Abstract
Colonization, speciation and extinction are dynamic processes that influence global patterns of species richness1,2,3,4,5,6. Island biogeography theory predicts that the contribution of these processes to the accumulation of species diversity depends on the area and isolation of the island7,8. Notably, there has been no robust global test of this prediction for islands where speciation cannot be ignored9, because neither the appropriate data nor the analytical tools have been available. Here we address both deficiencies to reveal, for island birds, the empirical shape of the general relationships that determine how colonization, extinction and speciation rates co-vary with the area and isolation of islands. We compiled a global molecular phylogenetic dataset of birds on islands, based on the terrestrial avifaunas of 41 oceanic archipelagos worldwide (including 596 avian taxa), and applied a new analysis method to estimate the sensitivity of island-specific rates of colonization, speciation and extinction to island features (area and isolation). Our model predicts—with high explanatory power—several global relationships. We found a decline in colonization with isolation, a decline in extinction with area and an increase in speciation with area and isolation. Combining the theoretical foundations of island biogeography7,8 with the temporal information contained in molecular phylogenies10 proves a powerful approach to reveal the fundamental relationships that govern variation in biodiversity across the planet.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
New sequence data produced for this study have been deposited in GenBank with the accession codes: MH307408–MH307656. The following datasets have been deposited in Mendeley: DNA alignments (https://doi.org/10.17632/vf95364vx6.1), new phylogenetic trees produced for this study (https://doi.org/10.17632/p6hm5w8s3b.2), and DAISIE R objects (https://doi.org/10.17632/sy58zbv3s2.2). The 11 previously published trees are available upon request.
Code availability
The custom computer code used for this study is freely available in the DAISIE R package (https://github.com/rsetienne/DAISIE).
References
Ricklefs, R. E. & Bermingham, E. Nonequilibrium diversity dynamics of the Lesser Antillean avifauna. Science 294, 1522–1524 (2001).
Triantis, K. A., Economo, E. P., Guilhaumon, F. & Ricklefs, R. E. Diversity regulation at macro-scales: species richness on oceanic archipelagos. Glob. Ecol. Biogeogr. 24, 594–605 (2015).
Whittaker, R. J., Triantis, K. A. & Ladle, R. J. A general dynamic theory of oceanic island biogeography. J. Biogeogr. 35, 977–994 (2008).
Kreft, H., Jetz, W., Mutke, J., Kier, G. & Barthlott, W. Global diversity of island floras from a macroecological perspective. Ecol. Lett. 11, 116–127 (2008).
Losos, J. B. & Schluter, D. Analysis of an evolutionary species–area relationship. Nature 408, 847–850 (2000).
Gillespie, R. G. & Baldwin, B. G. in The Theory of Island Biogeography Revisited (eds Losos, J. & Ricklefs, R. E.) 358–387 (Princeton Univ. Press, 2010).
MacArthur, R. H. & Wilson, E. O. An equilibrium theory of insular zoogeography. Evolution 17, 373–387 (1963).
MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967).
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).
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).
Lomolino, M. V. Species–area and species–distance relationships of terrestrial mammals in the Thousand Island Region. Oecologia 54, 72–75 (1982).
Diamond, J. M. Biogeographic kinetics: estimation of relaxation times for avifaunas of southwest Pacific islands. Proc. Natl Acad. Sci. USA 69, 3199–3203 (1972).
Whittaker, R. J. & Fernandez-Palacios, J. M. Island Biogeography: Ecology, Evolution, and Conservation (Oxford Univ. Press, 2007).
Matthews, T. J., Rigal, F., Triantis, K. A. & Whittaker, R. J. A global model of island species–area relationships. Proc. Natl Acad. Sci. USA 116, 12337–12342 (2019).
Weigelt, P., Steinbauer, M. J., Cabral, J. S. & Kreft, H. Late Quaternary climate change shapes island biodiversity. Nature 532, 99–102 (2016).
Lim, J. Y. & Marshall, C. R. The true tempo of evolutionary radiation and decline revealed on the Hawaiian archipelago. Nature 543, 710–713 (2017).
