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Type: Article
Published: 2021-06-01
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Integrative taxonomy and a new species description in the sturtevanti subgroup of the Drosophila saltans group (Diptera: Drosophilidae)

São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil.
São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil.
São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil.
São Paulo State University (UNESP), School of Pharmaceutical Sciences, Araraquara, São Paulo, Brazil.
São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil.
Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91198, Gif-sur-Yvette, France. Institut de Systématique, Évolution, Biodiversité (ISYEB), CNRS, EPHE, MNHN, Sorbonne Université, Univ. des Antilles, 57 rue Cuvier, CP 50, 75005 Paris, France.
Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91198, Gif-sur-Yvette, France.
Laboratory of Genome Dynamics, Department of Cell and Developmental Biology, Center for Anatomy, Medical University of Vienna, Austria.
Diptera Drosophilidae

Abstract


Although the biological concept of species is well established in animals, sometimes the decision about the specific status of a new species is difficult and hence requires support of an integrative analysis of several character sets. To date, the species Drosophila sturtevanti, D. magalhaesi, D. milleri and D. dacunhai, belonging to the sturtevanti subgroup of the Neotropical saltans species group, are identified mainly by the aedeagus morphology, but also present some differences in spot coloration and patterning of the female sixth tergite and in the shape and size of the spermathecae, parallel to a pattern of reproductive isolation. In the present study, we describe a novel saltans group species from French Guiana belonging to the sturtevanti subgroup. Our species designation is based on an integrative approach covering (i) aedeagi and spermathecae morphology by scanning electron microscopy, (ii) analysis of female sixth-tergite color, (iii) morphometrical analysis of aedeagi and wings, (iv) analysis of partial sequence of the COI, COII and ND4 mitochondrial genes as well as (v) intercrosses for analysis of reproductive isolation. The comparative analysis of the results on these markers with those of D. sturtevanti, D. milleri and D. dacunhai supports that this line belongs to a new species of the sturtevanti subgroup that we name Drosophila lehrmanae sp. nov. in honor of Prof. Lee Ehrman´s 85th birthday.

 

References

  1. Bächli, G. (2020) TaxoDros: The database on Taxonomy of Drosophilidae, v1.04, Database 2020/9. Available from: https://www.taxodros.uzh.ch/ (accessed 7 November 2020)

    Baião, G.C. (2020) Genomic and transcriptomic investigation of reproductive incompatibility in Drosophila. Acta Universitatis Upsaliensis, Uppsala, 69 pp.

    Ballard, J.W.O. (2000) Comparative genomics of mitochondrial DNA in members of the Drosophila melanogaster subgroup. Journal of Molecular Evolution, 51, 48–63.

    https://doi.org/10.1007/s002390010066

    Bernardo, A.A. & Bicudo, H.E.M.C. (2009) Variability of esterase patterns in adult flies of the saltans species group of Drosophila (subgenus Sophophora). Genetica, 137 (1), 111–124.

    https://doi.org/10.1007/s10709-009-9357-z

    Bicudo, H.E.M.C. (1979) Reproductive isolation in the saltans group of Drosophila. IV. The stutervanti subgroup. Revista Brasileira de Genética, 4, 247–258.

    Carareto, C.M.A. & Mourão, C.A. (1992) Darwinian fitness in Drosophila. III fitness componnts of Drosophila sturtevanti. Revista Brasileira de Genética, 15, 323–338.

    Dean, M.D. & Ballard, J.W.O. (2005) High divergence among Drosophila simulans mitochondrial haplogroups arose in midst of long-term purifying selection. Molecular Phylogenetics and Evolution, 36, 328–337.

    https://doi.org/10.1016/j.ympev.2005.02.016

    DeSalle, R., Egan, M.G. & Siddall, M. (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of The Royal Society, 360, 1905–1916.

    https://doi.org/10.1098/rstb.2005.1722

    Devescovi, F., Conte, C.A., Augustinos, A., Martinez, E.I.C., Segura, D.F., Caceres, C. Lanzavecchia, S.B. & Bourtzis, K. (2019) Symbionts do not affect the mating incompatibility between the Brazilian-1 and Peruvian morphotypes of the Anastrepha fraterculus cryptic species complex. Scientific Reports, 9, 18319.

    https://doi.org/10.1038/s41598-019-54704-y

    Dobzhansky, T. & Pavan, C. (1943) Studies on brazilian species of Drosophila. Separata do Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, 36, 7–72.

    Duda, O. (1927) Die sudamerikanischen Drosophiliden (Dipteren) unter Beruckssichtigung auch der anderen neotropischen sowie der nearktischen Arten. Archiv. Naturgesch, 91, 1–228.

