Article

Temporal niche expansion in mammals from a nocturnal ancestor after dinosaur extinction

  • Nature Ecology & Evolution 118891895 (2017)
  • doi:10.1038/s41559-017-0366-5
  • Download Citation
Received:
Accepted:
Published online:

Abstract

Most modern mammals, including strictly diurnal species, exhibit sensory adaptations to nocturnal activity that are thought to be the result of a prolonged nocturnal phase or ‘bottleneck’ during early mammalian evolution. Nocturnality may have allowed mammals to avoid antagonistic interactions with diurnal dinosaurs during the Mesozoic. However, understanding the evolution of mammalian activity patterns is hindered by scant and ambiguous fossil evidence. While ancestral reconstructions of behavioural traits from extant species have the potential to elucidate these patterns, existing studies have been limited in taxonomic scope. Here, we use an extensive behavioural dataset for 2,415 species from all extant orders to reconstruct ancestral activity patterns across Mammalia. We find strong support for the nocturnal origin of mammals and the Cenozoic appearance of diurnality, although cathemerality (mixed diel periodicity) may have appeared in the late Cretaceous. Simian primates are among the earliest mammals to exhibit strict diurnal activity, some 52–33 million years ago. Our study is consistent with the hypothesis that temporal partitioning between early mammals and dinosaurs during the Mesozoic led to a mammalian nocturnal bottleneck, but also demonstrates the need for improved phylogenetic estimates for Mammalia.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    Aronson, B. D. et al. Circadian rhythms. Brain Res. Rev. 18, 315–333 (1993).

  2. 2.

    Kronfeld-Schor, N. & Dayan, T. Partitioning of time as an ecological resource. Annu. Rev. Ecol. Evol. Syst. 34, 153–181 (2003).

  3. 3.

    DeCoursey, P. J. Diversity of function of SCN pacemakers in behavior and ecology of three species of sciurid rodents. Biol. Rhythm Res. 35, 13–33 (2004).

  4. 4.

    Hut, R. A., Kronfeld-Schor, N., van der Vinne, V. & De la Iglesia, H. in Progress in Brain Research: The Neurobiology of Circadian Timing Vol. 199 (eds Kalsbeek, A., Merrow, M., Roenneberg, T. & Foster, R. G.) 281–304 (Elsevier, Amsterdam, 2012).

  5. 5.

    Joffe, B., Peichl, L., Hendrickson, A., Leonhardt, H. & Solovei, I. Diurnality and nocturnality in primates: an analysis from the rod photoreceptor nuclei perspective. Evol. Biol. 41, 1–11 (2014).

  6. 6.

    Melin, A. D., Matsushita, Y., Moritz, G. L., Dominy, N. J. & Kawamura, S. Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates. Proc. R. Soc. B 280, 20130189 (2013).

  7. 7.

    Gutman, R. & Dayan, T. Temoral partitioning: a experiment with two species of spiny mice. Ecology 86, 164–173 (2005).

  8. 8.

    Jones, K. E. et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648–2648 (2009).

  9. 9.

    Refinetti, R. The diversity of temporal niches in mammals. Biol. Rhythm Res. 39,173–192 (2008).

  10. 10.

    Heesy, C. P. & Hall, M. I. The nocturnal bottleneck and the evolution of mammalian vision. Brain Behav. Evol. 75, 195–203 (2010).

  11. 11.

    Walls, G. L. The Vertebrate Eye and its Adaptive Radiation (Cranbrook Institute of Science, Bloomfield Hills, 1942).

  12. 12.

    Davies, W. I. L., Collin, S. P. & Hunt, D. M. Molecular ecology and adaptation of visual photopigments in craniates. Mol. Ecol. 21, 3121–3158 (2012).

  13. 13.

    Gerkema, M. P., Davies, W. I. L., Foster, R. G., Menaker, M. & Hut, R. A. The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc. R. Soc. B 280, 20130508 (2013).

  14. 14.

    Peichl, L. Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat. Rec. 287A, 1001–1012 (2005).

  15. 15.

    Hayden, S. et al. Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Res. 20, 1–9 (2010).

  16. 16.

    Coleman, M. N. & Boyer, D. M. Inner ear evolution in primates through the Cenozoic: implications for the evolution of hearing. Anat. Rec. 295, 615–631 (2012).

  17. 17.

