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Marine Biology

, 166:88 | Cite as

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

  • Lara BaptistaEmail author
  • António M. Santos
  • M. Pilar Cabezas
  • Ricardo Cordeiro
  • Carlos Melo
  • Sérgio P. Ávila
Original paper

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.

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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.

Supplementary material

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References

  1. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Proceedings of the 2nd international symposium on information theory. Akademiai Kiado, Budapest, pp 267–281Google Scholar
  2. Ávila SP (2005) Processos e padrões de dispersão e colonização nos Rissoidae (Mollusca: Gastropoda) dos Açores. Dissertation, University of the Azores, Ponta DelgadaGoogle Scholar
  3. Ávila SP (2006) Oceanic islands, rafting, geographical range and bathymetry: a neglected relationship? Occas Publ Irish Biogeogr Soc 9:22–39Google Scholar
  4. Ávila SP (2013) Unravelling the patterns and processes of evolution of marine life in oceanic islands: a global framework. In: Fernández-Palacios JM, Nascimento L, Hernández J, Clemente S, González A, Díaz-González JP (eds) Climate change perspectives from the atlantic: past, present and future. Universidad de La Laguna, Tenerife, pp 95–125Google Scholar
  5. Ávila SP, Madeira P, Mendes N, Rebelo A, Medeiros A, Gomes C, García-Talavera F, da Silva CM, Cachão M, Hillaire-Marcel C, Martins AMF (2008) Mass extinctions in the Azores during the last glaciation: fact or myth? J Biogeogr 35:1123–1129.  https://doi.org/10.1111/j.1365-2699.2008.01881.x CrossRefGoogle Scholar
  6. Ávila SP, da Silva CM, Schiebel R, Cecca F, Backeljau T, Martins AMF (2009) How did they get here? Palaeobiogeography of the Pleistocene marine Molluscs of the Azores. Bull la Soc Géologique la Fr 180:295–307.  https://doi.org/10.2113/gssgfbull.180.4.295 CrossRefGoogle Scholar
  7. Ávila SP, Goud J, Martins AMF (2012) Patterns of diversity of the Rissoidae (Mollusca: Gastropoda) in the Atlantic and the Mediterranean Region. Sci World J.  https://doi.org/10.1100/2012/164890 (Article ID:164890) CrossRefGoogle Scholar
  8. Ávila SP, Melo C, Silva L, Ramalho RS, Quartau R, Hipólito A, Cordeiro R, Rebelo AC, Madeira P, Rovere A, Hearty PJ, Henriques D, da Silva CM, Martins AMDF, Zazo C (2015) A review of the MIS 5e highstand deposits from Santa Maria Island (Azores, NE Atlantic): palaeobiodiversity, palaeoecology and palaeobiogeography. Quat Sci Rev 114:126–148.  https://doi.org/10.1016/j.quascirev.2015.02.012 CrossRefGoogle Scholar
  9. Ávila SP, Cachão M, Ramalho RS, Botelho AZ, Madeira P, Rebelo AC, Cordeiro R, Melo C, Hipólito A, Ventura MA, Lipps JH (2016) The palaeontological heritage of Santa Maria Island (Azores: NE Atlantic): a re-evaluation of Geosites in GeoPark Azores and their use in Geotourism. Geoheritage 8:155–171.  https://doi.org/10.1007/s12371-015-0148-x CrossRefGoogle Scholar
  10. Ávila SP, Cordeiro R, Madeira P, Silva L, Medeiros A, Rebelo AC, Melo C, Neto AI, Haroun R, Monteiro A, Rijsdijk K, Johnson ME (2018) Global change impacts on large-scale biogeographic patterns of marine organisms on Atlantic oceanic islands. Mar Pollut Bull 126:101–112.  https://doi.org/10.1016/j.marpolbul.2017.10.087 CrossRefPubMedGoogle Scholar
