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A historical stepping-stone path for an island-colonizing cactus across a submerged “bridge” archipelago

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Abstract

Here we use population genomic data (ddRAD-Seq) and ecological niche modeling to test biogeographic hypotheses for the divergence of the island-endemic cactus species Cereus insularis Hemsl. (Cereeae; Cactaceae) from its sister species C. fernambucensis Lem. The Cereus insularis grows in the Fernando de Noronha Islands (FNI), a Neotropical archipelago located 350 km off the Brazilian Atlantic Forest (BAF) coast. Phylogeographic reconstructions support a northward expansion by the common ancestor of C. insularis and C. fernambucensis along the mainland BAF coast, with C. insularis diverging from the widespread mainland taxon C. fernambucensis after colonizing FNI in the late Pleistocene. The morphologically distinct C. insularis is monophyletic and nested within C. fernambucensis, as expected from a progenitor-derivative speciation model. We tested alternative biogeographic and demographic hypotheses for the colonization of the FNI using Approximate Bayesian Computation. We found the greatest support for a stepping-stone path that emerged during periods of decreased sea level (the “bridge” hypothesis), in congruence with historical ecological niche modeling that shows highly suitable habitats on stepping-stone islands during glacial periods. The outlier analyses reveal signatures of selection in C. insularis, suggesting a putative role of adaptation driving rapid anagenic differentiation of this species in FNI.

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Fig. 1: Map of eastern Brazil highlighting the study area and the locations of Cereus sampled during this study (details in Table S1).
Fig. 2: Demographic models compared to test alternative scenarios for colonization of FNI by C. insularis.
Fig. 3: Phylogeography and population structure.
Fig. 4: Highlights of the Ecological niche modeling (ENM) of Cereus fernambucensis and C. insularis (first and second columns, respectively).
Fig. 5: Global sea-level change during the last 120 ka (adapted from Rijsdijk et al. 2014).

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Acknowledgements

We thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for a visiting scholar fellowship to FFF (2019/10341-6) to a stay at Columbia University, NY (Feb/Mar 2020). This work was supported by grants from FAPESP to FFF (2014/25227-0 and 2020/15161-3) and to IASB (2020/16162-3); and from the National Council for Scientific and Technological Development (CNPq) (402209/2016-8 to FFF). We thank the fellowships from CNPq to EMM (303940/2019-0) and DCZ (305301/2018-7), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES, Finance Code 001) to DTA. For sampling Cereus insularis, we had support from Fernando de Noronha Marine National Park (ICMBIO/PARNAMAR) and the governmental administration of Fernando de Noronha (DEFN). We thank the three anonymous reviewers for their critical comments on the paper.

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Author notes

  1. These authors contributed equally: Fernando Faria Franco, Danilo Trabuco Amaral.

Authors and Affiliations

  1. Departamento de Biologia. Centro de Ciências Humanas e Biológicas, Universidade Federal de São Carlos (UFSCar), Sorocaba, Brazil

    Fernando Faria Franco, Evandro Marsola Moraes & Nigel Paul Taylor

  2. Centro de Ciências Naturais e Humanas, Universidade Federal do ABC (UFABC), Santo André, São Paulo, Brazil

    Danilo Trabuco Amaral

  3. Programa de Pós Graduação em Biologia Comparada. Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo (USP), Ribeirão Preto, Brazil

    Danilo Trabuco Amaral

  4. Instituto de Ciências Ambientais, Químicas e Farmacêuticas. Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Paulo, Diadema, SP, Brazil

    Isabel A. S. Bonatelli

  5. Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, NY, 10027, USA

    Jared B. Meek & Deren A. R. Eaton

  6. Programa de Pós Graduação em Botânica, Instituto de Ciências Biológicas, Universidade de Brasília, PO Box 04457, Brasília, DF, 70910970, Brazil

    Daniela Cristina Zappi

Authors
  1. Fernando Faria Franco
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Contributions

FFF, DTA and DE conceived the idea. DE, DTA, FFF, JM and IASB performed data collection and analyses. FFF and DE led the writing. DZ, EMM, NT, DTA and IASB contributed to many conceptions and writing. All authors contributed to the intellectual development of the paper, made multiple revisions, and approved the final draft. Funding acquisition, FFF.

Corresponding author

Correspondence to Fernando Faria Franco.

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Competing interests

The authors declare no competing interests.

Ethics approval

Sampling was carried out in accordance with Brazilian law through special permits provided to FFF (permit from Chico Mendes Biodiversity Conservation Institute, SISBIO n° 38141-1).

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Associate editor: Dario Grattapaglia.

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Franco, F.F., Amaral, D.T., Bonatelli, I.A.S. et al. A historical stepping-stone path for an island-colonizing cactus across a submerged “bridge” archipelago. Heredity (2024). https://doi.org/10.1038/s41437-024-00683-4

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