Morphospace expansion paces taxonomic diversification after end Cretaceous mass extinction

Abstract

Highly resolved palaeontological records can address a key question about our current climate crisis: how long will it be before the biosphere rebounds from our actions? There are many ways to conceptualize the recovery of the biosphere; here, we focus on the global recovery of species diversity. Mass extinction may be expected to be followed by rapid speciation, but the fossil record contains many instances where speciation is delayed—a phenomenon about which we have a poor understanding. A probable explanation for this delay is that extinctions eliminate morphospace as they curtail diversity, and the delay in diversification is a result of the time needed for new innovations to rebuild morphospace, which can then be filled out by new species. Here, we test this morphospace reconstruction hypothesis using the morphological complexity of planktic foraminifer tests after the Cretaceous–Palaeogene mass extinction. We show that increases in complexity precede changes in diversity, indicating that plankton are colonizing new morphospace, then slowly filling it in. Preliminary diversification is associated with a rapid increase in the complexity of groups refilling relict Cretaceous ecospace. Subsequent jumps in complexity are driven by evolutionary innovations (development of spines and photosymbionts), which open new niche space. The recovery of diversity is paced by the construction of new morphospace, implying a fundamental speed limit on diversification after an extinction event.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Planktic foraminifer diversity and test compexity.
Fig. 2: Comparison of Early Palaeogene climate events with planktic foraminifer diversity and complexity trends.

Data availability

All data and code related to this study are available at https://github.com/Fraass.

References

  1. 1.

    Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57 (2011).

    CAS  Article  Google Scholar 

  2. 2.

    Schulte, P. et al. The Chicxulub asteroid impact and mass extinction at the Cretaceous–Paleogene boundary. Science 327, 1214–1218 (2010).

    CAS  Article  Google Scholar 

  3. 3.

    Coxall, H. K., D’Hondt, S. & Zachos, J. C. Pelagic evolution and environmental recovery after the Cretaceous–Paleogene mass extinction. Geology 34, 297–300 (2006).

    CAS  Article  Google Scholar 

  4. 4.

    Smit, J. Extinction and evolution of planktonic foraminifera after a major impact at the Cretaceous/Tertirary boundary. Geol. Soc. Am. Spec. Pap. 190, 329–352 (1982).

    Google Scholar 

  5. 5.

    Hemleben, C., Mühlen, D., Olsson, R. K. & Berggren, W. A. Surface texture and the first occurrence of spines in planktonic foraminifera from the Early Tertiary. Geol. Jb. 128, 117–146 (1991).

    Google Scholar 

  6. 6.

    Olsson, R. K., Hemleben, C., Berggren, W. A. & Liu, C. Wall texture classification of planktonic foraminifera genera in the lower Danian. J. Foraminiferal Res. 22, 195–213 (1992).

    Article  Google Scholar 

  7. 7.

    Arenillas, I., Arz, J. & Molina, E. A new high‐resolution planktic foraminiferal zonation and subzonation for the lower Danian. Lethaia 37, 79–95 (2004).

    Article  Google Scholar 

  8. 8.

    Smit, J. & Ten Kate, W. G. H. Z. Trace-element patterns at the Cretaceous–Tertiary boundary—consequences of a large impact. Cretac. Res. 3, 307–332 (1982).

    CAS  Article  Google Scholar 

  9. 9.

    D’Hondt, S. & Keller, G. Some patterns of planktic foraminiferal assemblage turnover at the Cretaceous–Tertiary boundary. Mar. Micropaleontol. 17, 77–118 (1991).

    Article  Google Scholar 

  10. 10.

    Alegret, L., Arenillas, I., Arz, J. A. & Molina, E. Foraminiferal event-stratigraphy across the Cretaceous/Paleogene boundary. Neues Jahrb. Geol. Palaontol. Abh. 231, 25–50 (2004).

    Google Scholar 

  11. 11.

    Koutsoukos, E. A. M. Phenotypic plasticity, speciation, and phylogeny in early Danian planktic foraminifera. J. Foraminiferal Res. 44, 109–142 (2014).

    Article  Google Scholar 

  12. 12.

    Lowery, C. et al. Rapid recovery of life at ground zero of the end Cretaceous mass extinction. Nature 558, 288–291 (2018).

    CAS  Article  Google Scholar 

  13. 13.

    Birch, H. S., Coxall, H. K. & Pearson, P. N. Evolutionary ecology of Early Paleocene planktonic foraminifera: size, depth habitat, and symbiosis. Paleobiology 38, 374–390 (2012).

    Article  Google Scholar 

  14. 14.

    Birch, H. S., Coxall, H. K., Pearson, P. N., Kroon, D. K. & Schmidt, D. N. Partial collapse of the marine carbon pump after the Cretaceous–Paleogene boundary. Geology 44, 287–290 (2016).

    CAS  Article  Google Scholar 

  15. 15.

    Fraass, A. J., Kelly, D. C. & Peters, S. E. Macroevolutionary history of the planktic foraminifera. Annu. Rev. Earth Planet. Sci. 43, 139–166 (2015).

