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The Calibrated Phylogeny of the Drosophila fasciola Subgroup (D. repleta Group Wasserman) Indicates Neogene Diversification of Its Internal Branches

  • Systematics, Morphology and Physiology
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Abstract

The species of the Drosophila fasciola subgroup Wasserman represent the dominant section of the Drosophila repleta group Wasserman in the American rainforests and have a broad geographical distribution in the New World. However, despite of its wide range, the D. fasciola subgroup is one of the most overlooked D. repleta subgroups. Here, we report a molecular phylogenetic analysis focused on the D. fasciola subgroup using two mitochondrial [cytochrome oxidase subunit I (COI), cytochrome oxidase subunit II (COII)] and two nuclear [elongation factor-1alpha F1 (EF-alphaF1) and transformer (tra)] genes. Overall, we found that this subgroup is a monophyletic taxon, subdivided into two main internal branches: named Fas1 and Fas2 clades. The diversification of these clades is estimated to have begun in the middle Miocene, around 12 Ma [95% high posterior density (HPD) 9.0–15 Ma], and might be associated with the colonization of South America by Central America populations after the closure of Isthmus of Panama due to the temporal congruence between these events. The terminal branches had their origins estimated to be in the Pliocene or the Plio-Pleistocene transition. For the later estimates, both the geomorphological influences and the climatic oscillations of the Pleistocene may have played a role in shaping the diversification of the D. fasciola group.

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References

  • Bachli G, Vilela CR (2002) Six new species of Drosophila (Diptera, Drosophilidae) from Parque Nacional Henri Pittier, Venezuela. Mitt Schweiz Ent Ges 75:223–244

    Google Scholar 

  • Bremer K (1994) Branch support and tree stability. Cladistics 10:295–304

    Article  Google Scholar 

  • Brower AVZ, Desalle R (1994) Practical and theoretical considerations for choice of a DNA sequence region in insect molecular systematics, with a short review of published studies using nuclear gene regions. Ann Entomol Soc Am 87:702–716

    Article  CAS  Google Scholar 

  • Costa CTA, Sene FM (2002) Characterization of courtship sounds of species of the subgroup fasciola (Diptera, Drosophilidae, Drosophila repleta group): interspecific and interpopulational analyses. Braz J Biol 62(4):573–583

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diniz NM, Sene FM (2004) Chromosomal phylogeny of the Drosophila fasciola species subgroup revisited (Diptera, Drosophilidae). Genet Mol Biol 27(4):561–566

    Article  Google Scholar 

  • Domingos FM, Bosque RJ, Cassimiro J, Colli GR, Rodrigues MT, Santos MG, Beheregaray LB (2014) Out of the deep: Cryptic speciation in a Neotropical gecko (Squamata, Phyllodactylidae) revealed by species delimitation methods. Mol Phylog Evol 80:113–124

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durando CM, Baker RH, Etges WJ, Heed WB, Wasserman M, DeSalle R (2000) Phylogenetic analysis of the repleta species group of the genus Drosophila using multiple sources of characters. Mol Phylogenet Evol 16(2):296–307

    Article  CAS  PubMed  Google Scholar 

  • Elmer KR, Bonett RM, Wake DB, Lougheed SC (2013) Early Miocene origin and cryptic diversification of South American salamanders. BMC Evol Biol 4:13–59

    Google Scholar 

  • Erixon P, Svennblad B, Britton T, Oxelman B (2003) Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Syst Biol 52:665–673

    Article  PubMed  Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Gross M, Ramos MIF, Piller WE. (2015) A minute ostracod (Crustacea: Cytheromatidae) from the Miocene Solimões Formation (western Amazonia, Brazil): evidence for marine incursions? J Syst Palaeontol 1–22

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192

    Article  Google Scholar 

  • Hoorn C, Wesselingh FP, Steege H, Bermudez MA, Mora A, Sevink J, Sanmartın I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T, Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931

    Article  CAS  PubMed  Google Scholar 

  • Kulathinal RJ, Skwarek L, Morton RA, Singh RS (2003) Rapid evolution of the sex-determining gene, transformer: structural diversity and rate heterogeneity among sibling species of Drosophila. Mol Biol Evol 20:441–452

    Article  CAS  PubMed  Google Scholar 

  • Lang M, Polihronakis RM, Acurio AE, Markow TA, Orgogozo V (2014) Radiation of the Drosophila nannoptera species group in Mexico. J Evol Biol 27:575–584

