Skip to main content
Log in

Molecular evidence to suggest the origin of a colonization: Drosophila subobscura in America

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The recent colonization of America by Drosophila subobscura represents a great opportunity for evolutionary biology studies. Knowledge of the populations from which the colonization started would provide an understanding of how genetic composition changed during adaptation to the new environment. Thus, a 793 nucleotide fragment of the Odh (Octanol dehydrogenase) gene was sequenced in 66 chromosomal lines from Barcelona (western Mediterranean) and in 66 from Mt. Parnes (Greece, eastern Mediterranean). No sequence of Odh fragment in Barcelona or Mt. Parnes was identical to any of those previously detected in America. However, an Odh sequence from Barcelona differed in only one nucleotide from another found in American populations. In both cases, the chromosomal lines presented the same inversion: O7, and the Odh gene was located within this inversion. This evidence suggests a possible western Mediterranean origin for the colonization. Finally, the molecular and inversion data indicate that the colonization was not characterized by multiple reintroductions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Araúz PA, Mestres F, Pegueroles C, Arenas C, Tzannidakis G, Krimbas CB, Serra L (2009a) Tracking the origin of the American colonization by D. subobscura: Genetic comparison between Eastern and Western Mediterranean populations. J Zool Syst Evol Res 47:25–34

    Article  Google Scholar 

  • Araúz PA, Pegueroles C, Zivanovic G, Fernández-Iriarte PJ, Ruiz-Martín H, Balanyà J, Serra L, Mestres F (2009b) Recent origin of a chromosomal inversion revealed by its association with nucleotide haplotypes. Hereditas 146:257–259

    Article  PubMed  Google Scholar 

  • Ayala FJ, Serra L, Prevosti A (1989) A grand experiment in evolution: the D. subobscura colonization of the Americas. Genome 31:246–255

    Article  Google Scholar 

  • Balanyà J, Segarra C, Prevosti A, Serra L (1994) Colonization of America by D. subobscura: the founder event and a rapid expansion. J Hered 85:427–432

    PubMed  Google Scholar 

  • Balanyà J, Serra L, Gilchrist GW, Huey RB, Pascual M, Mestres F, Solé E (2003) Evolutionary pace of chromosomal polymorphism in colonizing populations of D. subobscura: an evolutionary time series. Evolution 57:1837–1845

    PubMed  Google Scholar 

  • Beckenbach AT, Prevosti A (1986) Colonization of North America by the European species D. subobscura and D. ambigua. The Am Midl Nat 115:10–18

    Article  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Brncic D, Prevosti A, Budnik M, Monclús M, Ocaña J (1981) Colonization of D. subobscura in Chile. I. First population and cytogenetic studies. Genetica 56:3–9

    Article  Google Scholar 

  • Capy P, Gibert P (2004) Drosophila melanogaster, Drosophila simulans: so similar yet so different. Genetica 120:5–16

    Article  PubMed  CAS  Google Scholar 

  • Cirera S, Aguadé M (1998) Molecular evolution of duplication: the sex-peptide (Acp70A) gene region of D. subobscura and D. madeirensis. Mol Biol Evol 15:988–996

    Article  PubMed  CAS  Google Scholar 

  • Davies N, Villablanca FX, Roderick GK (1999) Bioinvasions of the Medfly Ceratitis capitata: source estimation using DNA sequences at multiple intron loci. Genetics 153:351–360

    PubMed  CAS  Google Scholar 

  • Dlugosh KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  Google Scholar 

  • Ellstrand NC, Schierenbek KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Iriarte PJ, Balanyà J, Pascual M, Mestres F, Hasson E, Fontdevila A, Serra L (2009) Tracking the origin of an invasive species: D. subobscura in Argentina. J Evol Biol 22:650–658

    Article  PubMed  Google Scholar 

  • Fontdevila A (1989) Founder effects in colonizing populations: the case of Drosophila buzzatii. In: Fontdevila A (ed) Evolutionary biology of transient unstable populations. Springer, Berlin, pp 74–95