  11. Ávila SP, Melo C, Sá N, Quartau R, Rijsdijk K, Ramalho RS, Berning B, Cordeiro R, de Sá NC, Pimentel A, Baptista L, Medeiros A, Gil A, Johnson ME (2019) Towards a “sea-level sensitive marine island biogeography” model: the impact of glacio-eustatic oscillations in global marine island biogeographic patterns. Biol Rev.  https://doi.org/10.1111/brv.12492 CrossRefPubMedGoogle Scholar
  12. Azevedo J (1998) Geologia e Hidrogeologia da Ilha das Flores (Açores-Portugal). Dissertation, University of Coimbra, CoimbraGoogle Scholar
  13. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537.  https://doi.org/10.1371/journal.pcbi.1003537 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552.  https://doi.org/10.1093/oxfordjournals.molbev.a026334 CrossRefPubMedGoogle Scholar
  15. Coan E (1964) A proposed revision of the Rissoacean families Rissoidae, Rissoinidae, and Cingulopsidae (Mollusca: Gastropoda). Veliger 6:164–171Google Scholar
  16. Conti MA, Monari S, Oliverio M (1993) Early rissoid gastropods from the Jurassic of Italy: the meaning of first appearances. Scr Geol 2:67–74Google Scholar
  17. Cordeiro R, Ávila SP (2015) New species of Rissoidae (Mollusca, Gastropoda) from the Archipelago of the Azores (northeast Atlantic) with an updated regional checklist for the family. Zookeys 480:1–19.  https://doi.org/10.3897/zookeys.480.8599 CrossRefGoogle Scholar
  18. Cordeiro R, Borges JP, Martins AMF, Ávila SP (2015) Checklist of the littoral gastropods (Mollusca Gastropoda) from the Archipelago of the Azores (NE Atlantic). Biodivers J 6:855–900Google Scholar
  19. Criscione F, Ponder WF (2013) A phylogenetic analysis of Rissooidean and Cingulopsoidean families (Gastropoda: Caenogastropoda). Mol Phylogenet Evol 66:1075–1082.  https://doi.org/10.1016/j.ympev.2012.11.026 CrossRefPubMedGoogle Scholar
  20. Criscione F, Ponder WF, Köhler F, Takano T, Kano Y (2017) A molecular phylogeny of Rissoidae (Caenogastropoda: Rissooidea) allows testing the diagnostic utility of morphological traits. Zool J Linn Soc 179:23–40.  https://doi.org/10.1111/zoj.12447 CrossRefGoogle Scholar
  21. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Degnan JH, Rosenberg NA (2006) Discordance of species trees with their most likely gene trees. PLoS Genet 2:762–768.  https://doi.org/10.1371/journal.pgen.0020068 CrossRefGoogle Scholar
  23. Demand J, Fabriol R, Gerard F, Lundt F, Chovelon P (1982) Prospection géothermique, íles de Faial et de Pico (Açores). Rapport géologique, geochimique et gravimétrique. Technical Report BRGM 82 SGN 003 GTHGoogle Scholar
  24. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376.  https://doi.org/10.1007/BF01734359 CrossRefPubMedGoogle Scholar
  25. Forest F (2009) Calibrating the tree of life: fossils, molecules and evolutionary timescales. Ann Bot 104:789–794.  https://doi.org/10.1093/aob/mcp192 CrossRefPubMedPubMedCentralGoogle Scholar
  26. França Z, Nunes J, Cruz J, Duarte J, Forjaz V (2002) Preliminary study of the Corvo Island volcanism, Azores. 3o Assembleia Luso-Espanhola de Geodesia e Geofísica S09:727–730Google Scholar
  27. Gadagkar S, Rosenberg MS, Kumar S (2005) Inferring species Phylogenies from multiple genes: concatenated sequence tree versus consensus gene tree. J Exp Zool 304B:64–74.  https://doi.org/10.1002/jez.b.21026 CrossRefGoogle Scholar
  28. García-Talavera F (1983) Los moluscos gasterópodos anfiatlánticos: estudio paleo y biogeográfico de las especies bentónicas litorales. Universidad de La Laguna, La LagunaGoogle Scholar
  29. GEBCO (2008) The GEBCO_2008 Grid, version 20100927. http://www.gebco.net
  30. Gerber J, Hemmen J, Groh K (1989) Eine pleistozäne marine Molluskenfauna on Porto Santo (Madeira-Archipel). Mitt dtsch malakozool Ges 44:19–30Google Scholar
  31. Gofas S (1990) The littoral Rissoidae and Anabathridae of São Miguel, Azores. In: Martins AMF (ed) The marine fauna and flora of the azores. (Proceedings of the First International Workshop of Malacology, Vila Franca Do Campo, São Miguel, Azores). Açoreana, Supplement 2, pp 97–134Google Scholar
  32. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  33. Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27(3):570–580.  https://doi.org/10.1093/molbev/msp274 CrossRefPubMedGoogle Scholar
  34. Hildenbrand A, Weis D, Madureira P, Marques F (2014) Recent plate re-organization at the Azores Triple Junction: evidence from combined geochemical and geochronological data on Faial, S. Jorge and Terceira volcanic islands. Lithos 210–211:27–39.  https://doi.org/10.1016/j.lithos.2014.09.009 CrossRefGoogle Scholar
  35. Hurley I, Mueller R, Dunn K, Schmidt E, Friedman M, Ho R, Prince V, Yang Z, Thomas M, Coates M (2007) A new time-scale for ray-finned fish evolution. Proc R Soc B 274:489–498.  https://doi.org/10.1098/rspb.2006.3749 CrossRefPubMedGoogle Scholar
  36. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518.  https://doi.org/10.1093/nar/gki198 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Knowles LL (2009) Estimating species trees: methods of phylogenetic analysis when there is incongruence across genes. Syst Biol 58:463–467.  https://doi.org/10.1093/sysbio/syp061 CrossRefPubMedGoogle Scholar
  38. Kowalke T, Harzhauser M (2004) Early ontogeny and palaeoecology of the Mid-Miocene rissoid gastropods of the Central Paratethys. Acta Palaeontol Pol 49:111–134Google Scholar
  39. Kubatko LS, Degnan JH (2007) Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 56:17–24.  https://doi.org/10.1080/10635150601146041 CrossRefPubMedGoogle Scholar
  40. Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1675–1701CrossRefGoogle Scholar
  41. Liu L, Xi Z, Wu S, Davis CC, Edwards SV (2015) Estimating phylogenetic trees from genome-scale data. Ann N Y Acad Sci 1360:36–53.  https://doi.org/10.1111/nyas.12747 CrossRefPubMedGoogle Scholar
  42. Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536.  https://doi.org/10.1093/sysbio/46.3.523 CrossRefGoogle Scholar
  43. Mata J, Fonseca PE, Prada S, Rodrigues D, Martins S, Ramalho RS, Madeira J, Cachão M, da Silva CM, Matias MJ (2013) O Arquipélago da Madeira. In: Dias R, Araújo A, Terrinha P, Kullberg JC (eds) Geologia de Portugal, 1st edn. Escolar Editora, Lisboa, pp 691–746Google Scholar
  44. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41:W597–W600CrossRefGoogle Scholar
  45. Meireles RP, Quartau R, Ramalho RS, Rebelo AC, Madeira J, Zanon V, Ávila SP (2013) Depositional processes on oceanic island shelves—evidence from storm-generated Neogene deposits from the mid-North Atlantic. Sedimentology 60:1769–1785.  https://doi.org/10.1111/sed.12055 CrossRefGoogle Scholar
  46. Mendes FK, Hahn MW (2016) Gene tree discordance causes apparent substitution rate variation. Syst Biol 65:711–721.  https://doi.org/10.1093/sysbio/syw018 CrossRefPubMedGoogle Scholar