    CAS  Article  Google Scholar 

  16. 16.

    Sepkoski, J. J. Jr. Rates of speciation in the fossil record. Phil. Trans. R. Soc. Lond. B 353, 315–326 (1998).

    Article  Google Scholar 

  17. 17.

    Kirchner, J. W. & Weil, A. Delayed biological recovery from extinctions throughout the fossil record. Nature 404, 177–180 (2000).

    CAS  Article  Google Scholar 

  18. 18.

    Alroy, J. Dynamics of origination and extinction in the marine fossil record. Proc. Natl Acad. Sci. USA 105, 11536–11542 (2008).

    CAS  Article  Google Scholar 

  19. 19.

    Ezard, T. H. G., Aze, T., Pearson, P. N. & Purvis, A. Interplay between changing climate and species’ ecology drives macroevolutionary dynamics. Science 332, 349–351 (2011).

    CAS  Article  Google Scholar 

  20. 20.

    Knoll, A. H. & Follows, M. J. A bottom-up perspective on ecosystem change in Mesozoic oceans. Proc. R. Soc. B 283, 2016755 (2016).

    Article  Google Scholar 

  21. 21.

    Jiang, S., Bralower, T. J., Patzkowsky, M. E., Kump, L. R. & Schueth, J. D. Geographic controls on nannoplankton extinction across the Cretaceous/Paleogene boundary. Nat. Geosci. 2010, 280–285 (2010).

    Article  Google Scholar 

  22. 22.

    Renne, P. R. et al. State shift in Deccan volcanism at the Cretaceous–Paleogene boundary, possibly induced by impact. Science 350, 76–78 (2015).

    CAS  Article  Google Scholar 

  23. 23.

    Gertsch, B. et al. Environmental effects of Deccan volcanism across the Cretaceous–Tertiary transition in Meghalaya, India. Earth Planet. Sci. Lett. 310, 272–285 (2011).

    CAS  Article  Google Scholar 

  24. 24.

    Punekar, J., Mateo, P. & Keller, G. Effects of Deccan volcanism on paleoenvironment and planktic foraminifera: a global survey. Geol. Soc. Am. Spec. Pap. 505, 91–116 (2014).

    Google Scholar 

  25. 25.

    Punekar, J. et al. Late Maastrichtian–early Danian high-stress environments and delayed recovery linked to Deccan volcanism. Cretac. Res. 49, 63–82 (2014).

    Article  Google Scholar 

  26. 26.

    Hull, P. M. & Norris, R. D. Diverse patterns of ocean export productivity change across the Cretaceous–Paleogene boundary: new insights from biogenic barium. Paleoceanography 26, PA3205 (2011).

    Article  Google Scholar 

  27. 27.

    Schueth, J. D., Bralower, T. J., Jiang, S. & Patzkowsky, M. E. The role of regional survivor incumbency in the evolutionary recovery of calcareous nannoplankton from the Cretaceous/Paleogene (K/Pg) mass extinction. Paleobiology 41, 661–679 (2015).

    Article  Google Scholar 

  28. 28.

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

    Article  Google Scholar 

  29. 29.

    Solé, R. V., Montoya, J. S. & Erwin, D. H. Recovery after mass extinction: evolutionary assembly in large-scale biosphere dynamics. Phil. Trans. R. Soc. Lond. 357, 697–707 (2002).

    Article  Google Scholar 

  30. 30.

    Yedid, G., Ofria, C. A. & Lenski, R. E. Selective press extinctions, but not random pulse extinctions, cause delayed ecological recovery in communities of digital organisms. Am. Nat. 173, E139–E154 (2009).

    Article  Google Scholar 

  31. 31.

    Foote, M. Morphological disparity in Ordovician–Devonian crinoids and the early saturation of morphological space. Paleobiology 20, 320–344 (1994).

    Article  Google Scholar 

  32. 32.

    Wagner, P. J. in Evolution Since Darwin: The First 150 Years 451–478 (Sinauer, Sunderland, 2010).

  33. 33.

    Hughes, M., Gerber, G. & Wulls, M. A. Clades reach highest morphological disparity early in their evolution. Proc. Natl Acad. Sci. USA 110, 13875–13879 (2010).

    Article  Google Scholar 

  34. 34.

    Leckie, R. M. Paleoecology of mid-Cretaceous planktonic foraminifera: a comparison of open ocean and epicontinental assemblages. Micropaleontology 33, 164–176 (1987).

    Article  Google Scholar 

  35. 35.

    Henehan, M. J., Hull, P. M., Penman, D. E., Rae, J. W. B. & Schmidt, D. N. Biogeochemical significance of pelagic ecosystem function: an end-Cretaceous case study. Phil. Trans. R. Soc. B 371, 20150510 (2016).

    Article  Google Scholar 

  36. 36.

    Malmgren, B. A., Berggren, W. A. & Lohmann, G. P. Species formation through punctuated gradualism in planktonic foraminifera. Science 225, 317–319 (1984).

