Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Explosive diversification of marine fishes at the Cretaceous–Palaeogene boundary

Nature Ecology & Evolution volume 2, pages 688–696 (2018)Cite this article

Subjects

Abstract

The Cretaceous–Palaeogene (K–Pg) mass extinction is linked to the rapid emergence of ecologically divergent higher taxa (for example, families and orders) across terrestrial vertebrates, but its impact on the diversification of marine vertebrates is less clear. Spiny-rayed fishes (Acanthomorpha) provide an ideal system for exploring the effects of the K–Pg on fish diversification, yet despite decades of morphological and molecular phylogenetic efforts, resolution of both early diverging lineages and enormously diverse subclades remains problematic. Recent multilocus studies have provided the first resolved phylogenetic backbone for acanthomorphs and suggested novel relationships among major lineages. However, these new relationships and associated timescales have not been interrogated using phylogenomic approaches. Here, we use targeted enrichment of >1,000 ultraconserved elements in conjunction with a divergence time analysis to resolve relationships among 120 major acanthomorph lineages and provide a new timescale for acanthomorph radiation. Our results include a well-supported topology that strongly resolves relationships along the acanthomorph backbone and the recovery of several new relationships within six major percomorph subclades. Divergence time analyses also reveal that crown ages for five of these subclades, and for the bulk of the species diversity in the sixth, coincide with the K–Pg boundary, with divergences between anatomically and ecologically distinctive suprafamilial clades concentrated in the first 10 million years of the Cenozoic.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Previous hypotheses for relationships among early diverging acanthomorphs.
Fig. 2: Previous hypotheses for relationships among major percomorph lineages.
Fig. 3: Evolutionary timescale for acanthomorph fishes.
Fig. 4: Fossil calibration placement.
Fig. 5: Divergence times of the acanthomorph radiation.

Similar content being viewed by others

References

  1. Erwin, D. H. Lessons from the past: biotic recoveries from mass extinctions. Proc. Natl Acad. Sci. USA 98, 5399–5403 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Krug, A. Z., Jablonski, D. & Valentine, J. W. Signature of the end-Cretaceous mass extinction in the modern biota. Science 323, 767–771 (2009).

    Article  CAS  PubMed  Google Scholar 

  3. Jarvis, E. D. et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320–1331 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).

    Article  CAS  PubMed  Google Scholar 

  5. O’Leary, M. A. et al. The placental mammal ancestor and the post-K–Pg radiation of placentals. Science 339, 662–667 (2013).

    Article  CAS  PubMed  Google Scholar 

  6. Longrich, N. R., Bhullar, B.-A. S. & Gauthier, J. A. Mass extinction of lizards and snakes at the Cretaceous–Paleogene boundary. Proc. Natl Acad. Sci. USA 109, 21396–21401 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Benton, M. J. Diversification and extinction in the history of life. Science 268, 52–58 (1995).

    Article  CAS  PubMed  Google Scholar 

  8. Near, T. J. et al. Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proc. Natl Acad. Sci. USA 110, 12738–12743 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Sanciangco, M. D., Carpenter, K. E. & Betancur-R, R. Phylogenetic placement of enigmatic percomorph families (Teleostei: Percomorphaceae). Mol. Phylogenet. Evol. 94, 565–576 (2016).

    Article  PubMed  Google Scholar 

  10. Santini, F., Harmon, L. J., Carnevale, G. & Alfaro, M. E. Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol. Biol. 9, 194 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Near, T. J. et al. Resolution of ray-finned fish phylogeny and timing of diversification. Proc. Natl Acad. Sci. USA 109, 13698–13703 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Patterson, C. & Smith, A. B. Periodicity in extinction: the role of systematics. Ecology 70, 802–811 (1989).

    Article  Google Scholar 

  13. MacLeod, N. et al. The Cretaceous–Tertiary biotic transition. J. Geol. Soc. Lond. 154, 265–292 (1997).

    Article  Google Scholar 

  14. Cavin, L. in Geological and Biological Effects of Impact Events (eds Buffetaut, E. & Koeberl, C.) 141–158 (Springer, Berlin & Heidelberg, 2002).

  15. Friedman, M. Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction. Proc. R. Soc. B 277, 1675–1683 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Friedman, M. Ecomorphological selectivity among marine teleost fishes during the end-Cretaceous extinction. Proc. Natl Acad. Sci. USA 106, 5218–5223 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Sibert, E. C. & Norris, R. D. New age of fishes initiated by the Cretaceous–Paleogene mass extinction. Proc. Natl Acad. Sci. USA 112, 8537–8542 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Patterson, C. An overview of the early fossil record of the acanthomorphs. Bull. Mar. Sci. 52, 29–59 (1993).

    Google Scholar 

  19. Johnson, D. G. Percomorph phylogeny: progress and problems. Bull. Mar. Sci. 52, 3–28 (1993).

    Google Scholar 

  20. Johnson, D. G. & Patterson, C. Percomorph phylogeny: a survey of acanthomorphs and a new proposal. Bull. Mar. Sci. 52, 554–626 (1993).

