Eur. J. Entomol. 121: 124-133, 2024 | DOI: 10.14411/eje.2024.015

Evidence of a South American origin for the Drosophila repleta group (Diptera: Drosophilidae)Original article

Andrea E. ACURIO ORCID...1, 2
1 Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain
2 Laboratory of Evolutionary Genetics, Institute of Entomology, Biology Centre, Czech Academy of Sciences, Brani¹ovská 31, 370 05 Èeské Budìjovice, Czech Republic; e-mail: andrea.acurio@entu.cas.cz

The Drosophila repleta group is one of the most widely used model systems for studying adaptation and speciation. Traditionally, five subgroups are recognized within the repleta group: fasciola, hydei, mercatorum, repleta and mulleri. A sixth subgroup, inca, was the last to be defined. The inca species subgroup includes three species: Drosophila inca, Drosophila huancavilcae and Drosophila yangana, all of which are endemic to Ecuador and Peru. Previous molecular phylogenetic studies have been inconclusive regarding the geographic location, time and mode of diversification of lineages within the repleta group. By applying a phylogenetic and biogeographical analysis of 54 taxa belonging to the repleta, nannoptera, atalaia and virilis groups, the aim of this study was to: (1) determine the relationships between the inca subgroup and the other five subgroups within the repleta group, (2) improve the unresolved branching and low supports of the early divergent lineages in the repleta group phylogeny and (3) estimate the geographic and temporal context of the early divergence within the repleta group. Based on these findings, it is proposed that the Drosophila repleta group first diversified during the mid-late Miocene, most likely following the uplift of the Northwestern Andes.

Keywords: repleta lineage, evolutionary relationships, systematics, phylogeny, biogeography

Received: December 7, 2023; Revised: March 18, 2024; Accepted: March 18, 2024; Published online: March 26, 2024  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
ACURIO, A.E. (2024). Evidence of a South American origin for the Drosophila repleta group (Diptera: Drosophilidae). EJE, 121, Article 124-133. https://doi.org/10.14411/eje.2024.015
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Acurio A. & Rafael V. 2009a: Diversity and geographical distribution of Drosophila (Diptera, Drosophilidae) in Ecuador. - Drosophila Inform. Serv. 92: 20-25.
    2. Acurio A. & Rafael V. 2009b: Taxonomic survey of Drosophilidae (Diptera) in the Yasuni National Park, Ecuadorian Amazon. - Acta Amazon. 39: 713-718. Go to original source...
    3. Acurio A.E., Rafael V., Céspedes D. & Ruiz A. 2013: Description of a new spotted-thorax Drosophila (Diptera: Drosophilidae) species and its evolutionary relationships inferred by a cladistic analysis of morphological traits. - Ann. Entomol. Soc. Am. 106: 695-705. Go to original source...
    4. Acurio A.E., Rhebergen F.T., Paulus S., Courtier-Orgogozo V. & Lang M. 2019: Repeated evolution of asymmetric genitalia and right-sided mating behavior in the Drosophila nannoptera species group. - BMC Evol. Biol. 19: 109, 14 pp. Go to original source...
    5. Arakaki M., Christin P.A., Nyffeler R., Lendel A., Eggli U., Ogburn R.M., Spriggs E., Moore M.J. & Edwards E.J. 2011: Contemporaneous and recent radiations of the world's major succulent plant lineages. - Proc. Natn. Acad. Sci. U. S. A. 108: 8379-8384. Go to original source...
    6. Bonacum J., DeSalle R., O'Grady P., Oliveira D., Wintermute J. & Zilversmit M. 2001: New nuclear and mitochondrial primers for systematics and comparative genomics in Drosophilidae. - Drosophila Inform. Serv. 84: 201-204.
    7. Calderón-Cortés N., Quesada M., Cano-Camacho H. & Zavala-Páramo G. 2010: A simple and rapid method for DNA isolation from xylophagous insects. - Int. J. Mol. Sci. 11: 5056-5064. Go to original source...
    8. Capitanio F.A., Faccenna C., Zlotnik S. & Stegman D.R. 2011: Subduction dynamics and the origin of Andean orogeny and the Bolivian orocline. - Nature 480: 83-86. Go to original source...
