Skip to main content

Thank you for visiting 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.

The true tempo of evolutionary radiation and decline revealed on the Hawaiian archipelago


Establishing the relationship between rates of change in species richness and biotic and abiotic environmental change is a major goal of evolutionary biology. Although exquisite fossil and geological records provide insight in rare cases1, most groups lack high-quality fossil records. Consequently, biologists typically rely on molecular phylogenies to study the diversity dynamics of clades, usually by correlating changes in diversification rate with environmental or trait shifts2,3,4,5,6. However, inferences drawn from molecular phylogenies can be limited owing to the challenge of accounting for extinct species, making it difficult7,8,9 to accurately determine the underlying diversity dynamics that produce them. Here, using a geologically informed model of the relationship between changing island area and species richness for the Hawaiian archipelago, we infer the rates of species richness change for 14 endemic groups over their entire evolutionary histories without the need for fossil data, or molecular phylogenies. We find that these endemic clades underwent evolutionary radiations characterized by initially increasing rates of species accumulation, followed by slow-downs. In fact, for most groups on most islands, their time of evolutionary expansion has long past, and they are now undergoing previously unrecognized long-term evolutionary decline. Our results show how landscape dynamism can drive evolutionary dynamics over broad timescales10, including driving species loss that is not readily detected using molecular phylogenies, or without a rich fossil record11. We anticipate that examination of other clades where the relationship between environmental change and species richness change can be quantified will reveal that many other living groups have also experienced similarly complex evolutionary trajectories, including long-term and ongoing evolutionary decline.

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

Prices vary by article type



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

Figure 1: Generalized growth and decay of the Hawaiian islands used in the island ontogeny model.
Figure 2: Species numbers and inferred diversity trajectories of Hawaiian clades for the major islands of the Hawaiian archipelago.
Figure 3: Species accumulation rates inferred for the 14 clades analysed under the island ontogeny model.
Figure 4: Representative inferred diversity trajectories (grey) and carrying capacities (orange) on the oldest island, Kauai, under the island ontogeny model.


  1. 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)

    Article  CAS  ADS  PubMed  Google Scholar 

  2. Baldwin, B. G. & Sanderson, M. J. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl Acad. Sci. USA 95, 9402–9406 (1998)

    Article  CAS  ADS  PubMed  Google Scholar 

  3. Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543 (2014)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Valente, L. M., Phillimore, A. B. & Etienne, R. S. Equilibrium and non-equilibrium dynamics simultaneously operate in the Galápagos islands. Ecol. Lett . 18, 844–852 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  5. Reyes, E., Morlon, H. & Sauquet, H. Presence in Mediterranean hotspots and floral symmetry affect speciation and extinction rates in Proteaceae. New Phytol . 207, 401–410 (2015)

    Article  PubMed  Google Scholar 

  6. Onstein, R. E. et al. Evolutionary radiations of Proteaceae are triggered by the interaction between traits and climates in open habitats. Glob. Ecol. Biogeogr . 25, 1239–1251 (2016)

    Article  Google Scholar 

  7. Liow, L. H., Quental, T. B. & Marshall, C. R. When can decreasing diversification rates be detected with molecular phylogenies and the fossil record? Syst. Biol . 59, 646–659 (2010)

    Article  PubMed  Google Scholar 

  8. Quental, T. B. & Marshall, C. R. The molecular phylogenetic signature of clades in decline. PLoS ONE 6, e25780 (2011)

    Article  CAS  ADS  PubMed  PubMed Central  Google Scholar 

  9. Morlon, H., Parsons, T. L. & Plotkin, J. B. Reconciling molecular phylogenies with the fossil record. Proc. Natl Acad. Sci. USA 108, 16327–16332 (2011)

    Article  CAS  ADS  PubMed  Google Scholar 

  10. Jetz, W. & Fine, P. V. A. Global gradients in vertebrate diversity predicted by historical area-productivity dynamics and contemporary environment. PLoS Biol . 10, e1001292 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Quental, T. B. & Marshall, C. R. How the Red Queen drives terrestrial mammals to extinction. Science 341, 290–292 (2013)

