

    Google Scholar 

  38. 38

    Wright, J. L., Quinn, L., Briggs, D. E. G. & Williams, S. H. A subaerial arthropod trackway from the Upper Silurian Clam Bank Formation of Newfoundland. Can. J. Earth Sci. 32, 304–313 (1995).

    Google Scholar 

  39. 39

    Marriott, S. B., Morrissey, L. B. & Hillier, R. D. Trace fossil assemblages in Upper Silurian tuff beds: evidence of biodiversity in the Old Red Sandstone of southwest Wales, UK. Palaeogeogr. Palaeoclimatol. Palaeoecol. 274, 160–172 (2009).

    Google Scholar 

  40. 40

    Minter, N. J. et al. in The Trace-Fossil Record of Major Evolutionary Events Vol. 1 (eds Mángano, M. G. & Buatois, L. A. ) 205–324 (Springer, 2016).

    Google Scholar 

  41. 41

    Davies, N. S., Sansom, I. J. & Turner, P. Trace fossils and paleoenvironments of a Late Silurian marginal-marine/alluvial system: the Ringerike Group (Lower Old Red Sandstone), Oslo Region, Norway. Palaios 21, 46–62 (2006).

    Google Scholar 

  42. 42

    Buatois, L. A. & Mángano, M. G . in Microbial Mats in Siliciclastic Sediments SEPM Special Publication 101 (eds Noffke, N. & Chafez, H. ) 15–28 (Society for Sedimentary Geology, 2012).

    Google Scholar 

  43. 43

    Gibling, M. R. & Davies, N. S. Palaeozoic landscapes shaped by plant evolution. Nat. Geosci. 5, 99–105 (2012).

    CAS  Google Scholar 

  44. 44

    Corenblit, D ., Davies, N. S ., Steiger, J ., Gibling, M. R & Bornette, G. Considering river structure and stability in the light of evolution: feedbacks between riparian vegetation and hydrogeomorphology. Earth Surf. Proc. Land. 40, 189–207 (2015).

    Google Scholar 

  45. 45

    Davies, N. S. & Gibling, M. R. The sedimentary record of Carboniferous rivers: continuing influence of land plant evolution on alluvial processes and Palaeozoic ecosystems. Earth Sci. Rev. 120, 40–79 (2013).

    Google Scholar 

  46. 46

    Ward, J. V., Tockner, K., Arscott, D. B & Claret, C. Riverine landscape diversity. Freshwater Biol. 47, 517–539 (2002).

    Google Scholar 

  47. 47

    Erwin, D. H. A preliminary classification of evolutionary radiations. Hist. Biol. 6, 133–147 (1992).

    Google Scholar 

  48. 48

    Ruta, M., Angielczyk, K. D., Fröbisch, J. & Benton, M. J. Decoupling of morphological disparity and taxic diversity during the adaptive radiation of the anomodont therapsids. Proc. R. Soc. B 280, 20131071 (2013).

    PubMed  Google Scholar 

  49. 49

    Chloe, J. C & Crespi, B. J. The Evolution of Social Behavior in Insects and Arachnids (Cambridge Univ. Press, 1997).

    Google Scholar 

  50. 50

    Buatois, L. A., Labandeira, C. C., Mángano, M. G., Cohen, A. & Voigt, S. in The Trace-Fossil Record of Major Evolutionary Events Vol. 2 (eds Mángano, M. G. & Buatois, L. A. ) 179–263 (Springer, 2016).

    Google Scholar 

  51. 51

    Bertling, M. et al. Names for trace fossils: a uniform approach. Lethaia 39, 265–286 (2006).

    Google Scholar 

  52. 52

    Minter, N. J., Braddy, S. J. & Davis, R. B. Between a rock and a hard place: arthropod trackways and ichnotaxonomy. Lethaia 40, 365–375 (2007).

    Google Scholar 

  53. 53

    Knaust, D. in Trace-Fossils as Indicators of Sedimentary Environments (eds Knaust, D. & Bromley, R. G. ) 79–101 (Elsevier, 2012).

    Google Scholar 

  54. 54

    Alroy, J. et al. Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proc. Natl Acad. Sci. USA 98, 6261–6266 (2001).

    CAS  PubMed  Google Scholar 

  55. 55

    Smith, A. B. & McGowan, A. J. The shape of the Phanerozoic marine palaeodiversity curve: how much can be predicted from the sedimentary rock record of Western Europe? Palaeontology 50, 765–774 (2007).

    Google Scholar 

  56. 56

    Lloyd, G. T. A refined modelling approach to assess the influence of sampling on palaeodiversity curves: new support for declining Cretaceous dinosaur richness. Biol. Lett. 8, 123–126 (2012).

    PubMed  Google Scholar 

  57. 57

    Sakamoto, M., Venditti, C. & Benton, M. J. ‘Residual diversity estimates’ do not correct for sampling bias in palaeodiversity data. Methods Ecol. Evol. 8, 453–459 (2017).

    Google Scholar 

  58. 58

    Ronov, A. B., Khain, V. E., Balukhovsky, A. N. & Seslavinsky, K. B. Quantitative analysis of Phanerozoic sedimentation. Sediment. Geol. 25, 311–325 (1980).

    Google Scholar 

  59. 59

    Peters, S. E. Macrostratigraphy of North America. J. Geol. 114, 391–412 (2006).

    Google Scholar 

  60. 60

    Buatois, L. A., Wisshak, M., Wilson, M. A. & Mángano, M. G. Categories of architectural designs in trace fossils: a measure of ichnodisparity. Earth-Sci. Rev. 164, 102–181 (2017).

