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.

Island biogeography of marine organisms

Abstract

Studies on the distribution and evolution of organisms on oceanic islands have advanced towards a dynamic perspective1, where terrestrial endemicity results from island geographical aspects and geological history2 intertwined with sea-level fluctuations3,4. Diversification on these islands may follow neutral models5, decreasing over time as niches are filled6, or disequilibrium states7 and progression rules8, where richness and endemism rise with the age of the archipelago owing to the splitting of ancestral lineages (cladogenesis). However, marine organisms have received comparatively little scientific attention. Therefore, island and seamount evolutionary processes in the aquatic environment remain unclear9. Here we analyse the evolutionary history of reef fishes that are endemic to a volcanic ridge of seamounts and islands to understand their relations to island evolution and sea-level fluctuations. We also test how this evolutionary history fits island biogeography theory. We found that most endemic species have evolved recently (Pleistocene epoch), during a period of recurrent sea-level changes and intermittent connectivity caused by repeated aerial exposure of seamounts, a finding that is consistent with an ephemeral ecological speciation process10. Similar to findings for terrestrial biodiversity7, our data suggest that the marine speciation rate on islands is negatively correlated with immigration rate. However, because marine species disperse better than terrestrial species, most niches are filled by immigration: speciation increases with the random accumulation of species with low dispersal ability, with few opportunities for in situ cladogenesis and adaptive radiation. Moreover, we confirm that sea-level fluctuations and seamount location play a critical role in marine evolution, mainly by intermittently providing stepping stones for island colonization.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: VTC in the southwestern Atlantic Ocean.
Figure 2: Origin of endemic reef fishes from the VTC, southwestern Atlantic Ocean.
Figure 3: Median-joining network for endemic reef fishes and respective mainland sister taxa.
Figure 4: Model of island biogeography and evolution of marine species.

Accession codes

Primary accessions

NCBI Reference Sequence

References

  1. 1

    Fernández-Palacios, J. M. Island biogeography: shaped by sea-level shifts. Nature 532, 42–43 (2016)

    ADS  Article  Google Scholar 

  2. 2

    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 

  3. 3

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

    CAS  ADS  Article  Google Scholar 

  4. 4

    Fernández-Palacios, J. M. et al. Towards a glacial-sensitive model of island biogeography. Glob. Ecol. Biogeogr. 25, 817–830 (2016)

    Article  Google Scholar 

  5. 5

    Rosindell, J., Hubbell, S. P. & Etienne, R. S. The unified neutral theory of biodiversity and biogeography at age ten. Trends Ecol. Evol. 26, 340–348 (2011)

    Article  Google Scholar 

  6. 6

    Kopp, M. Speciation and the neutral theory of biodiversity: modes of speciation affect patterns of biodiversity in neutral communities. BioEssays 32, 564–570 (2010)

    Article  Google Scholar 

  7. 7

    Heaney, L. R. Dynamic disequilibrium: a long-term, large-scale perspective on the equilibrium model of island biogeography. Glob. Ecol. Biogeogr. 9, 59–74 (2000)

    Article  Google Scholar 

  8. 8

    Shaw, K. L. & Gillespie, R. G. Comparative phylogeography of oceanic archipelagos: hotspots for inferences of evolutionary process. Proc. Natl Acad. Sci. USA 113, 7986–7993 (2016)

    CAS  Article  Google Scholar 

  9. 9

    Dawson, M. N. Island and island-like marine environments. Glob. Ecol. Biogeogr. 25, 831–846 (2016)

    Article  Google Scholar 

  10. 10

    Cutter, A. D. & Gray, J. C. Ephemeral ecological speciation and the latitudinal biodiversity gradient. Evolution 70, 2171–2185 (2016)

    Article  Google Scholar 

  11. 11

    Losos, J. B. & Ricklefs, R. E. Adaptation and diversification on islands. Nature 457, 830–836 (2009)

    CAS  ADS  Article  Google Scholar 

  12. 12

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

  13. 13

    Hubbell, S. P. (ed.) in The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, 2001)

  14. 14

    Sandin, S. A., Vermeij, M. J. A. & Hurlbert, A. H. Island biogeography of Caribbean coral reef fish. Glob. Ecol. Biogeogr. 17, 770–777 (2008)

    Article  Google Scholar 

  15. 15

    Hachich, N. F. et al. Island biogeography: patterns of marine shallow-water organisms in the Atlantic Ocean. J. Biogeogr. 42, 1871–1882 (2015)

    Article  Google Scholar 

  16. 16

    Ludt, W. B. & Rocha, L. A. Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. J. Biogeogr. 42, 25–38 (2015)

    Article  Google Scholar 

  17. 17

    Macieira, R. M., Simon, T., Pimentel, C. R. & Joyeux, J.-C. Isolation and speciation of tidepool fishes as a consequence of Quaternary sea-level fluctuations. Environ. Biol. Fishes 98, 385–393 (2015)

    Article  Google Scholar 

  18. 18

    Rosindell, J. & Phillimore, A. B. A unified model of island biogeography sheds light on the zone of radiation. Ecol. Lett. 14, 552–560 (2011)

    Article  Google Scholar 

  19. 19

    Borregaard, M. K. et al. Oceanic island biogeography through the lens of the general dynamic model: assessment and prospect. Biol. Rev. Camb. Philos. Soc. 92, 830–853 (2017)