    Article  CAS  ADS  PubMed  Google Scholar 

  12. MacArthur, R. H. & Wilson, E. An equilibrium theory of insular zoogeography. Int. J. Org. Evol. 17, 373–387 (1963)

    Article  Google Scholar 

  13. MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967)

  14. Warren, B. H. et al. Islands as model systems in ecology and evolution: prospects fifty years after MacArthur-Wilson. Ecol. Lett . 18, 200–217 (2015)

    Article  PubMed  Google Scholar 

  15. Rominger, A. J. et al. Community assembly on isolated islands: macroecology meets evolution. Glob. Ecol. Biogeogr . 25, 769–780 (2016)

    Article  Google Scholar 

  16. Whittaker, R. J., Triantis, K. A. & Ladle, R. J. A general dynamic theory of oceanic island biogeography. J. Biogeogr . 35, 977–994 (2008)

    Article  Google Scholar 

  17. Fattorini, S. On the general dynamic model of oceanic island biogeography. J. Biogeogr . 36, 1100–1110 (2009)

    Article  Google Scholar 

  18. Geist, D. J ., Snell, H ., Snell, H ., Goddard, C & Kurz, M. D. in The Galapagos: A Natural Laboratory for the Earth Sciences (Geophysical Monograph 204) (eds Harpp, K. S ., Mittlestaedt, E ., D’Ozouville, N . & Graham, D. W. ) 145–166 (American Geophysical Union, 2014)

  19. Borregaard, M. K. et al. Oceanic island biogeography through the lens of the general dynamic model: assessment and prospect. Biol. Rev . (2016)

  20. Lipman, P. W. & Calvert, A. T. Modeling volcano growth on the island of Hawaii: deep-water perspectives. Geosphere 9, 1348–1383 (2013)

    Article  ADS  Google Scholar 

  21. Clague, D. A. & Sherrod, D. R. Growth and degradation of Hawaiian volcanoes. U.S. Geol. Surv. Prof. Pap . 1801, 97–146 (2014)

    Google Scholar 

  22. Weigelt, P., Steinbauer, M. J., Cabral, J. S. & Kreft, H. Late Quaternary climate change shapes island biodiversity. Nature 532, 99–102 (2016)

    Article  CAS  ADS  PubMed  Google Scholar 

  23. Chen, X., Jiao, J. & Tong, X. A generalized model of island biogeography. Sci. China Life Sci . 54, 1055–1061 (2011)

    Article  PubMed  Google Scholar 

  24. Borges, P. A. V. & Hortal, J. Time, area and isolation: factors driving the diversification of Azorean arthropods. J. Biogeogr . 36, 178–191 (2009)

    Article  Google Scholar 

  25. Gillespie, R. G. & Baldwin, B. G. in The Theory of Island Biogeography Revisited (eds Losos, J. B . & Ricklefs, R. E. ) 358–387 (Princeton Univ. Press, 2010)

  26. Price, J. P. Floristic biogeography of the Hawaiian islands: influences of area, environment and paleogeography. J. Biogeogr . 31, 487–500 (2004)

    Article  Google Scholar 

  27. Price, J. P. & Wagner, W. L. A phylogenetic basis for species-area relationships among three Pacific Island floras. Am. J. Bot . 98, 449–459 (2011)

    Article  PubMed  Google Scholar 

  28. Ricklefs, R. E. & Bermingham, E. History and the species-area relationship in Lesser Antillean birds. Am. Nat . 163, 227–239 (2004)

    Article  PubMed  Google Scholar 

  29. Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001)

    Article  CAS  ADS  Google Scholar 

  30. Hall, C. A. Nearshore marine paleoclimatic regions, increasing zoogeographic provinciality, molluscan extinctions, and paleoshorelines, California: late Oligocene (27 Ma) to late Pliocene (2.5 Ma). Spec. Pap. Geol. Soc. Am. 357, 1–489 (2002)

    Google Scholar 

  31. Flinders, A. F., Ito, G. & Garcia, M. O. Gravity anomalies of the northern Hawaiian Islands: implications on the shield evolutions of Kauai and Niihau. J. Geophys. Res. Solid Earth 115, B08412 (2010)