    Ehrman, L. (1965) Direct Observation of Sexual Isolation between Allopatric and between Sympatric Strains of the Different Drosophila paulistorum Races. Evolution, 19 (4), 459–464.

    https://doi.org/10.1111/j.1558-5646.1965.tb03322.x

    Fallén, C.F. (1823) Geomyzides sveciae. Berlingianis, Lundae, 8 pp.

    Ferguson, J.W.H. (2002) On the use of genetic divergence for identifying species. Biological Journal of the Linnean Society, 75 (4), 509–516.

    https://doi.org/10.1046/j.1095-8312.2002.00042.x

    Franco, F.F., Prado, P.R.R, Sene, F.M., Costa, L.F. & Manfrin, M.H. (2006) Aedeagus morphology as a discriminant marker in two closely related Cactophilic species of Drosophila (Diptera; Drosophilidae) in South America. The Anais da Academia Brasileira de Ciências, 78 (2), 203–212.

    https://doi.org/10.1590/S0001-37652006000200002

    Freire-Maia, N. & Pavan, C. (1949) Introdução ao estudo de Drosophila, Cultus, 5, 71.

    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Symposium Series, 4, 95–98.

    Kaneshiro, K.Y. (1969) A study of the relationships of Hawaiian Drosophila species based on external male genitalia. University of Texas Publication, 6918, 55–70.

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.

    https://doi.org/10.1093/molbev/mst010

    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.

    https://doi.org/10.1007/BF01731581

    Kim, Y. (2005) Natural History of Lee Ehrman. Behavior Genetics, 35, 229–230. [2005]

    https://doi.org/10.1007/s10519-005-3215-2

    Kliman, R.M., Andolfatto, P., Coyne, J.A., Depaulis, F., Kreitman, M., Berry, A.J., McCarter, J., Wakeley, J. & Hey, J. (2000) The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics, 156, 1913–1931.

    https://doi.org/10.1093/genetics/156.4.1913

    Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.

    https://doi.org/10.1111/j.1755-0998.2010.02924.x

    Kobayashi, M.K. & Bicudo, H.E. (1997) Inversion polymorphism in laboratory strains and natural samples of Drosophila sturtevanti (saltans group, sturtevanti subgroup). Cytobios, 89 (356), 7–20.

    Kuhl, F.P. & Giardina, C.R. (1982) Elliptic Fourier Features of a Closed Contour. Computer Graphics and Images Processing, 18 (3), 236–258.

    https://doi.org/10.1016/0146-664X(82)90034-X

    Kulikov, A.M., Melnikov, A.I., Gornostaev, N.G., Lazebny, O.E. & Mitrofanov, V.G. (2004) Morphological analysis of male mating organ in the Drosophila virilis species group: a multivariate approach. Journal of Zoological Systematics and Evolutionary Research, 42 (2), 135–144.

    https://doi.org/10.1111/j.1439-0469.2004.00246.x

    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35 (6), 1547–1549.

    https://doi.org/10.1093/molbev/msy096

    Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34 (3), 772–773.

    https://doi.org/10.1093/molbev/msw260

    Lewis, Z., Crespigny, F.E.C., Sait, S.M., Tregenza, T. & Wedell, N. (2011) Wolbachia infection lowers fertile sperm transfer in a moth. Biology Letters, 7, 187–189.

    https://doi.org/10.1098/rsbl.2010.0605

    Li, Y.F., Wen, S.Y., Kawai, K., Gao, J.J., Hu, Y.G., Segawa, R. & Toda, M.J. (2012) DNA Barcoding and Molecular Phylogeny of Drosophila lini and Its Sibling Species. International Journal of Evolutionary Biology, 2012, 1–9.

    https://doi.org/10.1155/2012/329434

    Liu, H. & Beckenbach, A.T. (1992) Evolution of the mitochondrial cytochrome oxidase II gene among tem orders of insects. Molecular Phylogenetics Evolution, 1, 41–52.

    https://doi.org/10.1016/1055-7903(92)90034-E

    Loh, R, David, J.R., Debat, V. & Bitner-Mathé, B.C. (2008) Adaptation to different climates results in divergent phenotypic plasticity of wing size and shape in an invasive drosophilid. Journal of Genetics, 87 (3), 209–217.

    https://doi.org/10.1007/s12041-008-0034-2

    Magalhães, L.E. & Björnberg, A.J.S. (1957) Estudo da genitália masculina de “Drosophila” do grupo “saltans” (Diptera). Revista Brasileira de Biologia, 17, 435–450.

    Magalhães, L.E. (1962) Notes on the taxonomy, morphology and distribution of saltans group of Drosophila, with description of four new species. The University of Texas Publications, 6205, 135–154.

    Mardia, K.V., Kent, J.T. & Bibby, J.M. (1979) Multivariate Analysis. Academic Press, New York, 521 pp.

    Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York, New York, 334 pp.