    9. Daly M. 1989: Correlations between Nazca-Farallon Plate kine­matics and forearc basin evolution in Ecuador. - Tectonics 8: 769-790. Go to original source...
    10. Darriba D., Taboada G.L., Doallo R. & Posada D. 2012: jModelTest 2: more models, new heuristics and parallel computing. - Nat. Meth 9: 772. Go to original source...
    11. Descimon H. 1986: Origins of lepidopteran faunas in the high tropical Andes. In Vuilleumier F. & Monasterio M. (eds): High Altitude Tropical Biogeography. Oxford University Press, Oxford, pp. 500-532.
    12. Dobzhansky T. & Pavan C. 1943: Studies on Brazilian species of Drosophila. - Bol. Fac. Filos. Cienc. Letr. Univ. S. Paulo (Biol. Ger.) 36: 7-72.
    13. Drummond A.J. & Rambaut A. 2007: BEAST: Bayesian evolutionary analysis by sampling trees. - BMC Evol Biol, 7. Go to original source...
    14. Drummond A.J., Suchard M.A., Xie D. & Rambaut A. 2012: Bayesian phylogenetics with BEAUti and the BEAST 1.7. - Mol. Biol. Evol. 29: 1969-1973. Go to original source...
    15. Duellman W.E. & Wild E.R. 1993: Anuran amphibians from the Cordillera de Huancabamba, northern Peru: systematics, ecology, and biogeography. - Occas. Pap. Mus. Nat. Hist. Univ. Kansas 157: 1-53.
    16. Durando C.M., Baker R.H., Etges W.J., Heed W.B., Wasserman M. & DeSalle R. 2000: Phylogenetic analysis of the repleta species group of the genus Drosophila using multiple sources of characters. - Mol. Phylogen. Evol. 16: 296-307. Go to original source...
    17. Figuero M.L., Rafael V. & Céspedes D. 2012: Grupo Drosophila asiri (Diptera, Drosophilidae), un nuevo grupo de especies andinas con la descripción de dos nuevas especies y la redescripción de Drosophila asiri. - Iheringia (Zool.) 102: 33-42. Go to original source...
    18. Fontdevila A., Wasserman M., Pla C., Pilares L., De Armengol R., Suyo M. del P., Sanchez A., Vasquez J., Ruiz A. & Garcia J.L. 1990: Description and evolutionary relationships of two species of the Drosophila mulleri cluster (Diptera: Dro­so­philidae). - Ann. Entomol. Soc. Am. 83: 444-452. Go to original source...
    19. Gregory-Wodzicki K.M. 2000: Uplift history of the Central and Northern Andes: a review. - Geol. Soc. Am. Bull. 112: 1091-1105. Go to original source...
    20. Guillén Y., Rius N., Delprat A., Williford A., Muyas F., Puig M., Casillas S., Ràmia M., Egea R., Negre B. et al. 2014: Genomics of ecological adaptation in cactophilic Drosophila. - Genome Biol. Evol. 7: 349-366. Go to original source...
    21. Hedtke S.M., Townsend T.M. & Hillis D.M. 2006: Resolution of phyloegenetic conflict in large data sets by increasing taxon sampling. - Syst. Biol. 55: 522-529. Go to original source...
    22. Hoorn C., Palazzesi L. & Silvestro D. 2022: Editorial preface to special issue: Exploring the impact of Andean uplift and climate on life evolution and landscape modification: From Amazonia to Patagonia. - Glob. Planet. Change 211: 103759, 6 pp. Go to original source...
    23. Katoh K., Asimenos G. & Toh H. 2009: Multiple alignment of DNA sequences with MAFFT. In Posada D. (ed.): Bioinformatics for DNA Sequence Analysis. Vol. 537. Humana Press, Totowa, NJ, pp. 39-64. Go to original source...
    24. Lang M., Polihronakis Richmond M., Acurio A.E., Markow T.A. & Orgogozo V. 2014: Radiation of the Drosophila nannoptera species group in Mexico. - J. Evol. Biol. 27: 575-584. Go to original source...
    25. Liu H. & Beckenbach A.T. 1992: Evolution of the mitochondrial cytochrome oxidase II gene among ten orders of insects. - Mol. Phylog. Evol. 41: 31-52. Go to original source...