    Article  ADS  Google Scholar 

  32. Carson, H. L & Clague, D. A. in Hawaiian Biogeography: Evolution in a Hotspot Archipelago (eds . Wagner, W. L . & Funk, V. A. ) 14–29 (Smithsonian Institution Press, 1995)

  33. Moore, J. G. & Clague, D. A. Volcano growth and evolution of the island of Hawaii. Geol. Soc. Am. Bull . 104, 1471–1484 (1992)

    Article  ADS  Google Scholar 

  34. Mark, R. K. & Moore, J. G. Slopes of the Hawaiian ridge. U.S. Geol. Surv. Prof. Pap . 1350, 101–107 (1987)

    Google Scholar 

  35. Price, J. P. & Elliott-Fisk, D. Topographic history of the Maui Nui complex, Hawai’i, and its implications for biogeography. Pacif. Sci . 58, 27–45 (2004)

    Article  Google Scholar 

  36. Triantis, K. A., Guilhaumon, F. & Whittaker, R. J. The island species-area relationship: biology and statistics. J. Biogeogr . 39, 215–231 (2012)

    Article  Google Scholar 

  37. Peck, S. B., Wigfull, P. & Nishida, G. Physical correlates of insular species diversity: the insects of the Hawaiian islands. Ann. Entomol. Soc. Am . 92, 529–536 (1999)

    Article  Google Scholar 

  38. Juvik, J. O. & Austring, A. P. The Hawaiian avifauna: biogeographic theory in evolutionary time. J. Biogeogr . 6, 205–224 (1979)

    Article  Google Scholar 

  39. Wolfram Research, I. Mathematica v.10.1 (2015)

  40. Elzhov, T. V., Mullen, K. M., Spiess, A.-N. & Bolker, B. minpack.lm: R interface to the Levenberg-Marquardt nonlinear least-squares algorithm found in MINPACK, plus support for Bounds v1.2-1 (package for R statistical software, 2016)

  41. Borchers, H. W. pracma: Practical Numerical Math Functions v1.9.9 (package for R statistical software, 2017)

  42. Maechler, M. RMPFR: Multiple Precision Floating-Point Reliable v0.6-1 (package for R statistical software, 2016)

  43. Burnham, K. P. & Anderson, D. R. Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach (Springer, 2002)

  44. Pratt, H. D. The Hawaiian Honeycreepers (Oxford Univ. Press, 2005)

  45. Magnacca, K. N. & Price, D. K. Rapid adaptive radiation and host plant conservation in the Hawaiian picture wing Drosophila (Diptera: Drosophilidae). Mol. Phylogenet. Evol . 92, 226–242 (2015)

    Article  PubMed  Google Scholar 

  46. Nishida, G. M. Hawaiian Terrestrial Arthropod Checklist (Bishop Museum Press, 2002)

  47. Hormiga, G., Arnedo, M. & Gillespie, R. G. Speciation on a conveyor belt: sequential colonization of the Hawaiian islands by Orsonwelles spiders (Araneae, Linyphiidae). Syst. Biol . 52, 70–88 (2003)

    Article  PubMed  Google Scholar 

  48. Gillespie, R. G. & Rivera, M. A. J. Free-living spiders of the genus Ariamnes (Araneae, Theridiidae) in Hawaii. J. Arachnol . 35, 11–37 (2007)

    Article  Google Scholar 

  49. Otte, D. The Crickets of Hawaii (Orthopterists’ Society, 2000)

  50. Shaw, K. L. Further acoustic diversity in Hawaiian forests: two new species of Hawaiian cricket (Orthoptera: Gryllidae: Trigoniinau: Laupala). Zool. J. Linn. Soc . 129, 73–91 (2000)

    Article  Google Scholar 

  51. Liebherr, J. K. & Zimmerman, E. C. Insects of Hawaii. Hawaiian Carabidae (Coleoptera), Part 1: Introduction and Tribe Platynini, vol. 16 (Univ. Hawai’i Press, 2000)

  52. Liebherr, J. K. & Short, A. E. Z. Blackburnia riparia, new species (Coleoptera: Carabidae, Platynini): a novel element in the Hawaiian riparian insect fauna. J. NY Entomol. Soc . 114, 1–16 (2006)