    Miller, W.J., Ehrman, L. & Schneider, D. (2010) Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Pathogens, 6 (12), e1001214

    https://doi.org/10.1371/journal.ppat.1001214

    Moriyama, E.N. & Powell, J.R. (1997) Synonymous substitution rates in Drosophila: Mitochondrial versus nuclear genes. Journal of Molecular Evolution, 45, 378–391.

    https://doi.org/10.1007/PL00006243

    Mourão, C.A. & Bicudo, H.E.M.C. (1967) Duas espécies novas de Drosophila do grupo saltans (Drosophilidae, Diptera). Papéis avulsos de Zoologia, 12, 123–134.

    Nascimento, A.P. & Bicudo, H.E.M.C. (2002) Esterase patterns and phylogenetic relationships of Drosophila species in the saltans subgroup (saltans group). Genetica, 114, 41–51.

    https://doi.org/10.1023/A:1014672502359

    O’Grady, P.M., Clark, J.B. & Kidwell, M.G. (1998) Phylogeny of the Drosophila saltans species group based on combined analysis of nuclear and mitochondrial DNA sequences. Molecular Biology and Evolution, 15 (6), 656–664.

    https://doi.org/10.1093/oxfordjournals.molbev.a025969

    O’Grady, P.M. & Kidwell, M.G. (2002) Phylogeny of the Subgenus Sophophora (Diptera: Drosophilidae) Based on Combined Analysis of Nuclear and Mitochondrial Sequences, Molecular Phylogenetics and Evolution, 22, (3), 442–453.

    https://doi.org/10.1006/mpev.2001.1053.

    O’Grady, P.M. & DeSalle, R. (2018) Phylogeny of the Genus Drosophila. Genetics, 209, 1–25.

    https://doi.org/10.1534/genetics.117.300583

    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21 (8), 1868-1877.

    https://doi.org/10.1111/j.1365-294X.2011.05239.x

    Queiroz, K. (2007) Species Concepts and Species Delimitation. Systematic Biology, 56 (6), 879–886.

    https://doi.org/10.1080/10635150701701083

    Rambaut, A. (2009) FigTree, ver 1.4.3. Available from: http://tree.bio.ed.ac.uk/software/figtree (accessed 25 July 2020)

    Robe, L.J., Cordeiro, J., Loreto, E.L.S. & Valente, V.L.S. (2010) Taxonomic boundaries, phylogenetic relationships and biogeography of the Drosophila willistoni subgroup (Diptera: Drosphilidae). Genetica, 138, 601–617.

    https://doi.org/10.1007/s10709-009-9432-5

    Rodríguez-Trelles, F., Tarrío, R. & Ayala, F.J. (1999) Molecular Evolution and Phylogeny of the Drosophila saltans Species Group Inferred from the Xdh Gene. Molecular Phylogenetics and Evolution, 13 (1), 110–121.

    https://doi.org/10.1006/mpev.1999.0631

    Rohlf, F.J. (2005) tpsDig, digitize landmarks and outlines. Version 2.05. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.

    Roman, B.E. (2018) Reconstrução filogenética do grupo saltans de Drosophila utilizando marcadores morfológicos e moleculares. Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, 78 pp.

    Rondani, C.A. (1856) Dipterologiae italicae prodromus. Vol. 1. Ex tipografia Alexandri Stocchi, 245 pp.

    https://doi.org/10.5962/bhl.title.8160

    Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542.

    https://doi.org/10.1093/sysbio/sys029

    Satta, Y. & Takahata, N. (1990) Evolution of Drosophila mitochondrial DNA and the history of the melanogaster subgroup. Proceedings of the National Academy of Sciences of the United States of America, 87 (24), 9558–9562.

    https://doi.org/10.1073/pnas.87.24.9558

    Schaeffer, S.W. & Miller, E.L. (1991) Nucleotide sequence analysis of Adh genes estimates the time of geographic isolation of the Bogota population of Drosophila pseudoobscura. Proceedings of the National Academy of Sciences of the United States of America, 88 (14), 6097–6101.

    https://doi.org/10.1073/pnas.88.14.6097

    Schiffer, M., Carew, M.E. & Hoffmann, A.A. (2004) Molecular, morphological and behavioural data reveal the presence of a cryptic species in the widely studied Drosophila serrata species complex. Journal of Evolutionary Biology, 17, 430–442.

    https://doi.org/10.1046/j.1420-9101.2003.00657.x

    Schneider, D.I., Ehrman, L., Engl, T., Kaltenpoth. M., Hua-Van, A., Le Rouzic, A. & Miller, W.J. (2019), ‘Symbiont-driven male mating success in the Neotropical Drosophila paulistorum superspecies’, Behavior Genetics, 49 (1), 83–98.

    https://doi.org/10.1007/s10519-018-9937-8

    Segala, L.F. (2018) Diferenciação populacional em Drosophila sturtevanti (subgrupo sturtevanti, grupo saltans) avaliada por morfometria geométrica da asa e do edeago, Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, 106 pp.