Cabral, J. S., Weigelt, P., Kissling, W. D. & Kreft, H. Biogeographic, climatic and spatial drivers differentially affect α-, β- and γ-diversities on oceanic archipelagos. Proc. R. Soc. B 281, 20133246 (2014).
Matthews, T. J., Guilhaumon, F., Triantis, K. A., Borregaard, M. K. & Whittaker, R. J. On the form of species–area relationships in habitat islands and true islands. Glob. Ecol. Biogeogr. 25, 847–858 (2016).
Simberloff, D. S. & Wilson, E. O. Experimental zoogeography of islands: the colonization of empty islands. Ecology 50, 278–296 (1969).
Russell, G. J., Diamond, J. M., Reed, T. M. & Pimm, S. L. Breeding birds on small islands: island biogeography or optimal foraging? J. Anim. Ecol. 75, 324–339 (2006).
Rabosky, D. L. & Glor, R. E. Equilibrium speciation dynamics in a model adaptive radiation of island lizards. Proc. Natl Acad. Sci. USA 107, 22178–22183 (2010).
Emerson, B. C. & Gillespie, R. G. Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol. Evol. 23, 619–630 (2008).
Kisel, Y. & Barraclough, T. G. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175, 316–334 (2010).
Triantis, K., Whittaker, R. J., Fernández-Palacios, J. M. & Geist, D. J. Oceanic archipelagos: a perspective on the geodynamics and biogeography of the World’s smallest biotic provinces. Front. Biogeogr. 8, e29605 (2016).
Santos, A. M. C. et al. Are species–area relationships from entire archipelagos congruent with those of their constituent islands? Glob. Ecol. Biogeogr. 19, 527–540 (2010).
Ricklefs, R. E. & Lovette, I. J. The roles of island area per se and habitat diversity in the species–area relationships of four Lesser Antillean faunal groups. J. Anim. Ecol. 68, 1142–1160 (1999).
Rosindell, J. & Phillimore, A. B. A unified model of island biogeography sheds light on the zone of radiation. Ecol. Lett. 14, 552–560 (2011).
Losos, J. B. & Ricklefs, R. E. Adaptation and diversification on islands. Nature 457, 830–836 (2009).
Keil, P. et al. Spatial scaling of extinction rates: theory and data reveal nonlinearity and a major upscaling and downscaling challenge. Glob. Ecol. Biogeogr. 27, 2–13 (2016).
Wilcox, B. A. & Murphy, D. D. Conservation strategy: the effects of fragmentation on extinction. Am. Nat. 125, 879–887 (1985).
Plummer, P. S. & Belle, E. R. Mesozoic tectono-stratigraphic evolution of the Seychelles microcontinent. Sediment. Geol. 96, 73–91 (1995).
Weigelt, P., Jetz, W. & Kreft, H. Bioclimatic and physical characterization of the world’s islands. Proc. Natl Acad. Sci. USA 110, 15307–15312 (2013).
Norder, S. J. et al. Beyond the Last Glacial Maximum: island endemism is best explained by long–lasting archipelago configurations. Glob. Ecol. Biogeogr. 28, 184–197 (2019).
Thomson, J. & Walton, A. Redetermination of chronology of Aldabra atoll by 230Th/234U dating. Nature 240, 145–146 (1972).
Price, J. P. & Clague, D. A. How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence. Proc. R. Soc. B 269, 2429–2435 (2002).
Valente, L. et al. Equilibrium bird species diversity in Atlantic islands. Curr. Biol. 27, 1660–1666 (2017).
del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & Kirwan, G. (eds.) Handbook of the Birds of the World Alive (Lynx Edicions, 2018).
Valente, L., Etienne, R. S. & Dávalos, L. M. Recent extinctions disturb path to equilibrium diversity in Caribbean bats. Nat. Ecol. Evol. 1, 0026 (2017).
Steadman, D. W. Extinction and Biogeography of Tropical Pacific Birds (Univ. Chicago Press, 2006).
Cheke, A. & Hume, J. P. Lost Land of the Dodo: The Ecological History of Mauritius, Réunion and Rodrigues (Bloomsbury, 2010).