    CAS  Google Scholar 

  61. 61

    Bromley, R. G. Trace Fossils: Biology, Taphonomy and Applications (Chapman and Hall, 1996).

    Google Scholar 

  62. 62

    Bambach, R. K., Bush, A. M. & Erwin, D. H. Autecology and the filling of ecospace: key metazoan radiations. Palaeontology 50, 1–22 (2007).

    Google Scholar 

  63. 63

    Bush, A. M., Bambach, R. K. & Daley, G. M. Changes in theoretical ecospace utilization in marine fossil assemblages between the mid-Paleozoic and late Cenozoic. Paleobiology 33, 76–97 (2007).

    Google Scholar 

  64. 64

    Ausich, W. I. & Bottjer, D. J. Tiering in suspension-feeding communities on soft substrata throughout the Phanerozoic. Science 216, 173–174 (1982).

    CAS  PubMed  Google Scholar 

  65. 65

    Bottjer, D. J. & Ausich, W. I. Phanerozoic development of tiering in soft-substrate suspension-feeding communities. Paleobiology 12, 400–420 (1986).

    Google Scholar 

  66. 66

    Mángano, M. G. & Buatois, L. A. Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks. Proc. R. Soc. B 281, 20140038 (2014).

    PubMed  Google Scholar 

  67. 67

    Buatois, L. A & Mángano, M. G. Ichnology: Organism‒Substrate Interactions in Space and Time (Cambridge Univ. Press, 2011).

    Google Scholar 

  68. 68

    François, F., Poggiale, J.-C., Durbec, J.-P. & Stora, G. A new approach for the modeling of sediment reworking induced by a macrobenthic community. Acta Biotheor. 45, 295–319 (1997).

    Google Scholar 

  69. 69

    François, F., Gerino, M., Stora, G., Durbec, J.-P. & Poggiale, J.-C. Functional approach to sediment reworking by gallery-forming macrobenthic animals: modeling and application with the polychaete Nereis diversicolor . Mar. Ecol. Prog. Ser. 229, 127–136 (2002).

    Google Scholar 

  70. 70

    Solan, M. & Wigham, B. D. in Interactions Between Macro- and Microorganisms in Marine Sediments (eds Kristensen, E., Haese, R. R. & Kostka, J. E. ) 105–124 (Coastal and Estuarine Studies 60, American Geophysical Union, 2005).

    Google Scholar 

  71. 71

    Buatois, L. A. & Mángano, M. G. in Trace Fossils: Concepts, Problems, Prospects (ed. Miller, W. III ) 285–323 (Elsevier, 2007).

    Google Scholar 

  72. 72

    Buatois, L. A., Mángano, M. G., Maples, C. G. & Lanier, W. P. The paradox of nonmarine ichnofaunas in tidal rhythmites: integrating sedimentologic and ichnologic data from the Late Carboniferous of eastern Kansas, USA. Palaios 12, 467–481 (1997).

    Google Scholar 

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Acknowledgements

Financial support for the initial part of this project was provided to N.J.M. through a Government of Canada Post-doctoral Research Fellowship under the Canadian Commonwealth Scholarship Program. Additional funding was provided by the Natural Sciences and Engineering Research Council (NSERC) Discovery Grants 311726-05/08/15 and 311727-05/08/13 (to L.A.B. and M.G.M., respectively). M.R.G also acknowledges funding from an NSERC Discovery Grant. This is Earth Sciences Sector contribution number 20160255 and contribution 314 of the Evolution of Terrestrial Ecosystems Consortium of the National Museum of Natural History, Washington DC. We are grateful for the constructive comments of R. Garwood, which improved the manuscript.

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N.J.M., L.A.B. and M.G.M. conceived the study. N.J.M., L.A.B., M.G.M., N.S.D., M.R.G., R.B.M. and C.C.L. contributed data to the analysis. N.J.M. performed the analysis and analysed the results. N.J.M. led the writing of the paper, with input from the other authors.

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Correspondence to Nicholas J. Minter.

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Supplementary information

Supplementary Information

Supplementary Figures 1–6: patterns of colonization of subaerial coastal, subaqueous alluvial, aeolian, subaqueous lacustrine, marginal lacustrine, and ephemeral lacustrine environments. Supplementary Figure 7: comparison of patterns with data pooled at different temporal resolutions. Supplementary Figures 8–10: graphical correlations between diversification metrics and sampling measures. Supplementary Figure 11: numbers of ichnogenera per architectural design occupying different tiers. Supplementary Figure 12: principal co-ordinate analysis. Supplementary Tables 1,2: Statistical analyses of correlations between sampling measures and diversification metrics. (PDF 2070 kb)

Supplementary Table 3

Supplementary dataset of ichnogenera found globally by geological period within each environmental category. (XLSX 71 kb)

Supplementary Table 4

Supplementary dataset with presence–absence matrix of architectural designs. (XLSX 11 kb)

Supplementary Table 5

Supplementary dataset with presence–absence matrix of modes of life. (XLSX 40 kb)

Supplementary Table 6

Supplementary dataset with presence–absence matrix of impacts upon the sediment. (XLSX 40 kb)

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Minter, N., Buatois, L., Mángano, M. et al. Early bursts of diversification defined the faunal colonization of land. Nat Ecol Evol 1, 0175 (2017). https://doi.org/10.1038/s41559-017-0175

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