    Diamond, M. E., von Heimendahl, M., Knutsen, P. M., Kleinfeld, D. & Ahissar, E. ‘Where’ and ‘what’ in the whisker sensorimotor system. Nat. Rev. Neurosci. 9, 601–612 (2008).

  18. 18.

    Crompton, A. W., Taylor, C. R. & Jagger, J. A. Evolution of homeothermy in mammals. Nature 272, 333–336 (1978).

  19. 19.

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

  20. 20.

    Brusatte, S. L. et al. The extinction of the dinosaurs. Biol. Rev. 90, 628–642 (2015).

  21. 21.

    Angielczyk, K. D. & Schmitz, L. Nocturnality in synapsids predates the origin of mammals by over 100 million years. Proc. R. Soc. B 281, 20141642 (2014).

  22. 22.

    Schmitz, L. & Motani, R. Nocturnality in dinosaurs inferred from scleral ring and orbit morphology. Science 332, 705–708 (2011).

  23. 23.

    Hall, M. I., Kamilar, J. M. & Kirk, E. C. Eye shape and the nocturnal bottleneck of mammals. Proc. R. Soc. B 279, 4962–4968 (2012).

  24. 24.

    Emerling, C. A., Huynh, H. T., Nguyen, M. A., Meredith, R. W. & Springer, M. S. Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution. Proc. R. Soc. B 282, 20151817 (2015).

  25. 25.

    Reppert, S. M. & Weaver, D. R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 63, 647–676 (2001).

  26. 26.

    Griffin, R. H., Matthews, L. J. & Nunn, C. L. Evolutionary disequilibrium and activity period in primates: a Bayesian phylogenetic approach. Am. J. Phys. Anthropol. 147, 409–416 (2012).

  27. 27.

    Santini, L., Rojas, D. & Donati, G. Evolving through day and night: origin and diversification of activity pattern in modern primates. Behav. Ecol. 26, 789–796 (2015).

  28. 28.

    Heesy, C. P. & Ross, C. F. Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics. J. Hum. Evol. 40, 111–149 (2001).

  29. 29.

    Roll, U., Dayan, T. & Kronfeld-Schor, N. On the role of phylogeny in determining activity patterns of rodents. Evol. Ecol. 20, 479–490 (2006).

  30. 30.

    Meredith, R. W. et al. Impacts of the Cretaceous Terrestrial Revolution and K–Pg extinction on mammal diversification. Science 334, 521–524 (2011).

  31. 31.

    Bininda-Emonds, O. R. P. et al. The delayed rise of present-day mammals. Nature 446, 507–512 (2007).

  32. 32.

    Fritz, S. A., Bininda-Emonds, O. R. P. & Purvis, A. Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. Ecol. Lett. 12, 538–549 (2009).

  33. 33.

    Meade, A. & Pagel, M. BayesTraits: A Computer Package for Analyses of Trait Evolution. Version 3 (2017); http://www.evolution.rdg.ac.uk/BayesTraits.html

  34. 34.

    Melin, A. D. et al. Euarchontan opsin variation brings new focus to primate origins. Mol. Biol. Evol. 33, 1029–1041 (2016).

  35. 35.

    Sakamoto, M., Benton, M. J. & Venditti, C. Dinosaurs in decline tens of millions of years before their final extinction. Proc. Natl Acad. Sci. USA 113, 5036–5040 (2016).

  36. 36.

    Close R. A., Friedman, M., Lloyd G. T. & Benson R. B. J. Evidence for a mid-Jurassic adaptive radiation in mammals. Curr. Biol. 25, 2137–2142 (2015).

  37. 37.

    Lee, M. S. Y. & Beck, R. M. D. Mammalian evolution: a Jurassic spark. Curr. Biol. 25, R759–R761 (2015).

  38. 38.

    Wilson G. P. et al. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483, 457–460 (2012).

  39. 39.

    Krause, D. W. et al. First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism. Nature 515, 512–517 (2014).

  40. 40.

    Ross, C. F. Into the light: the origin of Anthropoidea. Annu. Rev. Anthropol. 29, 147–194 (2000).

  41. 41.

    Dos Reis, M., Donoghue, P. C. J. & Yang, Z. Neither phylogenomic nor palaeontological data support a Palaeogene origin of placental mammals. Biol. Lett. 10, 20131003 (2014).

  42. 42.