  47. Ogilvie HA, Heled J, Xie D, Drummond AJ (2016) Computational performance and statistical accuracy of ∗BEAST and comparisons with other methods. Syst Biol 65:381–396.  https://doi.org/10.1093/sysbio/syv118 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ogilvie HA, Bouckaert RR, Drummond AJ (2017) StarBEAST2 brings faster species tree inference and accurate estimates of substitution rates. Mol Biol Evol 34:2101–2114.  https://doi.org/10.1093/molbev/msx126 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Parham JF, Donoghue PCJ, Bell CJ, Calway TD, Head JJ, Holroyd PA, Inoue JG, Irmis RB, Joyce WG, Ksepka DT, Patané JSL, Smith ND, Tarver JE, Van Tuinen M, Yang Z, Angielczyk KD, Greenwood JM, Hipsley CA, Jacobs L, Makovicky PJ, Müller J, Smith KT, Theodor JM, Warnock RCM, Benton MJ (2012) Best practices for justifying fossil calibrations. Syst Biol 61:346–359.  https://doi.org/10.1093/sysbio/syr107 CrossRefPubMedGoogle Scholar
  50. Patiño J, Whittaker RJ, Borges PAV, Fernández-Palacios JM, Ah-Peng C, Araújo MB, Ávila SP, Cardoso P, Cornuault J, de Boer EJ, de Nascimento L, Gil A, González-Castro A, Gruner DS, Heleno R, Hortal J, Illera JC, Kaiser-Bunbury CN, Matthews TJ, Papadopoulou A, Pettorelli N, Price JP, Santos AMC, Steinbauer MJ, Triantis KA, Valente L, Vargas P, Weigelt P, Emerson BC (2017) A roadmap for island biology: 50 fundamental questions after 50 years of The Theory of Island Biogeography. J Biogeogr 44:963–983.  https://doi.org/10.1111/jbi.12986 CrossRefGoogle Scholar
  51. Paulay G (1994) Biodiversity on oceanic islands: its origin and extinction. Integr Comp Biol 34:134–144.  https://doi.org/10.1093/icb/34.1.134 CrossRefGoogle Scholar
  52. Pond SLK, Poon AFY, Frost SDW (2009) Estimating selection pressures on alignments of coding sequences. In: Lemey P, Salemi M, Vandamme A (eds) The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis, 2nd edn. Cambridge University Press, Cambridge, pp 419–451CrossRefGoogle Scholar
  53. Ponder WF (1967) Classification of Rissoidae and Orbitestellidae with descriptions of some new taxa. Trans R Soc N Zeal Zool 9:193–224Google Scholar
  54. Ponder WF (1984) A review of the Genera of the Rissoidae (Mollusca: Mesogastropoda: Rissoacea). Rec Aust Museum Suppl 4:1–221.  https://doi.org/10.3853/j.0812-7387.4.1985.100 CrossRefGoogle Scholar
  55. Ramalho RS, da Silveira AB, Fonseca PE, Madeira J, Cosca M, Cachão M, Fonseca MM, Prada SN (2015) The emergence of volcanic oceanic islands on a slow-moving plate: the example of Madeira Island, NE Atlantic. Geochem Geophys GeosyS 16:522–537.  https://doi.org/10.1002/2014GC005657 CrossRefGoogle Scholar
  56. Ramalho RS, Helffrich G, Madeira J, Cosca M, Thomas C, Quartau R, Hipólito A, Rovere A, Hearty PJ, Ávila SP (2017) Emergence and evolution of Santa Maria Island (Azores)—the conundrum of uplifted islands revisited. Geol Soc Am Bull 129:372–391.  https://doi.org/10.1130/B31538.1 CrossRefGoogle Scholar
  57. 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 61:539–542CrossRefGoogle Scholar
  58. Salemi M (2009) Genetic distances and nucleotide substitution models. In: Lemey P, Salemi M, Vandamme A (eds) The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis, 2nd edn. Cambridge University Press, Cambridge, pp 126–140Google Scholar
  59. Scheltema RS (1986a) Long-distance dispersal by planktonic larvae of shoal-water benthic invertebrates among central Pacific islands. Bull Mar Sci 39:241–256Google Scholar
  60. Scheltema RS (1986b) On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview and summary of problems. Bull Mar Sci 39:290–322Google Scholar
  61. Scheltema RS (1989) Planktonic and non-planktonic development among prosobranch gastropods and its relationship to the geographic range of species. In: Ryland JS, Tyles PA (eds) Reproduction, genetics and distribution of marine organisms. Olsen and Olsen, Fredensborg, pp 183–188Google Scholar
  62. Scheltema RS (1995) The relevance of passive dispersal for the biogeography of Caribbean mollusks. Am Malacol Bull 11:99–115Google Scholar