    Article  CAS  PubMed  Google Scholar 

  • Manfrin MH, Sene FM (2006) Cactophilic Drosophila in South America: a model for evolutionary studies. Genetica 126:57–75

    Article  PubMed  Google Scholar 

  • Matzkin LM (2014) Ecological genomics of host shifts in Drosophila mojavensis. Adv Exp Med Biol 781:233–247

    Article  PubMed  Google Scholar 

  • McAllister BF, McVean GA (2000) Neutral evolution of the sex-determining gene transformer in Drosophila. Genetics 154:1711–1720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Medeiros HFD, Klaczko LB (2004) How many species of drosophila (Diptera, Drosophilidae) remain to be described in the forests of São Paulo, Brazil?: species lists of three forest remnants. Biota Neotrop 4(1):01–12

    Article  Google Scholar 

  • Montes C, Cardona A, McFadden R, Morón SE, Silva CA, Restrepo-Moreno S et al (2012) Evidence for middle Eocene and younger land emergence in Central Panama: implications for isthmus closure. Geol Soc Am Bull 124:780–799

    Article  CAS  Google Scholar 

  • Morais PB, Rosa CA, Hagler AN, Mendonça-Hacler LC (1995) Yeast communities as descriptors of habitat use by the Drosophila fasciola subgroup (repleta group) in Atlantic rain forests. Oecologia 104:45–51

    Article  CAS  PubMed  Google Scholar 

  • Morrison DA (2007) Increasing the efficiency of searches for the maximum likelihood tree in a phylogenetic analysis of up to 150 nucleotide sequences. Syst Biol 56:988–1010

    Article  CAS  PubMed  Google Scholar 

  • Müller K (2004) PRAP—computation of Bremer support for large data sets. Mol Phylogenet Evol 31:780–782

    Article  PubMed  Google Scholar 

  • Muller KF (2005) SeqState—primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinforma 4:65–69

    Article  Google Scholar 

  • Novaes RML, Ribeiro RA, Lemos-Filho JP, Lovato MB (2014) Concordance between phylogeographical and biogeographical patterns in the Brazilian Cerrado: diversification of the endemic tree Dalbergia miscolobium (Fabaceae). PLoS One 8:e82198

  • Oliveira DC, Almeida FC, O’Grady PM, Armella MA, DeSalle R, Etges WJ (2012) Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group. Mol Phylogenet Evol 64:533–544

    Article  PubMed  Google Scholar 

  • Patterson JT, Wheeler MR (1942) Description of new species of the subgenera Hirtodrosophila and Drosophila. Univ Texas Publ 4213:67–109

    Google Scholar 

  • Pennington RT, Prado DE, Pendry CA (2000) Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr 27:261–273

  • Pereira MAQR, Vilela CR, Sene FM (1983) Notes on breeding and feeding sites of some species of the repleta group of the genus Drosophila (Diptera, Drosophilidae). Cienc Cult 35(9):1313–1319

    Google Scholar 

  • Pipkin SB (1965) The influence of adult and larval food habits on population size of neotropical ground-feeding Drosophila. Am Midl Nat 74:1–27

    Article  Google Scholar 

  • Pipkin SB, Rodriguez RL, Leon J (1966) Plant host specificity among flower-feeding neotropical Drosophila (Diptera: Drosophilidae). Am Nat 100:135–156

    Article  Google Scholar 

  • Rafael V, Arcos G (1989) Subgrupo inca, un nuevo subgrupo del grupo repleta, con descripcíon de Drosophila huancavilcae N.SP. (Diptera, Drosophilidae). Evol Biol 3:233–243

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Schmitz HJ, Valente VLS, Hofmann RP (2007) Taxonomic survey of Drosophilidae (Diptera) from mangrove forests of Santa Catarina Island, Southern Brazil. Neotrop Entomol 36(1):53–64

    Article  PubMed  Google Scholar 

  • Sene FM, Paganelli CHM, Pedroso LG, Garcia E, Palombo CR (1977) Local natural de criação de Drosophila onca Dobzhansky & Pavan, 1943. Cienc Cult 29(7):716

    Google Scholar 

  • Silva-Bernardi ECC, Morales AC, Sene FM, Manfrin MH (2006) Phylogenetic relationships in the Drosophila fasciola species subgroup (Diptera, Drosophilidae) inferred from partial sequences of the mitochondrial cytochrome oxidase subunit I (COI) gene. Genet Mol Biol 29(3):566–571

    Article  CAS  Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  CAS  PubMed  Google Scholar 