    Article  Google Scholar 

  20. 20

    Luiz, O. J. et al. Adult and larval traits as determinants of geographic range size among tropical reef fishes. Proc. Natl Acad. Sci. USA 110, 16498–16502 (2013)

    CAS  ADS  Article  Google Scholar 

  21. 21

    Motoki, A., Motoki, K. F. & Melo, D. P. Caracterização da morfologia submarina da cadeia Vitória–Trindade e áreas adjacentes, ES, com base na batimetria predita do topo versão 14.1. Rev. Bras. Geomorfol. 13, 151–170 (2012)

    Article  Google Scholar 

  22. 22

    Bowen, B. W., Rocha, L. A., Toonen, R. J. & Karl, S. A. The origins of tropical marine biodiversity. Trends Ecol. Evol. 28, 359–366 (2013)

    Article  Google Scholar 

  23. 23

    Floeter, S. R. et al. Atlantic reef fish biogeography and evolution. J. Biogeogr. 35, 22–47 (2008)

    Google Scholar 

  24. 24

    Gaither, M. R. & Rocha, L. A. Origins of species richness in the Indo–Malay–Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. J. Biogeogr. 40, 1638–1648 (2013)

    Article  Google Scholar 

  25. 25

    Gaither, M. R. et al. Genomic signatures of geographic isolation and natural selection in coral reef fishes. Mol. Ecol. 24, 1543–1557 (2015)

    CAS  MathSciNet  Article  Google Scholar 

  26. 26

    Pinheiro, H. T. et al. Fish biodiversity of the Vitória–Trindade Seamount Chain, southwestern Atlantic: an updated database. PLoS ONE 10, e0118180 (2015)

    Article  Google Scholar 

  27. 27

    Weigt, L. A. et al. Using DNA barcoding to assess Caribbean reef fish biodiversity: expanding taxonomic and geographic coverage. PLoS ONE 7, e41059 (2012)

    CAS  ADS  Article  Google Scholar 

  28. 28

    Rocha, L. A., Pinheiro, H. T. & Gasparini, J. L. Description of Halichoeres rubrovirens, a new species of wrasse (Labridae: Perciformes) from the Trindade and Martin Vaz Island group, southeastern Brazil, with a preliminary mtDNA molecular phylogeny of New World Halichoeres. Zootaxa 2422, 22–30 (2010)

    Article  Google Scholar 

  29. 29

    Robertson, D. R., Karg, F., Leao de Moura, R., Victor, B. C. & Bernardi, G. Mechanisms of speciation and faunal enrichment in Atlantic parrotfishes. Mol. Phylogenet. Evol. 40, 795–807 (2006)

    Article  Google Scholar 

  30. 30

    Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods) v.4.0a136 (2003)

  31. 31

    Lessios, H. A. The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annu. Rev. Ecol. Evol. Syst. 39, 63–91 (2008)

    Article  Google Scholar 

  32. 32

    Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983)

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33

    Fu, Y.-X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X. & Rozas, R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497 (2003)

    CAS  Article  Google Scholar 

  35. 35

    Bernardi, G. & Lape, J. Tempo and mode of speciation in the Baja California disjunct fish species Anisotremus davidsonii. Mol. Ecol. 14, 4085–4096 (2005)

    Article  Google Scholar 

Download references

Acknowledgements

We thank our colleagues that contributed to the studies on the VTC: E. Mazzei, J. B. Teixeira, L. B. Xavier, C. R. Pimentel, R. L. Moura, G. M. Amado-Filho, A. Carvalho-Filho, A. C. Braga, P. A. S. Costa, B. P. Ferreira, C. E. L. Ferreira, S. R. Floeter, R. B. Francini-Filho, A. S. Martins, G. Olavo, I. Sazima; J. B. Teixeira and S. Lacoste for helping with illustrations of Figs 1 and 4, respectively. CNPq (grant 470725/2009-5, 557043/2009-3 and 405426/2012-7) and Fundação O Boticário (grant 0938_20121) provided funding for the research. We are grateful for the support of donors who endorsed the California Academy of Sciences’ Hope for Reefs initiative and helped to make this publication possible. H.T.P. received a doctoral fellowship from CNPq (Ciência sem Fronteiras; GDE 202475/ 2011-5) and support from the EEB/UCSC department; T.S. and R.M.M. were recipients of CAPES (http://capes.gov.br) fellowships.

Author information

Affiliations

Authors

Contributions

H.T.P., T.S., J.-C.J., R.M.M., J.L.G., G.B. and L.A.R. designed the study; H.T.P., T.S., J.-C.J., R.M.M. and J.L.G. collected the data; H.T.P. and C.R. performed the molecular work; H.T.P., G.B. and L.A.R. analysed the data; H.T.P. wrote the paper. Photos in Fig. 3 were taken by R.M.M., J.-C.J. and T.S. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Hudson T. Pinheiro.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks J.-M. Fernandez-Palacios and K. Triantis 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 Table 1 Distribution and ecological traits of the endemic reef fishes of the VTC, south Atlantic Ocean
Extended Data Table 2 Summary statistics for endemics of the VTC and mainland sister species based on the mtDNA concatenated datasets
Extended Data Table 3 Genetic divergence and ages ranges of COI and CytB genes

Supplementary information

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pinheiro, H., Bernardi, G., Simon, T. et al. Island biogeography of marine organisms. Nature 549, 82–85 (2017). https://doi.org/10.1038/nature23680

Download citation

Further reading

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

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