  63. Scheltema RS, Williams IP (1983) Long-distance dispersal of planktonic larvae and the biogeography and evolution of some Polynesian and western Pacific mollusks. Bull Mar Sci 33:545–565Google Scholar
  64. Scheltema RS, Williams IP, Lobel PS (1996) Retention around and long-distance dispersal between oceanic islands by planktonic larvae of benthic gastropod Mollusca. Am Malacol Bull 12:67–75Google Scholar
  65. Sibrant A, Marques F, Hildenbrand A (2014) Construction and destruction of a volcanic island developed inside an oceanic rift: Graciosa Island, Terceira Rift, Azores. J Volcanol Geotherm Res 284:32–45.  https://doi.org/10.1016/j.jvolgeores.2014.07.014 CrossRefGoogle Scholar
  66. Sibrant A, Hildenbrand A, Marques F, Weiss B, Boulesteix T, Hübscher C, Lüdmann T, Costa A, Catalão J (2015) Morpho-structural evolution of a volcanic island developed inside an active oceanic rift: S. Miguel Island (Terceira Rift, Azores). J Volcanol Geotherm Res 301:90–106.  https://doi.org/10.1016/j.jvolgeores.2015.04.011 CrossRefGoogle Scholar
  67. Sukumaran J, Holder M (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26:1569–1571CrossRefGoogle Scholar
  68. Suzuki Y, Glazko GV, Nei M (2002) Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc Natl Acad Sci USA 99:16138–16143.  https://doi.org/10.1073/pnas.212646199 CrossRefPubMedGoogle Scholar
  69. Thiele J (1929) Handbuch der Systematischen Weichtierkunde. Gustav Fischer, JenaGoogle Scholar
  70. Uchman A, Torres P, Johnson ME, Berning B, Ramalho RS, Rebelo AC, Melo CS, Baptista L, Madeira P, Cordeiro R, Ávila SP (2018) Feeding traces of recent ray fish and occurrences of the trace fossil Piscichnus waitemata from the Pliocene of Santa Maria Island, Azores (Northeast Atlantic). Palaios 33:361–375.  https://doi.org/10.2110/palo.2018.027 CrossRefGoogle Scholar
  71. Wenz W (1938) Gastropoda. Teil 1, Allgemeiner Teil und Prosobranchia. In: Schindewolfe OH (ed) Handbuch der Paläozoologie, vol 6. Gebrüer Bornträger, Berlin, pp 1–231Google Scholar
  72. Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Lemey P, Salemi M, Vandamme A (eds) The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis. Cambridge University Press, Cambridge, pp 615–630CrossRefGoogle Scholar
  73. Zheng Y, Peng R, Kuro-o M, Zeng Z (2011) Exploring patterns and extent of bias in estimating divergence time from mitochondrial DNA sequence data in a particular lineage: a case study of Salamanders (Order Caudata). Mol Biol Evol 28:2521–2535.  https://doi.org/10.1093/molbev/msr072 CrossRefPubMedGoogle Scholar
  74. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. University of Texas, AustinGoogle Scholar

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Authors and Affiliations

  1. 1.CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Pólo dos AçoresUniversidade dos AçoresPonta DelgadaPortugal
  2. 2.MPB-Marine PalaeoBiogeography Working Group of the University of the AzoresPonta DelgadaPortugal
  3. 3.Faculdade de Ciências da Universidade do PortoPortoPortugal
  4. 4.CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório AssociadoUniversidade do PortoVairãoPortugal
  5. 5.Departamento de Biologia, Faculdade de Ciências e TecnologiaUniversidade dos AçoresPonta DelgadaPortugal
  6. 6.Departamento de Geologia, Faculdade de CiênciasUniversidade de LisboaLisbonPortugal
  7. 7.Instituto Dom Luiz, Faculdade de CiênciasUniversidade de LisboaLisbonPortugal

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