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).
Rando, J. C., Pieper, H., Olson, S. L., Pereira, F. & Alcover, J. A. A new extinct species of large bullfinch (Aves: Fringillidae: Pyrrhula) from Graciosa Island (Azores, North Atlantic Ocean). Zootaxa 4282, 567–583 (2017).
Illera, J. C., Rando, J. C., Richardson, D. S. & Emerson, B. C. Age, origins and extinctions of the avifauna of Macaronesia: a synthesis of phylogenetic and fossil information. Quat. Sci. Rev. 50, 14–22 (2012).
Hume, J. P., Martill, D. & Hing, R. A terrestrial vertebrate palaeontological review of Aldabra atoll, Aldabra group, Seychelles. PLoS ONE 13, e0192675 (2018).
Cheke, A. S. Extinct birds of the Mascarenes and Seychelles—a review of the causes of extinction in the light of an important new publication on extinct birds. Phelsuma 21, 4–19 (2013).
Hume, J. P. & Walters, M. Extinct Birds (A&C Black, 2012).
Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
Bouckaert, R. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Comput. Biol. 10, e1003537 (2014).
Posada, D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256 (2008).
Weir, J. T. & Schluter, D. Calibrating the avian molecular clock. Mol. Ecol. 17, 2321–2328 (2008).
Field, D. J. et al. Timing the extant avian radiation: the rise of modern birds, and the importance of modeling molecular rate variation. PeerJ Preprints 7, e27521v1 (2019).
Cicero, C. & Johnson, N. K. Higher-level phylogeny of new world Vireos (Aves: Vireonidae) based on sequences of multiple mitochondrial DNA genes. Mol. Phylogenet. Evol. 20, 27–40 (2001).
Valente, L., Phillimore, A. B. & Etienne, R. S. Using molecular phylogenies in island biogeography: it’s about time. Ecography 41, 1684–1686 (2018).
Rabosky, D. L. Extinction rates should not be estimated from molecular phylogenies. Evolution 64, 1816–1824 (2010).
Nee, S., May, R. M. & Harvey, P. H. The reconstructed evolutionary process. Phil. Trans. R. Soc. Lond. B 344, 305–311 (1994).
Etienne, R. S. et al. Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record. Proc. R. Soc. B 279, 1300–1309 (2012).
Stervander, M. et al. Disentangling the complex evolutionary history of the Western Palearctic blue tits (Cyanistes spp.) — phylogenomic analyses suggest radiation by multiple colonization events and subsequent isolation. Mol. Ecol. 24, 2477–2494 (2015).
Ogilvie, H. A., Heled, J., Xie, D. & Drummond, A. J. Computational performance and statistical accuracy of *BEAST and comparisons with other methods. Syst. Biol. 65, 381–396 (2016).
Maddison, W. P. & Knowles, L. L. Inferring phylogeny despite incomplete lineage sorting. Syst. Biol. 55, 21–30 (2006).
Lemmon, A. R., Brown, J. M., Stanger-Hall, K. & Lemmon, E. M. The effect of ambiguous data on phylogenetic estimates obtained by maximum likelihood and Bayesian inference. Syst. Biol. 58, 130–145 (2009).
Weigelt, P. & Kreft, H. Quantifying island isolation—insights from global patterns of insular plant species richness. Ecography 36, 417–429 (2013).
Nielson, D. L. & Sibbett, B. S. Geology of Ascension Island, South Atlantic Ocean. Geothermics 25, 427–448 (1996).
Ramalho, R. S. et al. Emergence and evolution of Santa Maria Island (Azores)—the conundrum of uplifted islands revisited. Geol. Soc. Am. Bull. 129, 372–390 (2017).
Hearty, P. J. & Olson, S. L. Geochronology, biostratigraphy, and changing shell morphology in the land snail subgenus Poecilozonites during the Quaternary of Bermuda. Palaeogeogr. Palaeoclimatol. Palaeoecol. 293, 9–29 (2010).
Carracedo, J. C. & Troll, V. R. The Geology of the Canary Islands (Elsevier, 2016).