    Chapter  Google Scholar 

  • Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385

    Article  PubMed  CAS  Google Scholar 

  • Gilchrist GW, Huey RB, Serra L (2001) Rapid evolution of wing size clines in D. subobscura. Genetica 112–113:273–286

    Article  PubMed  Google Scholar 

  • Goldschmidt E (1956) Chromosomal polymorphism in a population of D. subobscura from Israel. J Genet 54:474–496

    Article  Google Scholar 

  • Gómez-Baldó L, Latorre A, Serra L, Mestres F (2008) Molecular variation in the Odh gene in Chilean natural populations of D. subobscura. Hereditas 145:154–162

    Article  Google Scholar 

  • Gouin N, Granjean F, Pain S, Souty-Grosset C, Reynolds J (2003) Origin and colonization history of the white-clawed crayfish, Austropotamobius pallipes, in Ireland. Heredity 91:70–77

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Hess JE, Swalla BJ, Moran P (2009) New molecular markers to genetically differentiate populations of Didemnum vesillum (Kott, 2002): an invasive ascidian species. Aquat Invasions 4:299–310

    Article  Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Huey RB, Gilchrist GW, Hendry AP (2005) Using invasive species to study evolution. Case studies with Drosophila and Salmon. In: Sax DF, Gaines SD, Stachowicz JJ (eds) Species invasions: insights to ecology evolution and biogeography. Sinauer Associates, Sunderland, MA, pp 139–164

    Google Scholar 

  • Keller A (2007) Drosophila melanogaster’s history as a human commensal. Current Biol 17:R77–R81

    Article  CAS  Google Scholar 

  • Krafsur ES, Cummings MA, Endsley MA, Marquez JG, Nason JD (2005) Geographic differentiation in the house fly estimated by microsatellite and mitochondrial variation. J Hered 96:502–512

    Article  PubMed  CAS  Google Scholar 

  • Krimbas CB (1964) The genetics of D. subobscura populations. I. Inversion polymorphism in natural populations of Southern Greece. Evolution 18:541–552

    Article  Google Scholar 

  • Krimbas CB (1967) The genetics of D. subobscura populations. III. Inversion polymorphism and climatic factors. Mol Gen Genet 99:133–150

    Article  PubMed  CAS  Google Scholar 

  • Krimbas CB (1992) The inversion polymorphism in D. subobscura. In Krimbas CB, Powell JR (eds) Drosophila inversion polymorphism. CRC Press Inc., Boca Raton, pp 127–220

  • Krimbas CB (1993) D. subobscura: Biology, Genetics and Inversion polymorphism. Verlag Dr. Kovac, Hamburg

  • Krimbas CB, Alevizos V (1973) The genetics of D. subobscura populations. IV. Further data on inversion polymorphism in Greece: evidence of microdifferentiation. Egypt J Genet Cytol 2:121–132

    Google Scholar 

  • Latorre A, Moya A, Ayala FJ (1986) Evolution of mitochondrial DNA in D. subobscura. Proc Natl Acad Sci USA 83:8649–8653

    Article  PubMed  CAS  Google Scholar 

  • Latorre A, Hernandez C, Martinez D, Castro JA, Ramon M, Moya A (1992) Population structure and mitochondrial DNA gene flow in Old World populations of Drosophila subobscura. Heredity 68:15–24

    Article  PubMed  CAS  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Biol 17:386–391

    Article  Google Scholar 

  • Liggins L, Chapple DG, Daugherty CH, Ritchie PA (2008) Origin and post-colonization evolution of the Chatham Islands skink (Oligosoma nigroplantare nigroplantare). Mol Ecol 17:3290–3305

    Article  PubMed  CAS  Google Scholar 

  • Llopart A, Aguadé M (2000) Nucleotide polymorphism at the RpII215 gene in D. subobscura: Weak selection on synonymous mutations. Genetics 155:1245–1252

    PubMed  CAS  Google Scholar 

  • Loukas M, Krimbas CB, Vergini Y (1979) The genetics of D. subobscura populations. IX. Studies on linkage disequilibrium in four natural populations. Genetics 93:497–523