    Foley, N. M., Springer, M. S. & Teeling, E. C. Mammal madness: is the mammal tree of life not yet resolved? Phil. Trans. R. Soc. B 371, 20150140 (2016).

  43. 43.

    Tarver, J. E. et al. The interrelationships of placental mammals and the limits of phylogenetic inference. Genome Biol. Evol. 8, 330–344 (2016).

  44. 44.

    Springer, M. S. et al. Waking the undead: implications of a soft explosive model for the timing of placental mammal diversification. Mol. Phylogenet. Evol. 106, 86–102 (2017).

  45. 45.

    Donati, G. & Borgognini-Tarli, S. M. From darkness to daylight: cathemeral activity in primates. J. Anthropol. Sci. 84, 7–32 (2006).

  46. 46.

    Fullard, J. H. & Napoleone, N. Diel flight periodicity and the evolution of auditory defences in the Macrolepidoptera. Anim. Behav. 62, 349–368 (2001).

  47. 47.

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

  48. 48.

    Wilson, D. E. & Reeder, D. A. Mammal Species of the World (John Hopkins Univ. Press, Baltimore, 2005).

  49. 49.

    Price, S. A., Bininda-Emonds, O. R. P. & Gittleman, J. L. A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla). Biol. Rev. 80, 445–473 (2005).

  50. 50.

    O’Leary, M. A. & Gatesy, J. Impact of increased character sampling on the phylogeny of Cetartiodactyla (Mammalia): combined analysis including fossils. Cladistics 24, 397–442 (2008).

  51. 51.

    Springer, M. S., Meredith, R. W., Teeling, E. C. & Murphy, W. J. Technical comment on “The placental mammal ancestor and the Post-K–Pg radiation of placentals”. Science 341, 613–613 (2013).

  52. 52.

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

  53. 53.

    Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).

  54. 54.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2015).

  55. 55.

    Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006).

  56. 56.

    Kirk, E. C. Effects of activity pattern on eye size and orbital aperture size in primates. J. Hum. Evol. 51, 159–170 (2006).

  57. 57.

    Xie, W., Lewis, P. O., Fan, Y., Kuo, L. & Chen, M.-H. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst. Biol. 60,150–160 (2011).

  58. 58.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

  59. 59.

    Maddison, W. P. Confounding asymmetries in evolutionary diverification and character change. Evolution 60, 1743–1746 (2006).

  60. 60.

    FitzJohn, R. G. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084–1092 (2012).

  61. 61.

    Kuhn, T. S., Mooers, A. Ø. & Thomas, G. H. A simple polytomy resolver for dated phylogenies. Methods Ecol. Evol. 2, 427–436 (2011).

Download references

Acknowledgements

We thank T. C. D. Lucas, S. Meiri, E. E. Dyer, O. Comay and I. Pizer-Mason for technical assistance and providing data, and N. Kronfeld-Schor for discussion. This work was funded with support from Israel Science Foundation grant 785/09 (to T.D.), the Tel Aviv University Global Research and Training Fellowship fund and Naomi Kadar Foundation (to R.M.), and a NERC Open CASE PhD studentship (NE/H018565/1) (to H.F.-G.).

Author information

Affiliations

  1. School of Zoology, George S. Wise Faculty of Life Science, Tel Aviv University, Tel Aviv, 6997801, Israel

    • Roi Maor
    •  & Tamar Dayan
  2. Centre for Biodiversity and Environment Research, Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK

    • Roi Maor
    • , Henry Ferguson-Gow
    •  & Kate E. Jones
  3. The Steinhardt Museum of Natural History, Tel Aviv University, Tel Aviv, 6997801, Israel

    • Tamar Dayan
  4. Institute of Zoology, Zoological Society of London, Regent’s Park, London, NW1 4RY, UK

    • Kate E. Jones

Authors

  1. Search for Roi Maor in:

  2. Search for Tamar Dayan in:

  3. Search for Henry Ferguson-Gow in:

  4. Search for Kate E. Jones in:

Contributions

R.M., T.D. and K.E.J. developed the overall study design. R.M. collected and processed the data and carried out the analyses with assistance from H.F.-G. R.M. and K.E.J. led on the writing of the paper with significant contributions from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Roi Maor or Kate E. Jones.

Electronic supplementary material

  1. Supplementary Information

    Supplementary figure and table.

  2. Life Sciences Reporting Summary

  3. Supplementary Table

    Table with activity pattern data for 2415 mammalian species.