Ramalho, R. Building the Cape Verde Islands (Springer, 2011).
Eisenhauer, A., Heiss, G. A., Sheppard, C. R. C. & Dullo, W. C. in Ecology of the Chagos Archipelago (eds. Sheppard, C. R. C. & Seaward, M. R. D.) 21–31 (Linnean Society Occasional Publications, 1999).
Campbell, H. J. Fauna and flora of the Chatham Islands: less than 4 m.y. old. Geological Society of New Zealand Miscellaneous Publication 97 (eds Cooper, R. A. & Jones, C.) 15–16 (Geological Society of New Zealand, 1998).
Bullough, F. History and geology of Christmas Island. Geological Society of London Blog https://blog.geolsoc.org.uk/2013/12/18/door-18-history-and-geology-of-christmas-island/ (2013).
Castillo, P. et al. Anomalously young volcanoes on old hot-spot traces: I. Geology and petrology of Cocos Island. Geol. Soc. Am. Bull. 100, 1400–1414 (1988).
Woodroffe, C. D., Veeh, H. H., Falkland, A. C., McLean, R. F. & Wallensky, E. Last interglacial reef and subsidence of the Cocos (Keeling) Islands, Indian Ocean. Mar. Geol. 96, 137–143 (1991).
Nougier, J., Cantagrel, J. M. & Karche, J. P. The Comores archipelago in the western Indian Ocean: volcanology, geochronology and geodynamic setting. J. Afr. Earth Sci. 5, 135–144 (1986).
Almeida, F. in Sítios Geológicos e Paleontológicos do Brasil (eds Schobbenhaus, C. et al.) 361–368 (Comissão Brasileira de Sítios Geológicos e Paleobiológicos, 2000).
Ali, J. R. & Aitchison, J. C. Exploring the combined role of eustasy and oceanic island thermal subsidence in shaping biodiversity on the Galápagos. J. Biogeogr. 41, 1227–1241 (2014).
Ryan, P. G. in Encyclopedia of Islands (eds. Gillespie, R. & Clague, D.) 929–932 (Univ. California Press, 2009).
Batiza, R. Petrology and chemistry of Guadalupe Island: an alkalic seamount on a fossil ridge crest. Geology 5, 760–764 (1977).
Stuessy, T. F., Foland, K. A., Sutter, J. F., Sanders, R. W. & Silva O., M. Botanical and geological significance of potassium–argon dates from the Juan Fernandez islands. Science 225, 49–51 (1984).
McDougall, I., Embleton, B. J. J. & Stone, D. B. Origin and evolution of Lord Howe Island, Southwest Pacific Ocean. J. Geol. Soc. Aust. 28, 155–176 (1981).
Mata, J. et al. in Geologia de Portugal, Volume II Geologia Meso-cenozoica de Portugal (eds. Dias, R. et al.) 691–746 (Escolar Editora, 2013).
Guille, G. et al. Les marquises (Polynésie Françaises): un archipel intraocéanique atypique. Geol. France 2, 5–36 (2002).
Montaggioni, L. & Nativel, P. La Reunion, Ile Maurice. Géologie et Aperçus Biologiques, Plantes et Animaux (Masson, 1988).
Grandcolas, P. et al. New Caledonia: a very old Darwinian island? Phil. Trans. R. Soc. B 363, 3309–3317 (2008).
Anthoni, J. Geography and geology of Niue. http://www.seafriends.org.nz/niue/geo.htm (2005).
Jones, J. G. & McDougall, I. Geological history of Norfolk and Philip islands, southwest Pacific Ocean. J. Geol. Soc. Aust. 20, 239–254 (1973).
Suzuki, M., Taisuke, S. & Hideo, T. Nomination of the Ogasawara Islands for Inscription on the World Heritage List (Government of Japan, 2010).
Neall, V. E. & Trewick, S. A. The age and origin of the Pacific islands: a geological overview. Phil. Trans. R. Soc. B 363, 3293–3308 (2008).
Hekinian, R. et al. The Pitcairn hotspot in the South Pacific: distribution and composition of submarine volcanic sequences. J. Volcanol. Geotherm. Res. 121, 219–245 (2003).
