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.

Hurricane-induced selection on the morphology of an island lizard

Nature volume 560, pages 88–91 (2018)Cite this article

Subjects

Abstract

Hurricanes are catastrophically destructive. Beyond their toll on human life and livelihoods, hurricanes have tremendous and often long-lasting effects on ecological systems1,2. Despite many examples of mass mortality events following hurricanes3,4,5, hurricane-induced natural selection has not previously been demonstrated. Immediately after we finished a survey of Anolis scriptus—a common, small-bodied lizard found throughout the Turks and Caicos archipelago—our study populations were battered by Hurricanes Irma and Maria. Shortly thereafter, we revisited the populations to determine whether morphological traits related to clinging capacity had shifted in the intervening six weeks and found that populations of surviving lizards differed in body size, relative limb length and toepad size from those present before the storm. Our serendipitous study, which to our knowledge is the first to use an immediately before and after comparison6 to investigate selection caused by hurricanes, demonstrates that hurricanes can induce phenotypic change in a population and strongly implicates natural selection as the cause. In the decades ahead, as extreme climate events are predicted to become more intense and prevalent7,8, our understanding of evolutionary dynamics needs to incorporate the effects of these potentially severe selective episodes9,10,11.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Fig. 1: Location of Pine Cay and Water Cay with respect to Hurricanes Irma and Maria.
Fig. 2: Parallel shifts in body-size-corrected humerus and femur length and surface area of the forelimb and hindlimb toepads for lizards on both Pine Cay and Water Cay.

References

  1. Walker, L. R., Lodge, D. J., Brokaw, N. V. L. & Walde, R. B. An introduction to hurricanes in the Caribbean. Biotropica 23, 313–316 (1991).

    Article  Google Scholar 

  2. Scalley, T. H., Scatena, F. N., Lugo, A. E., Moya, S. & Estrada Rulz, C. R. Changes in structure, composition, and nutrients during 15 years of hurricane-induced succession in a subtropical wet forest in Puerto Rico. Biotropica 42, 455–463 (2010).

    Article  Google Scholar 

  3. Pavelka, M. S. M., McGoogan, K. & Steffens, T. S. Population size and characteristics of Alouatta pigra before and after a major hurricane. Int. J. Primatol. 28, 919–929 (2007).

    Article  Google Scholar 

  4. Willig, M. R. & Camilo, G. R. The effect of Hurricane Hugo on six invertebrate species in the Luquillo experimental forest of Puerto Rico. Biotropica 23, 455–461 (1991).

    Article  Google Scholar 

  5. Wiley, J. W. & Wunderle, J. M. The effects of hurricanes on birds, with special reference to Caribbean islands. Bird Conserv. Int. 3, 319–349 (1993).

    Article  Google Scholar 

  6. Endler, J. A. Natural Selection in the Wild (Princeton Univ. Press, Princeton, 1986).

    Google Scholar 

  7. Hegerl, G. C., Hanlon, H. & Beierkuhnlein, C. Climate science: elusive extremes. Nat. Geosci. 4, 142–143 (2011).

    Article  ADS  CAS  Google Scholar 

  8. Ummenhofer, C. C. & Meehl, G. A. Extreme weather and climate events with ecological relevance: a review. Phil. Trans. R. Soc. B 372, 20160135 (2017).

    Article  PubMed  Google Scholar 

  9. Grant, P. R. Evolution, climate change, and extreme events. Science 357, 451–452 (2017).

    Article  ADS  PubMed  CAS  Google Scholar 

  10. van de Pol, M., Jenouvrier, S., Cornelissen, J. H. C. & Visser, M. E. Behavioral, ecological and evolutionary responses to extreme climactic events: challenges and directions. Phil. Trans. R. Soc. B 372, 20160134 (2017).