    Article  Google Scholar 

  53. Liebherr, J. K. Blackburnia gastrellariformis sp. n. (Coleoptera: Carabidae), from Molokai: successful prediction of a new taxon by reconciled tree analysis. Insect Syst. Evol . 32, 133–141 (2001)

    Article  Google Scholar 

  54. Liebherr, J. K. Recognition and description of Blackburnia kavanaughi, new species (Coleoptera: Carabidae, Platynini) from Kauai, Hawaii. J. NY Entomol. Soc . 114, 17–27 (2006)

    Article  Google Scholar 

  55. Liebherr, J. K. Blackburnia lata sp. n. (Coleoptera: Carabidae) from Kauai: morphological transformation in the arboreal microhabitat. Insect Syst. Evol . 34, 41–52 (2003)

    Article  Google Scholar 

  56. Jordan, S., Simon, C. & Polhemus, D. Molecular systematics and adaptive radiation of Hawaii’s endemic damselfly genus Megalagrion (Odonata: Coenagrionidae). Syst. Biol . 52, 89–109 (2003)

    Article  PubMed  Google Scholar 

  57. Wagner, W. L., Herbst, D. R. & Sohmer, S. H. Manual of the Flowering Plants of Hawai’i (Univ. Hawai’i Press and Bishop Museum Press, 1999)

  58. Wagner, W. L., Herbst, D. R. & Lorence, D. H. Flora of the Hawaiian Islands. (2005)

  59. Wagner, W. L., Herbst, D. R., Khan, N. & Flynn, T. Hawaiian vascular plant updates: a supplement to the manual of the flowering plants of Hawaii and Hawai’i’s ferns and fern allies (version 1.3). (Smithsonian National Museum of Natural History, 2012)

  60. Fleischer, R. C., McIntosh, C. E. & Tarr, C. L. Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K-Ar-based ages of the Hawaiian Islands to estimate molecular evolutionary rates. Mol. Ecol . 7, 533–545 (1998)

    Article  CAS  PubMed  Google Scholar 

  61. Lerner, H. R. L., Meyer, M., James, H. F., Hofreiter, M. & Fleischer, R. C. Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr. Biol . 21, 1838–1844 (2011)

    Article  CAS  PubMed  Google Scholar 

  62. Gillespie, R. G., Croom, H. B. & Hasty, G. L. Phylogenetic relationships and adaptive shifts among major clades of Tetragnatha spiders (Araneae: Tetragnathidae) in Hawai’i. Pac. Sci . 51, 380–394 (1997)

    CAS  Google Scholar 

  63. Shaw, K. L. Sequential radiations and patterns of speciation in the Hawaiian cricket genus Laupala inferred from DNA sequences. Evolution 50, 237–255 (1996)

    Article  CAS  PubMed  Google Scholar 

  64. Cryan, J. R., Liebherr, J. K., Fetzner, J. W., Jr & Whiting, M. F. Evaluation of relationships within the endemic Hawaiian Platynini (Coleoptera: Carabidae) based on molecular and morphological evidence. Mol. Phylogenet. Evol . 21, 72–85 (2001)

    Article  CAS  PubMed  Google Scholar 

  65. Givnish, T. J. et al. Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proc. R. Soc. B 276, 407–416 (2009)

    Article  PubMed  Google Scholar 

  66. Cronk, Q. C. B., Kiehn, M., Wagner, W. L. & Smith, J. F. Evolution of Cyrtandra (Gesneriaceae) in the Pacific Ocean: the origin of a supertramp clade. Am. J. Bot . 92, 1017–1024 (2005)

    Article  PubMed  Google Scholar 

  67. Clark, J. R., Wagner, W. L. & Roalson, E. H. Patterns of diversification and ancestral range reconstruction in the southeast Asian-Pacific angiosperm lineage Cyrtandra (Gesneriaceae). Mol. Phylogenet. Evol . 53, 982–994 (2009)

    Article  CAS  PubMed  Google Scholar 

  68. Nepokroeff, M., Sytsma, K. J., Wagner, W. L. & Zimmer, E. A. Reconstructing ancestral patterns of colonization and dispersal in the Hawaiian understory tree genus Psychotria (Rubiaceae): a comparison of parsimony and likelihood approaches. Syst. Biol . 52, 820–838 (2003)