Vezzoli, L. & Acocella, V. Easter Island, SE Pacific: an end-member type of hotspot volcanism. Bull. Geol. Soc. Am. 121, 869–886 (2009).
Gillot, P.-Y., Lefèvre, J.-C. & Nativel, P.-E. Model for the structural evolution of the volcanoes of Réunion Island. Earth Planet. Sci. Lett. 122, 291–302 (1994).
Safford, R. & Hawkins, F. The Birds of Africa: Volume VIII: The Malagasy Region: Madagascar, Seychelles, Comoros, Mascarenes (A&C Black, 2013).
Baker, I., Gale, N. H. & Simons, J. Geochronology of the St Helena volcanoes. Nature 215, 1451–1456 (1967).
Duncan, R. A. in Investigations of the Northern Melanesian Borderland, Earth Science Series (Circum Pacific Council Publications, 1985).
Lee, D. C., Halliday, A. N., Fitton, J. G. & Poli, G. Isotopic variations with distance and time in the volcanic islands of the Cameroon line: evidence for a mantle plume origin. Earth Planet. Sci. Lett. 123, 119–138 (1994).
Geldmacher, J., Hoernle, K., Van Den Bogaard, P., Zankl, G. & Garbe-Schönberg, D. Earlier history of the ≥70-Ma-old Canary hotspot based on the temporal and geochemical evolution of the Selvagen Archipelago and neighboring seamonts in the Eastern North Atlantic. J. Volcanol. Geotherm. Res. 111, 55–87 (2001).
Clouard, V. & Bonneville, A. A in Plates, Plumes and Paradigms (eds Foulger, G. R. et al.) 71–90 (Geological Society of America, 2005).
Bohrson, W. A. et al. Prolonged history of silicic peralkaline volcanism in the eastern Pacific Ocean. J. Geophys. Res. 101, 11457–11474 (1996).
Kroenke, L. W. in The Origin and Evolution of Pacific Island Biotas, New Guinea to Eastern Polynesia: Patterns and Processes (eds. Keast, A. & Miller, S.) 19–34 (SPD Academic Publishing, 1996).
Ollier, C. D. Geomorphology of South Atlantic volcanic islands. Part I: the Tristan da Cunha group. Z. Geomorphol. 28, 367–382 (1984).
Kocher, T. D. et al. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl Acad. Sci. USA 86, 6196–6200 (1989).
Dietzen, C., Witt, H.-H. & Wink, M. The phylogeographic differentiation of the European robin Erithacus rubecula on the Canary Islands revealed by mitochondrial DNA sequence data and morphometrics: evidence for a new robin taxon on Gran Canaria? Avian Sci. 3, 115–132 (2003).
Edwards, S. V., Arctander, P. & Wilson, A. C. Mitochondrial resolution of a deep branch in the genealogical tree for perching birds. Proc. R. Soc. Lond. B 243, 99–107 (1991).
Helm-Bychowski, K. & Cracraft, J. Recovering phylogenetic signal from DNA sequences: relationships within the corvine assemblage (class Aves) as inferred from complete sequences of the mitochondrial DNA cytochrome-b gene. Mol. Biol. Evol. 10, 1196–1214 (1993).
Warren, B. H., Bermingham, E., Bowie, R. C. K., Prys-Jones, R. P. & Thébaud, C. Molecular phylogeography reveals island colonization history and diversification of western Indian Ocean sunbirds (Nectarinia: Nectariniidae). Mol. Phylogenet. Evol. 29, 67–85 (2003).
Farrington, H. L., Lawson, L. P., Clark, C. M. & Petren, K. The evolutionary history of Darwin’s finches: speciation, gene flow, and introgression in a fragmented landscape. Evolution 68, 2932–2944 (2014).
Warren, B. H. et al. Hybridization and barriers to gene flow in an island bird radiation. Evolution 66, 1490–1505 (2012).
Warren, B. H., Bermingham, E., Prys-Jones, R. P. & Thebaud, C. Tracking island colonization history and phenotypic shifts in Indian Ocean bulbuls (Hypsipetes: Pycnonotidae). Biol. J. Linn. Soc. 85, 271–287 (2005).
Andersen, M. J., Hosner, P. A., Filardi, C. E. & Moyle, R. G. Phylogeny of the monarch flycatchers reveals extensive paraphyly and novel relationships within a major Australo-Pacific radiation. Mol. Phylogenet. Evol. 83, 118–136 (2015).
Sari, E. H. R. & Parker, P. G. Understanding the colonization history of the Galápagos flycatcher (Myiarchus magnirostris). Mol. Phylogenet. Evol. 63, 244–254 (2012).
Chaves, J. A., Parker, P. G. & Smith, T. B. Origin and population history of a recent colonizer, the yellow warbler in Galápagos and Cocos Islands. J. Evol. Biol. 25, 509–521 (2012).
Martínez-Gómez, J. E., Barber, B. R. & Peterson, A. T. Phylogenetic position and generic placement of the Socorro wren (Thryomanes sissonii). Auk 122, 50–56 (2005).
Warren, B. H., Bermingham, E., Prys-Jones, R. P. & Thébaud, C. Immigration, species radiation and extinction in a highly diverse songbird lineage: white-eyes on Indian Ocean islands. Mol. Ecol. 15, 3769–3786 (2006).
McGuire, J. A. et al. Molecular phylogenetics and the diversification of hummingbirds. Curr. Biol. 24, 910–916 (2014).
Derryberry, E. P. et al. Lineage diversification and morphological evolution in a large-scale continental radiation: the neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution 65, 2973–2986 (2011).
Jønsson, K. A. et al. A supermatrix phylogeny of corvoid passerine birds (Aves: Corvides). Mol. Phylogenet. Evol. 94, 87–94 (2016).
Scofield, R. P. et al. The origin and phylogenetic relationships of the New Zealand ravens. Mol. Phylogenet. Evol. 106, 136–143 (2017).
Cibois, A., Thibault, J. C., Bonillo, C., Filardi, C. E. & Pasquet, E. Phylogeny and biogeography of the imperial pigeons (Aves: Columbidae) in the Pacific Ocean. Mol. Phylogenet. Evol. 110, 19–26 (2017).
Friis, G., Aleixandre, P., Rodríguez-Estrella, R., Navarro-Sigüenza, A. G. & Milá, B. Rapid postglacial diversification and long-term stasis within the songbird genus Junco: phylogeographic and phylogenomic evidence. Mol. Ecol. 25, 6175–6195 (2016).
Marki, P. Z. et al. Supermatrix phylogeny and biogeography of the Australasian Meliphagides radiation (Aves: Passeriformes). Mol. Phylogenet. Evol. 107, 516–529 (2017).
Fuchs, J. et al. Long-distance dispersal and inter-island colonization across the western Malagasy Region explain diversification in brush-warblers (Passeriformes: Nesillas). Biol. J. Linn. Soc. 119, 873–889 (2016).
Cibois, A. et al. Phylogeny and biogeography of the fruit doves (Aves: Columbidae). Mol. Phylogenet. Evol. 70, 442–453 (2014).
Carmi, O., Witt, C. C., Jaramillo, A. & Dumbacher, J. P. Phylogeography of the vermilion flycatcher species complex: multiple speciation events, shifts in migratory behavior, and an apparent extinction of a Galápagos-endemic bird species. Mol. Phylogenet. Evol. 102, 152–173 (2016).
Cornetti, L. et al. The genome of the ‘great speciator’ provides insights into bird diversification. Genome Biol. Evol. 7, 2680–2691 (2015).
Acknowledgements
We thank the skilled guides and field assistants who helped with sample collection in the field; the ornithologists and collection curators who were kind enough to reply to requests for material; T. von Rintelen, K. von Rintelen and C. Zorn for support or advice; A. Pigot for comments on the manuscript; N. Bunbury (Seychelles Islands Foundation), who organized sample loans of Aldabra island; J. van de Crommenacke, J. Groombridge and H. Jackson for providing samples or DNA sequences; J. A. Alcover, J. C. Rando, F. Sayol and S. Faurby for sharing data on extinct species; C. Baeta, M. Hammers, J. Hume, D. Shapiro, J. Varela and P. Cascão for permission to use photographs or illustrations; P. Hearty, R. Stern and M. Reagan for expertise on island geological ages; A. Cibois, J. McGuire, H. Lerner, P. Marki, B. Milá, G. Friis, J. Fuchs, J. P. Dumbacher and O. Carmi for providing phylogenetic data; P. Weigelt for map data. We thank the following for permission to obtain new samples or to access existing samples, and for logistic support (locations are given in brackets): A. Carvalho and the Department of the Environment (São Tomé and Príncipe); J. Obiang, N. Calvo and the Universidad Nacional de Guinea Ecuatorial for Bioko and Annobón samples (Equatorial Guinea); the Ministry of Environment, Energy and Climate Change of the Republic of Seychelles, the Seychelles Bureau of Standards, BirdLife Seychelles and Seychelles Islands Foundation (Seychelles); Centre National de Documentation et de Recherche Scientifique (Grande Comore & Anjouan), Action Comores, Direction de l’Agriculture et de la Foret (Mayotte) (Comoros); Ministere des Eaux et Forets (Madagascar) and the Madagascar Institute pour la Conservation des Ecosystemes Tropicaux (Madagascar); Mauritius National Parks and Conservation Service and Mauritius Wildlife Foundation (Mauritius); O. Hébert, W. Waheoneme, N. Clark, the Direction de L’Environment (South Province), Direction du Développement Economique (Loyalty Islands Province), and local chiefs and landowners (New Caledonia); Moroccan Environment Ministry (Morocco); Cape Verde Agriculture and Environment Ministry (Cape Verde); F. Njie and the Limbe Botanical and Zoological Garden (Cameroon); Station de Recherche de l’IRET at Ipassa-Makokou (Gabon); Fernanda Lages (ISCED-Huíla) (Angola); the regional governments of Andalucía and the Canary Islands (Spain); regional governments of Madeira and the Azores (Portugal). We thank the Department of Ornithology and Mammalogy of the California Academy of Sciences (L. Wilkinson and M. Flannery) for loaning Galápagos samples; the Natural History Museum at Tring (M. Adams) for loaning Comoros samples; the Stuttgart State Museum of Natural History for loaning stonechat samples from Madagascar. S. Block assisted with cluster analyses at the Museum für Naturkunde. The Center for Information Technology of the University of Groningen provided support and access to the Peregrine high-performance computing cluster. L.V. was funded by the German Science Foundation (DFG Research grant VA 1102/1-1), the Alexander von Humboldt Foundation, the Brandenburg Postdoc Prize 2015 and by a VIDI grant from the Netherlands Organisation for Scientific Research (NWO); R.S.E. was supported by a NWO VICI grant; M.M. was supported by the Portuguese Science and Technology Foundation (post-doctoral grant: SFRH/BPD/100614/2014); S.M.C. was supported by the National Geographic Society (CRE grant 9383-13); J.C.I. was supported by the Spanish Ministry of Science, Innovation and Universities (PGC2018-097575-B-I00) and by a GRUPIN research grant from the Regional Government of Asturias (IDI/2018/000151); and C.T. was supported by the ‘Laboratoire d’Excellence’ TULIP (ANR-10-LABX-41).
Author information
Authors and Affiliations
Contributions
L.V., A.B.P. and R.S.E. designed the study, developed the analytical framework and performed statistical analyses. L.V. compiled the data, conducted most of the analyses and wrote the first draft. R.S.E. developed the likelihood method. A.B.P. and R.S.E. contributed substantially to the writing. M.M., B.H.W., S.M.C., J.C.I. and C.T. provided expertise on island birds, collected bird tissue samples, and provided molecular and/or phylogenetic data. K.H. and J.C.I. performed laboratory work. R.T. contributed to molecular analyses. T.A. performed analyses. All authors commented on the draft.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature thanks Thomas Matthews, Kostas Triantis, Jason Weir 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 Fig. 1 Variation of cladogenesis with isolation and area.