    CAS  Article  Google Scholar 

  37. 37.

    Kelly, C. D., Bralower, T. J. & Zachos, J. C. Evolutionary consequences of the latest Paleocene thermal maximum for tropical planktonic foraminifera. Palaeogeogr. Palaeoclimatol. Palaeoecol. 141, 139–161 (1998).

    Article  Google Scholar 

  38. 38.

    Leckie, R. M., Bralower, T. J. & Chasman, R. Oceanic anoxic events and plankton evolution: biotic response to tectonic forcing in the mid-Cretaceous. Paleoceanography 17, 13-1–13-29 (2002).

    Article  Google Scholar 

  39. 39.

    Brombacher, A., Wilson, P. A., Bailey, I. & Ezard, T. H. G. The breakdown of static and evolutionary allometries during climatic upheaval. Am. Nat. 190, 350–362 (2017).

    Article  Google Scholar 

  40. 40.

    Peters, S. E., Kelly, D. C. & Fraass, A. J. Oceanographic controls on the diversity and extinction of planktonic foraminifera. Nature 493, 398–401 (2013).

    CAS  Article  Google Scholar 

  41. 41.

    Quillévéré, F., Norris, R. D., Kroon, D. & Wilson, P. A. Transient ocean warming and shifts in carbon reservoirs during the early Danian. Earth Planet. Sci. Lett. 265, 600–615 (2008).

    Article  Google Scholar 

  42. 42.

    Bornemann, A. et al. Latest Danian carbon isotope anomaly and associated environmental change in the southern Tethys (Nile Basin, Egypt). J. Geol. Soc. Lond. 166, 1135–1142 (2009).

    CAS  Article  Google Scholar 

  43. 43.

    Petrizzo, M. R. An early Late Paleocene event on Shatsky Rise, northwest Pacific Ocean (ODP Leg 198): evidence from planktonic foraminiferal assemblages. In Proc. Ocean Drilling Program (eds Bralower, T. J., Premoli Silva, I. & Malone, M. J.) 1–29 (Scientific Results Volume 198, 2005).

  44. 44.

    Schoene, B. et al. U–Pb geochronology of the Deccan Traps and relation to the end-Cretaceous mass extinction. Science 347, 182–184 (2015).

    CAS  Article  Google Scholar 

  45. 45.

    Jehle, S., Bornemann, A., Deprez, A. & Speijer, R. P. The impact of the Latest Danian Event on planktic foraminifera faunas at ODP Site 1210 (Shatsky Rise, Pacific Ocean). PLoS ONE 10, e0141644 (2015).

    Article  Google Scholar 

  46. 46.

    Quillévéré, F. & Norris, R. D. Ecological development of acarininids (planktonic foraminifera) and hydrographic evolution of Paleoecene surface waters. In Causes and Consequences of Globally Warm Climates in the Early Paleogene: Boulder, Colorado (eds Wing, S. L., Gingerich, P. D., Schmitz, B. & Thomas, E.) 223–238 (Special Paper 369, Geological Society of America, 2003).

  47. 47.

    Olsson, D. K., Hemleben, C., Berggren, W. A. & Huber, B. T. Atlas of Paleocene Planktonic Foraminifera 85 (Smithsonian Contributions to Paleobiology, 1999).

  48. 48.

    Huber, B. T. et al. Mesozoic planktonic foraminiferal taxonomic dictionary. Chronos www.chronos.org (2006).

  49. 49.

    Aze, T. et al. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biol. Rev. 86, 900–927 (2011).

    Article  Google Scholar 

  50. 50.

    Huber, B. T. et al. Pforams@microtax: a new online taxonomic database for planktonic foraminifera. Micropaleontology 62, 429–438 (2017).

    Google Scholar 

  51. 51.

    Spero, H. Life history and stable isotope geochemistry of planktonic foraminifera. Paleontological Soc. Pap. 4, 7–36 (1998).

    Google Scholar 

  52. 52.

    Vandenberghe, N. et al. in The Geologic Time Scale, 855–921 (Elsevier, Amsterdam, 2012).

    Google Scholar 

Download references

Acknowledgements

The authors acknowledge support to C.M.L. via NSF-OCE-1737351. We are also grateful for the efforts of the scientific drilling community over the past 50 years in collecting the deep-sea cores that form the bulk of large datasets such as this.

Author information

Affiliations

Authors

Contributions

Both authors contributed to data interpretation, figure plotting, and writing and editing the manuscript. A.J.F. wrote the R code and performed the morphometric measurements.

Corresponding author

Correspondence to Christopher M. Lowery.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Analysis, Supplementary Figures 1 and 2 and Supplementary Table 1

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lowery, C.M., Fraass, A.J. Morphospace expansion paces taxonomic diversification after end Cretaceous mass extinction. Nat Ecol Evol 3, 900–904 (2019). https://doi.org/10.1038/s41559-019-0835-0

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing