The biogeographical history of Macaronesian and South African sand-smelt is approached for the first time with the inclusion of A. lopeziana in the genus’ phylogenetic analysis, using a fragment of the mitochondrial control region. The fossil-calibrated phylogeny revealed an early process of vicariance close to the estimated age of Atherina (~ 19 Mya) leading to two old clades separating European from South African sand-smelts; these two groups evolved into the five extant species. The question raised by previous studies about the identity of the Macaronesian sand-smelt was confirmed; A. presbyter reached Canary Islands and Azores (~ 1.1 Ma) and the populations in these archipelagos have remained highly isolated. The poor dispersal capability of this genus in conjunction with the fast cooling events during Pliocene and Pleistocene was pointed out as the main factor causing the isolation and speciation processes of the populations inhabiting these regions.
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Akaike H (1974) A new look at the statistical model identification. IEEE Trans on Automat Contr 19:716–723. https://doi.org/10.1109/TAC.1974.1100705
Astolfi L, Dupanlouop I, Rossi R, Bisol PM, Faure E, Congiu L (2005) Mitochondrial variability of sand smelt (Atherina boyeri, Risso 1810) populations from North Mediterranean coastal lagoons. Mar Ecol Prog Ser 297:233–243. https://doi.org/10.3354/meps297233
Bamber RN, Henderson PA, Turnpenny AWH (1985) The early life history of the sand smelt (Atherina presbyter). J Mar Biol Assoc UK 65:697–706. https://doi.org/10.1017/S002531540005253X
Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Campanella D, Hughes LC, Unmack PJ, Bloom DD, Piller KR, Orti G (2015) Multilocus fossil-calibrated phylogeny of Atheriniformes (Teleostei, Ovalentaria). Mol Phylogenet Evol 86:8–23. https://doi.org/10.1016/j.ympev.2015.03.001
Carnevale G, Haghfarshi E, Abbasi S, Alimohammadian H, Reichenbacher B (2011) A new species of silverside from the Late Miocene of NW Iran. Acta Palaeontol Pol 56:749–756. https://doi.org/10.4202/app.2011.0003
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
deMenocal PB (2004) African climate change and faunal evolution during the Pliocene– Pleistocene. Earth Planet Sci Lett 220:3–24. https://doi.org/10.1016/S0012-821X(04)00003-2
Dolan AM, Haywood AM, Hunter SJ, Tindall JC, Dowsett HJ, Hill DJ, Pickering SJ (2015) Modelling the enigmatic Late Pliocene Glacial Event - Marine Isotope Stage M2. Glob Planet Chang 128:47–60. https://doi.org/10.1016/j.gloplacha.2015.02.001
Domingues VS, Santos RS, Brito A, Alexandrou M, Almada VC (2007) Mitochondrial and nuclear markers reveal isolation by distance and effects of Pleistocene glaciations in the northeastern Atlantic and Mediterranean populations of the white seabream (Diplodus sargus, L.). J Exp Mar Biol Ecol 346:102–113. https://doi.org/10.1016/j.jembe.2007.03.002
Domingues VS, Santos RS, Brito A, Almada VC (2006) Historical population dynamics and demography of the eastern Atlantic pomacentrid Chromis limbata (Valenciennes, 1833). Mol Phylogenet Evol 40:139–147. https://doi.org/10.1016/j.ympev.2006.02.009
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50. https://doi.org/10.1177/117693430500100003
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Felsenstein J (1985) ConWdence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Francisco SM, Castilho R, Soares M, Congiu L, Brito A, Vieira MN, Almada VC (2009) Phylogeography and demographic history of Atherina presbyter (Pisces: Atherinidae) in the North-eastern Atlantic based on mitochondrial DNA. Mar Biol 156:1421–1432. https://doi.org/10.1007/s00227-009-1182-5
Francisco SM, Congiu L, Stefanni S, Castilho R, Brito A, Ivanova PP, Levy A, Cabral H, Kilias G, Doadrio I, Almada VC (2008) Phylogenetic relationships of the north-eastern Atlantic and Mediterranean forms of Atherina (Pisces, Atherinidae). Mol Phylogenet Evol 48:782–788. https://doi.org/10.1016/j.ympev.2007.12.009
Francisco SM, Congiu L, von der Heyden S, Almada VC (2011) Multilocus phylogenetic analysis of the genus Atherina (Pisces: Atherinidae). Mol Phylogenet Evol 61:71–78. https://doi.org/10.1016/j.ympev.2011.06.002
Froese R, Pauly D (2017). FishBase. World Wide Web electronic publication. URL: http://www.fishbase.org. Accessed 2 Jul 2019
Hasegawa M, Kishino H, Yano T (1985) Dating of human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174. https://doi.org/10.1007/BF02101694
Klossa-Kilia E, Papasotiropoulos V, Tryfonopoulos G, Alahiotis S, Kilias G (2007) Phylogenetic relationships of Atherina hepsetus and Atherina boyeri (Pisces: Atherinidae) populations from Greece, based on mtDNA sequences. Biol J Linn Soc 92:151–161. https://doi.org/10.1111/j.1095-8312.2007.00829.x
Klossa-Kilia E, Prassa M, Papasotiropoulos V, Alahiotis S, Kilias G (2002) Mitochondrial DNA diversity in Atherina boyeri populations as determined by RFLP analysis of three mtDNA segments. Heredity 89:363–370. https://doi.org/10.1038/sj.hdy.6800144
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