    Article  PubMed  Google Scholar 

  11. Grant, P. R. et al. Evolution caused by extreme events. Phil. Trans. R. Soc. B 372, 20160146 (2017).

    Article  ADS  PubMed  Google Scholar 

  12. Johnson, A. B. & Winker, K. Short-term hurricane impacts on a neotropical community of marked birds and implications for early-stage community resilience. PLoS ONE 5, e15109 (2010).

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  13. Lodge, D. J. & McDowell, W. H. Summary of ecosystem-level effects of Caribbean hurricanes. Biotropica 23, 373–378 (1991).

    Article  Google Scholar 

  14. Batista, W. B. & Platt, W. J. Tree population responses to hurricane disturbance: syndromes in a south-eastern USA old-growth forest. J. Ecol. 91, 197–212 (2003).

    Google Scholar 

  15. Wulff, J. L. Effects of a hurricane on survival and orientation of large erect coral reef sponges. Coral Reefs 14, 55–61 (1995).

    Article  ADS  Google Scholar 

  16. Spiller, D. A., Losos, J. B. & Schoener, T. W. Impact of a catastrophic hurricane on island populations. Science 281, 695–697 (1998).

    Article  ADS  PubMed  CAS  Google Scholar 

  17. Crandell, K. E., Herrel, A., Sasa, M., Losos, J. B. & Autumn, K. Stick or grip? Co-evolution of adhesive toepads and claws in Anolis lizards. Zoology 117, 363–369 (2014).

    Article  PubMed  Google Scholar 

  18. Kolbe, J. Effects of hind-limb length and perch diameter on clinging performance in Anolis lizards from the British Virgin Islands. J. Herp. 49, 284–290 (2015).

    Article  Google Scholar 

  19. Losos, J. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles (Univ. of California Press, Berkeley, 2009).

    Google Scholar 

  20. Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).

    Article  PubMed  CAS  Google Scholar 

  21. Kingsolver, J. G. & Diamond, S. E. Phenotypic selection in natural populations: what limits directional selection? Am. Nat. 177, 346–357 (2011).

    Article  PubMed  Google Scholar 

  22. Siepielski, A. M., DiBattista, J. D. & Carlson, S. M. It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 12, 1261–1276 (2009).

    Article  PubMed  Google Scholar 

  23. Grant, P. R. & Grant, B. R. Evolution of character displacement in Darwin’s finches. Science 313, 224–226 (2006).

    Article  ADS  PubMed  CAS  Google Scholar 

  24. Forsman, A. Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity 115, 276–284 (2015).

    Article  PubMed  CAS  Google Scholar 

  25. Losos, J. B. et al. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54, 301–305 (2000).

    PubMed  CAS  Google Scholar 

  26. Kolbe, J. J. & Losos, J. B. Hind-limb length plasticity in Anolis carolinensis. J. Herp. 39, 674–678 (2005).

    Article  Google Scholar 

  27. Wikelski, M. & Thom, C. Marine iguanas shrink to survive El Niño. Nature 403, 37–38 (2000).

    Article  ADS  PubMed  CAS  Google Scholar 

  28. Stuart, Y. E. et al. Rapid evolution of a native species following invasion by a congener. Science 346, 463–466 (2014).

    Article  ADS  PubMed  CAS  Google Scholar 

  29. Lázaro, J., Dechmann, D. K. N., LaPoint, S., Wikelski, M. & Hertel, M. Profound reversible seasonal changes of individual skull size in a mammal. Curr. Biol. 27, R1106–R1107 (2017).

    Article  PubMed  CAS  Google Scholar 

  30. Schoener, T. W., Kolbe, J. J., Leal, M., Losos, J. B. & Spiller, D. A. A multigenerational field experiment on eco-evolutionary dynamics of the influential lizard Anolis sagrei: a mid-term report. Copeia 105, 543–549 (2017).

    Article  Google Scholar 

  31. Macrini, T. E., Irschick, D. J. & Losos, J. B. Ecomorphological differences in toepad characteristics between mainland and island anoles. J. Herp. 37, 52–58 (2003).

