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Island biogeography of marine organisms

Nature volume 549, pages 82–85 (2017)Cite this article

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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.

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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.

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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.

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Author notes

  1. Thiony Simon: Deceased.

Authors and Affiliations

  1. California Academy of Sciences, San Francisco, 94118, California, USA

    Hudson T. Pinheiro, Claudia Rocha & Luiz A. Rocha

  2. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 95060, California, Santa Cruz, USA

    Hudson T. Pinheiro & Giacomo Bernardi

  3. Departamento de Oceanografia e Ecologia, Universidade Federal do Espírito Santo, Vitória, 29075-910, Espírito Santo, Brazil

    Hudson T. Pinheiro, Thiony Simon, Jean-Christophe Joyeux, Raphael M. Macieira & João Luiz Gasparini

  4. Complexo Biopráticas, Universidade Vila Velha, Vila-Velha, 29102-770, Espírito Santo, Brazil

    Raphael M. Macieira

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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.

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The authors declare no competing financial interests.

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Reviewer Information Nature thanks J.-M. Fernandez-Palacios and K. Triantis for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Table 1 Distribution and ecological traits of the endemic reef fishes of the VTC, south Atlantic Ocean
Full size table
Extended Data Table 2 Summary statistics for endemics of the VTC and mainland sister species based on the mtDNA concatenated datasets
Full size table
Extended Data Table 3 Genetic divergence and ages ranges of COI and CytB genes
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Pinheiro, H., Bernardi, G., Simon, T. et al. Island biogeography of marine organisms. Nature 549, 82–85 (2017). https://doi.org/10.1038/nature23680

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