    26. Liu K., Warnow T.J., Holder M.T., Nelesen S.M., Yu J., Stamatakis A.P. & Linder C.R. 2012: SATé-II: Very fast and accurate simultaneous estimation of multiple sequence alignments and phylogenetic trees. - Syst. Biol. 61: 90-106. Go to original source...
    27. Llangarí-Arizo L.M. & Rafael V. 2020: Five new species of Drosophila (Diptera, Drosophilidae) related with Araceae. - Iheringia (Zool.) 110: e2020012, 13 pp. Go to original source...
    28. Loaiza C. & Morrone J. 2011: Análisis panbiogeográfico de algunas Cactaceae del Ecuador. - Gayana Bot. 68: 220-225. Go to original source...
    29. Maddison W.P. & Maddison D.R. 2010: Mesquite: A Modular System for Evolutionary Analysis, Version 2.74. URL: http://mesquiteproject.org
    30. Mafla M.A.B. & Romero E.G. 2009: The heterocromatin of Drosophila inca, Drosophila yangana and Drosophila huancavilcae of the inca subgroup, repleta group. - Dros. Inf. Serv. 92: 10-15.
    31. Matzke N.J. 2013: BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis in R Scripts. R Package, Version 0.2.1. URL: https://github.com/nmatzke/BioGeoBEARS.
    32. Montes C., Cardona A., McFadden R., Morón S.E., Silva C.A., Restrepo-Moreno S., Ramírez D.A., Hoyos N., Wilson J. & Farris D. 2012: Evidence for middle Eocene and younger land emergence in central Panama: Implications for Isthmus closure. - Geol. Soc. Am. Bull. 124: 780-799. Go to original source...
    33. Morales-Hojas R. & Vieira J. 2012: Phylogenetic patterns of geographical and ecological diversification in the subgenus Drosophila. - PLoS ONE 7(11): e49552, 15 pp. Go to original source...
    34. Moriyama E. & Powell J. 1997: Synonymous substitution rates in Drosophila: Mitochondrial versus nuclear genes. - J. Mol. Evol. 45: 378-391. Go to original source...
    35. Nabhan A.R. & Sarkar I.N. 2012: The impact of taxon sampling on phylogenetic inference: A review of two decades of controversy. - Briefings Bioinform. 13: 122-134. Go to original source...
    36. O'Grady P.M. & DeSalle R. 2018: Phylogeny of the genus Drosophila. - Genetics 209: 1-25. Go to original source...
    37. Obbard D.J., Maclennan J., Kim K.-W., Rambaut A., O'Grady P.M. & Jiggins F.M. 2012: Estimating divergence dates and substitution rates in the Drosophila phylogeny. - Mol. Biol. Evol. 29: 3459-3473. Go to original source...
    38. Oliveira D.C.S.G., O'Grady P.M., Etges W.J., Heed W.B. & DeSalle R. 2005: Molecular systematics and geographical distribution of the Drosophila longicornis species complex (Diptera: Drosophilidae). - Zootaxa 1069: 1-32. Go to original source...
    39. Oliveira D.C.S.G., Leonidas M., Etges W.J., O'Grady P.M. & Desalle R. 2008: Species delimitation in the Drosophila aldrichi subcluster (Diptera: Drosophilidae) using DNA sequences. - Zootaxa 1725: 37-47. Go to original source...
    40. Oliveira D.C.S.G., Almeida F.C., O'Grady P.M., Armella M.A., DeSalle R. & Etges W.J. 2012: Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group. - Mol. Phylogen. Evol. 64: 533-544. Go to original source...
    41. Patterson J.T. & Mainland G.B. 1945: The Drosophilidae of Mexico. University of Texas, Austin, TX, 101 pp.
    42. Patterson J.T. & Stone W.S. 1952: Evolution in the Genus Drosophila. Macmillan, New York, 610 pp.
    43. Pfeiler E. 2019: Genetic diversity and demographic history in the cactophilic Drosophila repleta species group (Di­pte­ra: Drosophilidae) in North America inferred from mitochondrial DNA barcodes. - J. Heredity 110: 34-45. Go to original source...
    44. Posada D. 2008: jModelTest: Phylogenetic model averaging. - Mol. Biol. Evol. 25: 1253-1256. Go to original source...
    45. R Development Core Team 2011: R: A language and environment for statistical computing. In R. D. C. Team (ed.): R Foundation for Statistical Computing. Vol. 1, Issue 2.11.1. R Foundation for Statistical Computing, p. 409.