    Silva, J.C. & Kidwell, M.G. (2004) Evolution of P Elements in natural populations of Drosophila willistoni and D. sturtevanti. Genetics, 168 (3), 1323–1335.

    https://doi.org/10.1534/genetics.103.025775

    Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Entomological Society of America, 87 (6), 651–701.

    https://doi.org/10.1093/aesa/87.6.651

    Soto, I.M., Carreira, V.P., Soto, E.M., Márquez, F., Lipko, P. & Hasson, E. (2013) Rapid divergent evolution of male genitalia among populations of Drosophila buzzatii. Evolutionary Biology, 40 (3), 395–407.

    https://doi.org/10.1007/s11692-013-9223-x

    Souza, T.A.J., Noll, F.B., Bicudo, H.E.M.C. & Madi-Ravazzi, L. (2014) Scanning Electron Microscopy of Male Terminalia and Its Application to Species Recognition and Phylogenetic Reconstruction in the Drosophila saltans Group. PLOS One, 9 (6), e97156.

    https://doi.org/10.1371/journal.pone.0097156

    Sperling, F.A.H. & Hickey, D.A. (1994) Mitochondrial DNA sequence variation in the spruce budworm species complex (Choristoneura: Lepidoptera). Molecular Biology and Evolution, 11, 656–665.

    Statsoft, Inc. (2004) Statistica (data analysis software system). Version 7. Available from: https://statistica.software.informer.com/7.0/ (accessed 3 May 2021)

    Sturtevant, A.H. (1916) Notes on North American Drosophilidae with descriptions of twenty-three new species. Annals of the Entomological Society of America, 9 (4), 323–343.

    https://doi.org/10.1093/aesa/9.4.323

    Sturtevant, A.H. (1939) On the subdivision of the genus Drosophila. Proceedings of the National Academy of Sciences, 25, 137–141.

    https://doi.org/10.1073/pnas.25.3.137

    Sturtevant, A.H. (1942) The classification of the genus Drosophila, with descriptions of nine new species. University of Texas Publications, 421, 5–51.

    Ting, C.T., Tsaur, S.C., Sun, S., Browne, W.E., Chen, Y.C., Patel, N.H. & Wu, C.I. (2004) Gene duplication and speciation in Drosophila: Evidence from the Odysseus locus. Proceedings of the National Academy of Sciences of the United States of America, 101 (33), 12232–12235.

    https://doi.org/10.1073/pnas.0401975101

    Torres, F.R. & Madi-Ravazzi, L. (2006) Seasonal variation in natural populations of Drosophila spp. (Diptera) in two woodland in the state of São Paulo, Brazil. Iheringia, Série Zoologia, 96 (4), 437–444.

    https://doi.org/10.1590/S0073-47212006000400008

    Trava, B.M. (2018) Estrutura populacional de Drosophila sturtevanti (subgrupo sturtevanti; grupo saltans) por meio de microssatélites espécie-específicos e biodiversidade de drosofilídeos em domínios da Mata Atlântica. Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, 124 pp.

    Vilela, C.R. & Bächli, G. (1990) Taxonomic studies on Neotropical species of seven genera of Drosophilidae (Diptera). Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 63, 1–332.

    Wang, R.L., Wakeley, J. & Hey, J. (1997) Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics, 147, 1091–1106.

    https://doi.org/10.1093/genetics/147.3.1091

    Watanabe, T.K. & Kawanishi, M. (1979) Mating Preference and the Direction of Evolution in Drosophila. Science, 205 (4409), 906–907.

    https://doi.org/10.1126/science.205.4409.906

    Yassin, A. (2009) Phylogenetic Relationships Among Species Subgroups in the Drosophila saltans Group (Diptera: Drosophilidae): Can Morphology Solve a Molecular Conflict? Zoological Research, 30, 225–232.

    https://doi.org/10.3724/SP.J.1141.2009.03225

    Zhang, A., Hao, M., Yang, C. & Shi, Z. (2017) BarcodingR: an integrated R package for species identification using DNA barcodes. Methods in Ecology and Evolution, 8, 627–634.

    https://doi.org/10.1111/2041-210X.12682

    Zanini, R., Müller, M.J., Vieira, G.C., Valiati, V.H., Deprá, M. & Valente, V.L. da S. (2018) Combining morphology and molecular data to improve Drosophila paulistorum (Diptera, Drosophilidae) taxonomic status. Fly, 12, 81–94.

    https://doi.org/10.1080/19336934.2018.1429859

    Zorzato, S.V. (2019) Filogeografia de Drosophila sturtevanti (Diptera: Drosophilidae) em biomas Neotropicais. Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, 98 pp.