McKay R, Naish T, Carter L, Riesselman C, Dunbar R, Sjunneskog C, Winter D, Sangiorgi F, Warren C, Pagani M, Schouten S, Willmott V, Levy R, DeConto R, Powell RD (2012) Antarctic and Southern Ocean influences on Late Pliocene global cooling. Proc Natl Acad Sci 109(17):6423–6428. https://doi.org/10.1073/pnas.1112248109
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Maugé LA (1990). Atherinidae. In: Quero JC, Hureau JC, Karrer C, Post A, Saldanha L (eds.) Check-list of the fishes of the eastern tropical Atlantic (CLOFETA). JNICT, Lisbon; SEI, Paris; and UNESCO, Paris Vol 2, pp 604–605
Miller MA, Pfeiffer W, Schwartz T (2011) The CIPRES science gateway: a community resource for phylogenetic analyses. In: Proceedings of the 2011 TeraGrid Conference: extreme digital discovery (TG ’11). ACM, New York, pp 41–48. https://doi.org/10.1145/2016741.2016785
Morais LT, Sylla M, Ivantsoff W (2016) Atherinidae. In: Carpenter KE and De Angelis N (eds) FAO species identification guide for fishery purposes. The living marine resources of the Eastern Central Atlantic Vol. 4. Bony fishes part 1 (Elopiformes to Scorpaeniformes) Rome (FAO), pp. 2111-2118
Morato T, Machete M, Kitchingman A, Tempera F et al (2008) Abundance and distribution of seamounts in the Azores. Mar Ecol Prog Ser 357:17–21. https://doi.org/10.3354/meps07268
Neira FJ, Beckley LE, Whitfield AK (1988) Larval development of the Cape silverside, Atherina breviceps Cuv, and Val . 1835 (Teleostei : Atherinidae) from southern Africa. S Afr J Zool 23:176–183
Ostellari L, Bargelloni L, Penzo E, Patarnello P, Patarnello T (1996) Optimization of single-strand conformation polymorphism and sequence analysis of the mitochondrial control region in Pagellus bogaraveo (Sparidae, Teleostei): rationalized tools in fish population biology. Anim Genet 27:423–427. https://doi.org/10.1111/j.1365-2052.1996.tb00510.x
Palmer CJ, Culley MB (1984) The egg and early life stages of the sandsmelt, Atherina presbyter Cuvier. J Fish Biol 24:537–544. https://doi.org/10.1111/j.1095-8649.1984.tb04824.x
Pujolar JM, Zane L, Congiu L (2012) Phylogenetic relationships and demographic histories of the Atherinidae in the Eastern Atlantic and Mediterranean Sea re-examined by Bayesian inference. Mol Phylogenet Evol 63:857–865. https://doi.org/10.1016/j.ympev.2012.02.027
Quignard JP, Pras A (1986) Atherinidae. In: Whitehead P, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the North-Eastern Atlantic and the Mediterranean. UNESCO, Paris, pp 1207–1210
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032
Rambaut A (2009) Figtree v1.4. Available from: http://tree.bio.ed.ac.uk/. Last accessed 2 April 2018
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rossignol M, Blache J (1961) Sur le statut spécifique de deux poissons pélagiques du Golfe de Guinée. Anchoviella guineensis nov. sp. (Clupei− formes, Engraulidae) et Atherina lopeziana nov. sp. (Mugiliformes, Atherinidae). Bull Mus Natl Hist Nat 33:285–293 https://www.biodiversitylibrary.org/item/240925#page/299/mode/1up. Last accessed 28 March 2019
Santos SR, Hawkins SJ, Montieiro LR, Alves M, Isidro EJ (1995) Marine research, resources and conservation in the Azores. Aquat Conserv 5:311–354
Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlacion extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632. https://doi.org/10.2307/2413122
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Thompson J, Higgins D, Gibson T (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4690. https://doi.org/10.1093/nar/22.22.4673
Trabelsi M, Faure E, Quignard JP, Boussaïd M, Focant B, Mâamouri F (2002a) Atherina punctata and Atherina lagunae (Pisces, Atherinidae), new species in the Mediterranean Sea. Article 1: biometric investigations of three Atherinid species. C R Biol 325:967–975. https://doi.org/10.1016/S1631-0691(02)01506-8
Trabelsi M, Gilles A, Fleury C, Mâamouri F, Quignard JP, Faure E (2002b) Atherina punctata and Atherina lagunae (Pisces, Atherinidae), new species in the Mediterranean Sea. Article 2: molecular investigations of three Atherinid species. C R Biol 325:1119–1128. https://doi.org/10.1016/S1631-0691(02)01529-9
This study was funded by MARE (UID/MAR/04292/2019)—Fundação para a Ciência e a Tecnologia—FCT (partially FEDER funded) and by the Erasmus+ Programme as a project developed during a 3-month traineeship by the first author.
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The datasets generated during and/or analyzed during the current study were deposited in the GenBank repository (accession numbers MH177219- MH177228). Any dataset generated during and/or analyzed during the current study is available from the corresponding author on reasonable request. Any publicly available data on which the conclusions of the paper rely in the manuscript are cited in the reference list and when available full URL DOIs are included.
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Moreno-Borges, S., Brito, A. & Francisco, S.M. Biogeographical history of the genus Atherina (Pisces: Atherinidae) in the central Eastern Atlantic. Mar. Biodivers. 49, 2633–2639 (2019). https://doi.org/10.1007/s12526-019-00996-2
- Atherina. lopeziana