    PubMed  Google Scholar 

  69. Soltis, P. S. et al. Molecular phylogenetic analysis of the Hawaiian endemics Schiedea and Alsinidendron . Am. Soc. Plant Taxon . 21, 365–379 (2016)

    Google Scholar 

  70. Willyard, A. et al. Estimating the species tree for Hawaiian Schiedea (Caryophyllaceae) from multiple loci in the presence of reticulate evolution. Mol. Phylogenet. Evol . 60, 29–48 (2011)

    Article  PubMed  Google Scholar 

  71. Lindqvist, C. & Albert, V. A. Origin of the Hawaiian endemic mints within North American Stachys (Lamiaceae). Am. J. Bot . 89, 1709–1724 (2002)

    Article  PubMed  Google Scholar 

Download references


We thank R. Gillespie, B. Baldwin, D. Clague, and M. Manga, K. Magnacca, I. Cooper, D. Polhemus, and the Berkeley Dimensions in Biodiversity research group for help with the primary biological and geological data and their interpretation. We also thank L. Chang, J. Ly, A. Jordon, M. Pires, K. Roy, R. Bowie, and S. P. Quek.

Author information

Authors and Affiliations



C.R.M. developed the analytic approach, augmented by ideas from J.Y.L. J.Y.L. developed the model comparison and statistical approaches. J.Y.L. coded the analytic approach into R, and ran all the analyses. J.Y.L. compiled the species richness data. C.R.M. compiled the island ontogeny data. C.R.M. and J.Y.L. co-wrote the manuscript.

Corresponding authors

Correspondence to Jun Y. Lim or Charles R. Marshall.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks P. Weigelt and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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

Extended data figures and tables

Extended Data Figure 1 Schematic description of the island ontogeny model.

Extended Data Figure 2 Sensitivity of the model comparison results in uncertainties in the ontogenies of the islands.

See Fig. 1 and Extended Data Table 1. For the columns labelled ‘Mean’, the mean values of the durations of growth (tgrowth), and decay (tdecay) were used; ‘Old Island’ means oldest of time of growth first habitability was used; ‘Young Island’ means youngest estimate of time of first habitability was used; ‘Longer Growth’ means youngest estimate of time of maximum area was used; ‘Shorter Growth’ means oldest estimate of time of maximum area was used. The corresponding values of r0,max and Kmax can be found in Extended Data Tables 3, 4, 5, 6, 7.

Extended Data Figure 3 Sensitivity of island ontogeny model to uncertainties in area estimates of older islands.

a, AIC weights for the island ontogeny model (x axis) plotted against the weights when the maximum areas of the two older islands (Kauai and Oahu) were increased by 60% (y axis). b, AIC weights for the island ontogeny model (x axis) plotted against the weights when the maximum areas of the two older islands were decreased by 40% (y axis). If there were no changes in the AIC weight for a clade, its data point would lie on the diagonal line.

Extended Data Table 1 Estimated time of growth (tgrowth), time of decay (tdecay), current area (Acurr), estimated area at the last glacial maximum22 (ALGM), and estimated maximum area (Amax) for the major Hawaiian islands
Extended Data Table 2 The species richness values for each of the 14 clades for each of the four major islands
Extended Data Table 3 Model parameter estimates and Akaike weights (ω) using mean times of first habitability and maximum area
Extended Data Table 4 Model parameter estimates and Akaike weights (ω) using oldest times of first habitability and youngest times of maximum area
Extended Data Table 5 Model parameter estimates and Akaike weights (ω) using oldest times of first habitability and oldest times of maximum area
Extended Data Table 6 Model parameter estimates and Akaike weights (ω) using youngest times of first habitability and youngest times of maximum area
Extended Data Table 7 Model parameter estimates and Akaike weights (ω) using youngest times of first habitability and oldest times of maximum area

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lim, J., Marshall, C. The true tempo of evolutionary radiation and decline revealed on the Hawaiian archipelago. Nature 543, 710–713 (2017).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


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.


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