    46. Rafael V. & Arcos G. 1989: Subgrupo inca, un nuevo subgrupo del grupo repleta, con desacripción de Drosophila huancavilcae n. sp (Diptera, Drosophilidae). - Evolución Biológica 3: 233-243.
    47. Rafael V. & Vela D. 2003: Drosophila yangana sp. nov. un nuevo miembro del grupo repleta, subgrupo inca (Diptera: Drosophilidae). - Revta Pontif. Univ. Catol. Ecuador 71: 129-139.
    48. Ramos V.A. 2009: Anatomy and global context of the Andes: Main geologic features and the Andean orogenic cycle. - Mem. Geol. Soc. Am. 204: 31-65. Go to original source...
    49. Ree R.H. & Smith S.A. 2008: Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. - Syst. Biol. 57: 4-14. Go to original source...
    50. Reig O.A. 1986: Diversity patterns and differentiation of high Andean rodents. In Vuilleumier F. & Monasterio M. (eds): High Altitude Tropical Biogeography. Oxford University Press, Oxford, pp. 404-439.
    51. Russo C.a.M., Mello B., Frazão A. & Voloch C.M. 2013: Phylogenetic analysis and a time tree for a large drosophilid data set (Diptera: Drosophilidae). - Zool. J. Linn. Soc. 169: 765-775. Go to original source...
    52. Soares A.E.R. & Schrago C.G. 2015: The influence of taxon sampling on Bayesian divergence time inference under scenarios of rate heterogeneity among lineages. - J. Theor. Biol. 364: 31-39. Go to original source...
    53. Stefanini M.I., Gottschalk M.S., Calvo N.S. & Soto I.M. 2021: Evolution of male genitalia in the Drosophila repleta species group (Diptera: Drosophilidae). - J. Evol. Biol. 34: 1488-1502. Go to original source...
    54. Sturtevant A.H. 1915: A sex-linked character in Drosophila repleta. - Am. Nat. 49: 189-192. Go to original source...
    55. Sturtevant A.H. 1921: The North American Species of Droso­phila. Carnegie Institute, Washington, iv + 150 pp. + 3 pl. Go to original source...
    56. Throckmorton L.H. 1975: The phylogeny, ecology and geography of Drosophila. In King R.C. (ed.): Handbook of Genetics Vol. 3. Plenum, New York, pp. 421-469. Go to original source...
    57. Townsend J.P. & Leuenberger C. 2011: Taxon sampling and the optimal rates of evolution for phylogenetic inference. - Syst. Biol. 60: 358-365. Go to original source...
    58. Vilela C.R. 1983: A revision of the Drosophila repleta species group (Diptera, Drosophilidae). - Revta Bras. Entomol. 27: 1-114.
    59. Vilela C.R. & Bächli G. 1990: Taxonomic studies on Neotropical species of seven genera of Drosophilidae (Diptera). - Mitt. Schweiz. Entomol. Ges. (Suppl.) 63: 332 pp.
    60. Vuilleumier F. 1969: Pleistocene speciation in birds living in the High Andes. - Nature 223: 1179-1180. Go to original source...
    61. Wasserman M. 1992: Cytological evolution of the Drosophila repleta species group. In Powell J.R. & Krimbas C.B. (eds): Inversion Polymorphism in Drosophila. CRC Press, Boca Raton, FL, pp. 455-541.
    62. Weir J.T. & Price M. 2011: Andean uplift promotes lowland speciation through vicariance and dispersal in Dendrocincla woodcreepers. - Mol. Ecol. 20: 4550-4563. Go to original source...
    63. Wharton L.H. 1942: Analysis of the repleta group of Drosophila. - Univ. Texas Publ. 4228: 23-52.
    64. Young K.R. & Reynel C. 1997: Huancabamba region, Peru and Ecuador. In Davis S.D, Heywood V.H., Herrera-MacBryde O., Villa-Lobos J. & Hamilton A.C. (eds): Centres of Plant Diversity: A Guide and Strategy for their Conservation, 3: North America, Middle America, South America, Caribbean Islands. IUCN, Geneva, pp. 465-469.

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content