    Article  Google Scholar 

  32. Laska, A. L. The structural niche of Anolis scriptus on Inagua. Breviora 349, 1–6 (1970).

    Google Scholar 

  33. Kamath, A. & Losos, J. B. Does ecological specialization transcend scale? Habitat partitioning among individuals and species of Anolis lizards. Evolution 71, 541–549 (2017).

    Article  PubMed  Google Scholar 

  34. Spendelow, P. Niche Width and Morphological Variation (Anole). PhD thesis, Univ. of Washington (1985).

  35. Irschick, D. J., Vanhooydonck, B., Herrel, A. & Meyers, J. Intraspecific correlations among morphology, performance and habitat use within a green anole lizard (Anolis carolinensis) population. Biol. J. Linn. Soc. 85, 211–221 (2005).

    Article  Google Scholar 

  36. R Core Team. R: A Language and Environment for Statistical Computing http://www.R-project.org/ (R Foundation for Statistical Computing, Vienna, 2017).

    Google Scholar 

  37. Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was made possible thanks to the Pine Cay Homeowners Association and the US National Science Foundation. All procedures were approved by the Turks and Caicos DECR (Initial Permit: 17-08-02-14; Revisit Permit: 17-10-01-15) and Harvard University IACUC (26-11). We thank C. Santoro for help in the field and with the manuscript, and members of the Losos laboratory for valuable feedback. A.H. thanks the Caribaea Initiative for promoting science in the Caribbean and facilitating the networking that made the initial Turks and Caicos study possible.

Reviewer information

Nature thanks E. Palkovacs and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

  1. Harvard University, Department of Organismic and Evolutionary Biology, Cambridge, MA, USA

    Colin M. Donihue & Anthony J. Geneva

  2. UMR 7179 CNRS/MNHN, Département Adaptations du Vivant, Paris, France

    Colin M. Donihue, Anthony Herrel & Anne-Claire Fabre

  3. Ghent University, Department of Biology, Evolutionary Morphology of Vertebrates, Ghent, Belgium

    Anthony Herrel

  4. University of Antwerp, Department of Biology, Functional Morphology, Antwerp, Belgium

    Anthony Herrel

  5. University of California, Department of Ecology, Evolution, and Marine Biology, Santa Barbara, CA, USA

    Ambika Kamath

  6. University of California, Department of Evolution and Ecology, Davis, CA, USA

    Thomas W. Schoener

  7. University of Rhode Island, Department of Biological Sciences, Kingston, RI, USA

    Jason J. Kolbe

  8. Washington University, Department of Biology, St. Louis, MO, USA

    Jonathan B. Losos

Authors
  1. Colin M. Donihue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony Herrel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne-Claire Fabre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ambika Kamath
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anthony J. Geneva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thomas W. Schoener
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jason J. Kolbe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jonathan B. Losos
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.M.D., A.H., J.J.K. and J.B.L. conceived the study; C.M.D., A.H. and A.-C.F. conducted fieldwork; C.M.D., A.J.G., A.-C.F. and A.K. conducted analyses; C.M.D. and J.B.L. wrote the initial draft of the manuscript; and T.W.S., J.J.K., A.H., A.-C.F., A.J.G. and A.K. all contributed to interpretation of the data and to editing of subsequent drafts of the manuscript.

Corresponding author

Correspondence to Colin M. Donihue.

Additional information

Competing interests: The authors declare no competing interests.

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

Supplementary information

Supplementary Information

This file contains: (1) Description of lizard behaviour on a perch in hurricane-force winds; (2) Additional analysis details and results; and (3) Variance estimates.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Donihue, C.M., Herrel, A., Fabre, AC. et al. Hurricane-induced selection on the morphology of an island lizard. Nature 560, 88–91 (2018). https://doi.org/10.1038/s41586-018-0352-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-018-0352-3

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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