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

Nature Ecology & Evolution volume 1, pages 1889–1895 (2017)Cite this article

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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.

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Fig. 1: Activity pattern distributions across the SF and LF estimates of mammalian evolution.
Fig. 2: PP density of ancestral activity pattern reconstructions of the MRCA of crown-group Mammalia from SF and LF phylogenies.
Fig. 3: Reconstruction of ancestral activity patterns and character accumulation across the SF hypothesis of mammalian evolution.
Fig. 4: Reconstruction of ancestral activity patterns and character accumulation across the LF hypothesis of mammalian evolution.

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References

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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. 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).

    Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  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. 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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  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).

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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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.).

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Authors and 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

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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.

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Correspondence to Roi Maor or Kate E. Jones.

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Table with activity pattern data for 2415 mammalian species.

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Maor, R., Dayan, T., Ferguson-Gow, H. et al. Temporal niche expansion in mammals from a nocturnal ancestor after dinosaur extinction. Nat Ecol Evol 1, 1889–1895 (2017). https://doi.org/10.1038/s41559-017-0366-5

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