  • Simmons MP, Pickett KM, Miya M (2004) How meaningful are Bayesian support values? Mol Biol Evol 21:188–199

    Article  CAS  PubMed  Google Scholar 

  • Soto IM, Carreira VP, Corio C, Padró J, Soto EM, Hasson E (2014) Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii. PLoS One 10:e88370

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony and other methods. Version 4. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Tatarenkov A, Ayala FJ (2001) Phylogenetic relationships among species groups of the virilis-repleta radiation of Drosophila. Mol Phylogenet Evol 21(2):327–331

    Article  CAS  PubMed  Google Scholar 

  • Tidon-Sklorz R, Sene FM (1995) Fauna of Drosophila (Diptera, Drosophilidae) in the northern area of the “Cadeia do Espinhaço”, states of Minas Gerais and Bahia, Brazil: biogeographical and ecological aspects. Iheringia. Ser Zool 78:85–94

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Throckmorton LH (1975) The phylogeny, ecology and geography of Drosophila. In: King RC (ed) Handbook of Genetics. Plenum Press, New York, pp 421–459

    Google Scholar 

  • Turchetto-Zolet AC, Pinheiro F, Salgueiro S, Palma-Silva C (2013) Phylogeographical patterns shed light on evolutionary process in South America. Mol Ecol 22:1193–1213

  • Vilela CR (1983) A revision of the Drosophila repleta species group (Diptera, Drosophilidae). Rev Bras Entomol 27:1–114

  • Vilela CR, Bächli G (1990) Taxonomic studies on neotropical species of seven genera of Drosophilidae (Diptera). Mitt Schweiz Ent Ges 63:1–332

    Google Scholar 

  • Vilela CR, Mori L (1999) The genus Drosophila (Diptera, Drosophilidae) in the Serra do Cipó: further notes. Rev Bras Entomol 43:319–328

    Google Scholar 

  • Wasseman M (1960) Cytological and phylogenetic relationships in the repleta group of the genus Drosophila. Proc Nat Acad Sci 46:842–859

    Article  Google Scholar 

  • Wasserman M (1962) Cytological studies of the repleta group of the genus Drosophila: VI. The fasciola subgroup. Univ Texas Publ 6205:119–134

    Google Scholar 

  • Wasserman M (1982) Evolution of the repleta group. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology of Drosophila, vol 3b. Academic Press, London, pp 61–139

    Google Scholar 

  • Wasserman M (1992) Cytological evolution of the Drosophila repleta species group. In: Krimbas CB, Powell JR (eds) Drosophila Inversion Polymorphism. CRC Press, Boca Raton, pp 455–555

    Google Scholar 

  • Werneck FP (2011). The diversification of eastern South American open vegetation biomes: historical biogeography and perspectives. Quat Sci Rev 30:1630–1648

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Acknowledgements

We are particularly grateful to PR Epifânio for their technical assistance. This work was supported by several grants from Coordination for the Improvement of Higher Education Personnel (CAPES), National Counsel of Technological and Scientific Development (CNPq), University of São Paulo (USP) and São Paulo Research Foundation (FAPESP 03⁄05031-011/51652-2) to MHM.

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Authors and Affiliations

  1. Depto de Biologia, Centro de Ciências Humanas e Biológicas, Univ Federal de São Carlos, Rodovia João Leme dos Santos, Km 110, SP264, Sorocaba, 18052-780, Brasil

    F F Franco

  2. Secretaria do Meio Ambiente do Estado de São Paulo, São Paulo, Brasil

    E C C Silva

  3. Pós-Graduação do Depto de Genética—Faculdade de Medicina de Ribeirão Preto, Univ de São Paulo, São Paulo, Brasil

    D Y Barrios-Leal, F M Sene & M H Manfrin

  4. Depto de Biologia—Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Univ de São Paulo, Ribeirão Preto, Brasil

    F M Sene & M H Manfrin

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  1. F F Franco
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  2. E C C Silva
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  3. D Y Barrios-Leal
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  4. F M Sene
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Correspondence to F F Franco.

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Edited by Fernando B Noll – UNESP

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Franco, F.F., Silva, E.C.C., Barrios-Leal, D.Y. et al. The Calibrated Phylogeny of the Drosophila fasciola Subgroup (D. repleta Group Wasserman) Indicates Neogene Diversification of Its Internal Branches. Neotrop Entomol 46, 537–545 (2017). https://doi.org/10.1007/s13744-017-0484-4

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