    Google Scholar 

  21. Davesne, D. et al. The phylogenetic intrarelationships of spiny-rayed fishes (Acanthomorpha, Teleostei, Actinopterygii): fossil taxa increase the congruence of morphology with molecular data. Front. Ecol. Evol. 4, 129 (2016).

    Article  Google Scholar 

  22. Alfaro, M. E. et al. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl Acad. Sci. USA 106, 13410–13414 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nelson, J. S. Fishes of the World 4th edn (Wiley, Hoboken, 2006).

  24. Betancur, R. et al. The tree of life and a new classification of bony fishes. PLoS Curr. 5, https://doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288 (2013).

  25. Wainwright, P. C. et al. The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. Syst. Biol. 61, 1001–1027 (2012).

    Article  PubMed  Google Scholar 

  26. Faircloth, B. C., Sorenson, L., Santini, F. & Alfaro, M. E. A phylogenomic perspective on the radiation of ray-finned fishes based upon targeted sequencing of ultraconserved elements (UCEs). PLoS ONE 8, e65923 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bejerano, G. et al. Ultraconserved elements in the human genome. Science 304, 1321–1325 (2004).

    Article  CAS  PubMed  Google Scholar 

  28. Faircloth, B. C. et al. Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst. Biol. 61, 717–726 (2012).

    Article  PubMed  Google Scholar 

  29. Setiamarga, D. H. E. et al. Divergence time of the two regional medaka populations in Japan as a new time scale for comparative genomics of vertebrates. Biol. Lett. 5, 812–816 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Yamanoue, Y., Miya, M., Inoue, J. G., Matsuura, K. & Nishida, M. The mitochondrial genome of spotted green pufferfish Tetraodon nigroviridis (Teleostei: Tetraodontiformes) and divergence time estimation among model organisms in fishes. Genes Genet. Syst. 81, 29–39 (2006).

    Article  CAS  PubMed  Google Scholar 

  31. Yang, Z. & Rannala, B. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23, 212–226 (2006).

    Article  CAS  PubMed  Google Scholar 

  32. Zheng, Y., Peng, R., Kuro-o, M. & Zeng, X. Exploring patterns and extent of bias in estimating divergence time from mitochondrial DNA sequence data in a particular lineage: a case study of salamanders (order Caudata). Mol. Biol. Evol. 28, 2521–2535 (2011).

    Article  CAS  PubMed  Google Scholar 

  33. Brown, J. W. & Van Tuinen, M. (eds) in Living Dinosaurs: The Evolutionary History of Modern Birds 306–324 (Wiley, Chichester, 2011).

  34. Smith, B. T. & Klicka, J. Examining the role of effective population size on mitochondrial and multilocus divergence time discordance in a songbird. PLoS ONE 8, e55161 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Friedman, M. & Sallan, L. C. Five hundred million years of extinction and recovery: a Phanerozoic survey of large-scale diversity patterns in fishes. Palaeontology 55, 707–742 (2012).

    Article  Google Scholar 

  36. Miya, M. et al. Evolutionary origin of the scombridae (tunas and mackerels): members of a Paleogene adaptive radiation with 14 other pelagic fish families. PLoS ONE 8, e73535 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Harrington, R. C. et al. Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in a blink of the evolutionary eye. BMC Evol. Biol. 16, 224 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Carnevale, G. & Johnson, G. D. A Cretaceous cusk-eel (Teleostei, Ophidiiformes) from Italy and the Mesozoic diversification of percomorph fishes. Copeia 103, 771–791 (2015).

    Article  Google Scholar 

  39. Schwarzhans, W. in Mesozoic Fishes—Systematics and Paleoecology (ed. Viohl, G.) 417–431 (F. Pfeil, München, 1996).

  40. Faircloth, B. C. & Glenn, T. C. Not all sequence tags are created equal: designing and validating sequence identification tags robust to indels. PLoS ONE 7, e42543 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Glenn, T. C. et al. Adapterama I: universal stubs and primers for thousands of dual-indexed Illumina libraries (iTru & iNext). Preprint at https://doi.org/10.1101/049114 (2016).

  42. Blumenstiel, B. et al. Targeted exon sequencing by in-solution hybrid selection. Curr. Protoc. Hum. Genet. 66, 18.4.1–18.4.24 (2010).

    Google Scholar 

  43. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Faircloth, B. C. PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32, 786–788 (2015).

    Article  PubMed  CAS  Google Scholar 

  45. Lanfear, R., Calcott, B., Ho, S. Y. W. & Guindon, S. Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695–1701 (2012).

    Article  CAS  PubMed  Google Scholar 

  46. Lanfear, R., Calcott, B., Kainer, D., Mayer, C. & Stamatakis, A. Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evol. Biol. 14, 82 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Aberer, A. J., Kobert, K. & Stamatakis, A. ExaBayes: massively parallel Bayesian tree inference for the whole-genome era. Mol. Biol. Evol. 31, 2553–2556 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Phillips, M. J. & Penny, D. The root of the mammalian tree inferred from whole mitochondrial genomes. Mol. Phylogenet. Evol. 28, 171–185 (2003).