Contour plot showing how the local rate of cladogenesis varies with area and Dm assuming the maximum-likelihood global hyperparameters of the M19 model (equations describing the relationships are provided in Supplementary Table 1). Numbers correspond to the archipelago numbers from Fig. 1 and show the local cladogenesis rates for each of the archipelagos in our dataset. Area is shown as a log scale.
Extended Data Fig. 2 Bootstrap precision estimates of the parameters of the M19 model.
Parametric bootstrap analysis fitting the M19 model to 1,000 global datasets simulated with maximum-likelihood parameters of the M19 model. Plots are frequency histograms of estimated parameters. Black lines show the median estimated values across all simulations and the blue lines the simulated values. Dashed lines show 2.5–97.5 percentiles. Parameters are explained in Supplementary Table 1. Bootstrap parameter estimates for the M14 model are shown in Extended Data Table 5.
Extended Data Fig. 3 Randomization analysis of the M19 model.
Distribution of global hyperparameters estimated from each of 1,000 datasets with the same phylogenetic data as our main global dataset but randomly reshuffling archipelago area and isolation among the 41 archipelagos in the dataset. Grey histograms show DAISIE maximum-likelihood parameter estimates for the M19 model. Red arrows show the estimated parameter from the real data. In most cases, the hyperparameters describing the exponent of the power models (x, α, β and d0) are estimated as zero in the reshuffled datasets, which is not the case in the real data (red). Parameters are explained in Supplementary Table 1.
Extended Data Fig. 4 Goodness of fit of the preferred model (M19).
Plots show the observed total number of species, cladogenetic species and colonizations versus those simulated by the model. Median and 95% percentiles are shown for 1,000 simulations of each archipelago. Selected archipelagos mentioned in the main text or well-known archipelagos for which one or more of the diversity metrics are under- or overestimated are highlighted in colour. Dashed line is y = x. See also Fig. 3.
Extended Data Fig. 5 Ratio of pseudo-R2 observed over pseudo-R2 simulated.
Estimates were based on 10,000 datasets simulated using the M19 model. A ratio centred on 1 would indicate that the model explains the observed data as well as it is able to explain the average dataset simulated under the maximum-likelihood parameters.
Extended Data Fig. 6 Sensitivity to colonization and branching times.
a, Maximum-likelihood parameter estimates of the M19 model (preferred model) for datasets differing in colonization and branching times. D6 represents 100 datasets, therefore, the 2.5 and 97.5 percentiles are shown. Parameter symbols are described in Supplementary Table 1. b, Estimated relationships between island area and isolation and local island biogeography parameters for each dataset. Under the M19 model, cladogenesis rate increases with both area and isolation, and thus plots for more (far, 5,000 km) and less (near, 50 km) isolated islands are shown.
Supplementary information
Supplementary Tables
This file contains Supplementary Tables 1-7.
Supplementary Data 1
| Island birds database Includes the database of taxa of our focal group found on each of the 41 archipelagos.
Supplementary Data 2
| Full archipelago data Includes physical data, species richness and sampling (from the focal group of taxa) for the 41 archipelagos included in this study.
Supplementary Data 3
| Sensitivity to archipelago selection and isolation metrics Results of the sensitivity analyses excluding single islands, using different isolation metrics and with Mascarenes fused as a single archipelago.
Rights and permissions
About this article
Cite this article
Valente, L., Phillimore, A.B., Melo, M. et al. A simple dynamic model explains the diversity of island birds worldwide. Nature 579, 92–96 (2020). https://doi.org/10.1038/s41586-020-2022-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41586-020-2022-5
This article is cited by
-
The macroevolutionary impact of recent and imminent mammal extinctions on Madagascar
Nature Communications (2023)
-
Undiscovered bird extinctions obscure the true magnitude of human-driven extinction waves
Nature Communications (2023)
-
The relationship between geographic range size and rates of species diversification
Nature Communications (2023)
-
Passive acoustic monitoring in difficult terrains: the case of the Principe Scops-Owl
Biodiversity and Conservation (2023)
-
Geographic range size and speciation in honeyeaters
BMC Ecology and Evolution (2022)
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.