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Intertidal or subtidal/circalittoral species: which appeared first? A phylogenetic approach to the evolution of non-planktotrophic species in Atlantic Archipelagos

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Abstract

Volcanic oceanic archipelagos are fascinating natural laboratories of evolutionary patterns and processes in remote, unique conditions. In the insular marine realm, deepwaters and sea-surface circulation hamper dispersal and, for marine invertebrates, this ability is linked to larval development: planktotrophic organisms disperse easily, whereas non-planktotrophic species usually have restricted ranges. Similarly, bathymetric zonation also influences dispersal: intertidal species are more prone to engage in the process than subtidal/circalittoral species. Therefore, the presence of endemic congeneric non-planktotrophic marine gastropods in two Atlantic archipelagos, hundreds of kilometers apart, inspired a biogeographical hypothesis. It predicts that when two congeneric non-planktotrophic gastropod species, with different bathymetric specific ranges, simultaneously occur and are restricted to two remote archipelagos, the subtidal/circalittoral species is expected to be evolutionarily older than the intertidal species. The present study aims to test this theoretical prediction from a multidisciplinary perspective, with a molecular, Bayesian, fossil-calibrated, phylogenetic analysis of selected Rissoidae species to test the theoretical predictions. We hereby corroborate the earlier speciation of the subtidal/circalittoral Alvania sleursi, compared to the congeneric intertidal Alvania mediolittoralis. Supported by ecological and palaeontological observations in the Azores and Madeira archipelagos, our study provides the first phylogenetic approach to this biogeographical hypothesis, unveiling the evolution of Rissoids in two insular Atlantic systems. In a broader perspective, combining molecular and palaeontological data contributes to better understand past processes that shaped current diversity in Atlantic Archipelagos. This approach can be further replicated in other related non-planktotrophic invertebrates in remote Archipelagos, to corroborate the biogeographical hypothesis in other marine taxa.

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Data availability

All the mitochondrial COI and nuclear 28S sequences analyzed during the current study are deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/). COI sequences are deposited in GenBank with the accession numbers: MG652373-8 (Alvania angioyi), MG652379-80 (A. formicarum), MG652381-5 (A. mediolittoralis), MG652386-7 (A. sleursi), MG652395-407 (Cingula trifasciata), MG652392-4 (Crisilla postrema), MG652408-13 and MG652419-21 (Rissoa guernei), MG652414-8 and MG652422 (R. cf. guernei), MG652429-31 (Setia subvaricosa), and MG652432-36 (Pisinna glabrata). Sequences of 28S rRNA gene are available under the following accession numbers: MG663173-8 (A. angioyi), MG663179 (A. formicarum), MG663180-1 (A. mediolittoralis), MG663182-3 (A. sleursi), MG663189-96 (C. trifasciata), MG663185-8 (C. postrema), MG663197-203, MG663207 and MG663209 (R. guernei), MG663204-6 and MG663208 (R. cf. guernei), MG663215-6 (S. subvaricosa), and MH047302-4 (P. glabrata).

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Acknowledgements

This work was supported by Fundação para a Ciência e Tecnologia, IP (Grant number SFRH/BD/135918/2018 to L.B.; research contract IF/00465/2015 to S.P.A.); by Fundo Regional para a Ciência e Tecnologia (Grant number M3.1.a/F/100/2015 to C.S.M.); by FEDER funds through the Operational Programme for Competitiveness Factors—COMPETE and national funds through Fundação para a Ciência e Tecnologia, IP (projects UID/BIA/50027/2013, POCI-01-0145-FEDER-006821); by regional funds through Direção Regional para a Ciência e Tecnologia (DRCT-M1.1.a/005/Funcionamento-C-/2016); and by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF) under project MarInfo (NORTE-01-0145-FEDER-000031). This work was also supported by FEDER funds (in 85%) and by funds of the Regional Government of the Azores (15%) through Programa Operacional Açores 2020, in the scope of the project “AZORESBIOPORTAL—PORBIOTA”: ACORES-01-0145-FEDER-000072. We thank the reviewers for comments that greatly improved the manuscript.

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The sequences used in the molecular phylogenies of COI and 28S were mainly retrieved from the GenBank database. The new sequences were obtained from specimens deposited in the Marine Molluscs Reference Collection of the Department of Biology of the University of the Azores (DBUA). Sampling was not performed for this work. All applicable national and/or institutional guidelines for the use of collection material were followed. Only invertebrates were used in this study.

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Baptista, L., Santos, A.M., Cabezas, M.P. et al. Intertidal or subtidal/circalittoral species: which appeared first? A phylogenetic approach to the evolution of non-planktotrophic species in Atlantic Archipelagos. Mar Biol 166, 88 (2019). https://doi.org/10.1007/s00227-019-3536-y

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