    Article  CAS  PubMed  Google Scholar 

  50. Phillips, M. J., Delsuc, F. & Penny, D. Genome-scale phylogeny and the detection of systematic biases. Mol. Biol. Evol. 21, 1455–1458 (2004).

    Article  CAS  PubMed  Google Scholar 

  51. Seo, T.-K. Calculating bootstrap probabilities of phylogeny using multilocus sequence data. Mol. Biol. Evol. 25, 960–971 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Mirarab, S. & Warnow, T. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44–i52 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sukumaran, J. & Holder, M. T. DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569–1571 (2010).

    Article  CAS  PubMed  Google Scholar 

  54. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. Dos Reis, M. & Yang, Z. Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times. Mol. Biol. Evol. 28, 2161–2172 (2011).

    Article  CAS  PubMed  Google Scholar 

  56. Smith, S., Brown, J. W. & Walker, J. F. So many genes, so little time: comments on divergence-time estimation in the genomic era. Preprint at https://doi.org/10.1101/114975 (2017).

  57. Huerta-Cepas, J., Serra, F. & Bork, P. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol. Biol. Evol. 33, 1635–1638 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Vaidya, G., Lohman, D. J. & Meier, R. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180 (2011).

    Article  PubMed  Google Scholar 

  59. Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2017).

    CAS  PubMed  Google Scholar 

  60. Chen, W.-J. et al. New insights on early evolution of spiny-rayed fishes (Teleostei: Acanthomorpha). Front. Mar. Sci. 1, 1–17 (2014).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Johnson for the illustrations used in the figures. This work was partially supported by National Science Foundation grants DEB-0842397 (to M.E.A.); DEB-1242260, DEB-1655624 (to B.C.F.); and startup funds from Louisiana State University (to B.C.F.). DNA alignment was supported in part by resources and technical expertise from the Georgia Advanced Computing Resource Center—a partnership between the University of Georgia’s Office of the Vice President for Research and Office of the Vice President for Information Technology. Phylogenetic analysis portions of this research were conducted using high-performance computing resources provided by Louisiana State University (http://www.hpc.lsu.edu).

Author information

Author notes

  1. These authors contributed equally: Michael E. Alfaro and Brant C. Faircloth.

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA

    Michael E. Alfaro, Laurie Sorenson & David Černý

  2. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA

    Brant C. Faircloth & Carl H. Oliveros

  3. Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA

    Brant C. Faircloth

  4. Department of Earth Sciences, University of Oxford, Oxford, UK

    Richard C. Harrington & Matt Friedman

  5. Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA

    Richard C. Harrington & Thomas J. Near

  6. Museum of Paleontology, University of Michigan, Ann Arbor, MI, USA

    Matt Friedman

  7. Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA

    Matt Friedman

  8. Natural History Museum of Los Angeles County, Los Angeles, CA, USA

    Christine E. Thacker

  9. Peabody Museum of Natural History, Yale University, New Haven, CT, USA

    Thomas J. Near

Authors
  1. Michael E. Alfaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brant C. Faircloth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard C. Harrington
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laurie Sorenson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matt Friedman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christine E. Thacker
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carl H. Oliveros
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. David Černý
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Thomas J. Near
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.E.A. conceived the study. M.E.A., B.C.F., R.C.H., M.F. and T.J.N. designed the study. L.S., R.C.H. and B.C.F. collected the sequence data from enriched UCE loci. M.F. selected appropriate calibration points. B.C.F., M.E.A., D.Č. and C.H.O. performed the data analyses. M.E.A. and B.C.F. wrote the manuscript with help from R.C.H., L.S., M.F., D.Č. and T.J.N. All authors read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Michael E. Alfaro or Brant C. Faircloth.

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 Information, Methods, Results, References and Figures

Life Sciences Reporting Summary

Supplementary Table 1

Species, family, institutional or personal voucher code, preparation method (Prep.), enrichment method (Enrich.), sequencing platform (Plat.), and NCBI BioSample and SRA accession information for each individual used in this study

Supplementary Table 2

Statistics for trimmed sequence reads collected from each library enriched for ultraconserved element loci

Supplementary Table 3

Statistics for all contigs assembled from trimmed sequence data collected from each library enriched for ultraconserved element loci

Supplementary Table 4

Statistics for ultraconserved element (UCE) contigs assembled from trimmed sequence data collected from each library enriched for ultraconserved element loci

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alfaro, M.E., Faircloth, B.C., Harrington, R.C. et al. Explosive diversification of marine fishes at the Cretaceous–Palaeogene boundary. Nat Ecol Evol 2, 688–696 (2018). https://doi.org/10.1038/s41559-018-0494-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0494-6

This article is cited by

Search

Advanced search

Quick links

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