    PubMed  CAS  Google Scholar 

  • Loukas M, Krimbas CB, Morgan K (1980) The genetics of D. subobscura populations. XIV. Further data on linkage disequilibria. Genetics 95:757–768

    PubMed  CAS  Google Scholar 

  • Loukas M, Vergini Y, Krimbas CB (1981) The genetics of D. subobscura populations. XVII. Further genetic heterogeneity within electromorphs by urea denaturation and the effect of the increased genic variability on linkage disequilibrium studies. Genetics 97:429–441

    PubMed  CAS  Google Scholar 

  • Malogolowkin-Cohen C, Sperlich D (1981) The effect of isolation and marginality on the inversion polymorphism of D. subobscura in Israel. Rev Bras Genet 2:213–230

    Google Scholar 

  • Mestres F, Pegueroles G, Prevosti A, Serra L (1990) Colonization of America by D. subobscura: lethal genes and the problem of the O5 inversion. Evolution 44:1823–1836

    Article  Google Scholar 

  • Mestres F, Balanyà J, Segarra C, Prevosti A, Serra L (1992) Colonization of America by D. subobscura: analysis of the O5 inversions from Europe and America and their implications for the colonizing process. Evolution 46:1564–1568

    Article  Google Scholar 

  • Mestres F, Balanyà J, Segarra C, Prevosti A, Serra L (1994) O chromosome inversion polymorphism in Northern and Atlantic Europe and its implications in the American colonization of D. subobscura. Z Zool Syst Evol Forsch 32:108–116

    Article  Google Scholar 

  • Mestres F, Serra L, Ayala FJ (1995) Colonization of the Americas by D. subobscura: lethal-gene allelism and association with chromosomal arrangements. Genetics 140:1297–1305

    PubMed  CAS  Google Scholar 

  • Mestres F, Balanyà J, Arenas C, Solé E, Serra L (2001) Colonization of America by D. subobscura: heterotic effect of chromosomal arrangements revealed by the persistence of lethal genes. Proc Natl Acad Sci USA 98:9167–9170

    Article  PubMed  CAS  Google Scholar 

  • Mestres F, Abad L, Sabater-Muñoz B, Latorre A, Serra L (2004) Colonization of America by D. subobscura: Association between Odh gene haplotypes, lethal genes and chromosomal arrangements. Genes Genet Syst 79:233–244

    Article  PubMed  CAS  Google Scholar 

  • Mestres F, Balanyà J, Pascual M, Arenas C, Solé E, Serra L (2005) Lethal genes and the colonization of America by D. subobscura. Curr Top Genet 1:31–55

    CAS  Google Scholar 

  • Mestres F, Balanyà J, Pascual M, Arenas C, Gilchrist GW, Huey RB, Serra L (2009) Evolution of Chilean colonizing populations of D. subobscura: lethal genes and chromosomal arrangements. Genetica 136:37–48

    Article  PubMed  CAS  Google Scholar 

  • Munté A, Rozas J, Aguadé M, Segarra C (2005) Chromosomal inversion polymorphism leads to extensive genetic structure: a multilocus survey in D. subobscura. Genetics 169:1573–1581

    Article  PubMed  Google Scholar 

  • Nardon C, Deceliere G, Loevenbruck C, Weiss M, Vieira C, Biémont C (2005) Is genome size influenced by colonization of new environments in dipteran species? Mol Ecol 14:869–878

    Article  PubMed  CAS  Google Scholar 

  • Navarro-Sabaté A, Aguadé M, Segarra C (1999) The relationship between allozyme and chromosomal polymorphism inferred from nucleotide variation at the Acph-1 gene region of D. subobscura. Genetics 153:871–889

    PubMed  Google Scholar 

  • Novak SJ, Mack RN (2005) Genetic bottlenecks in alien plant species: influence of mating systems and introduction dynamics. In: Sax DF, Gaines SD, Stachowicz JJ (eds) Exotic species–bane to conservation and boon to understanding: ecology, evolution and biogeography. Sinauer Associates, Sunderland, MA, pp 95–122

    Google Scholar 

  • Pascual M, Balanyà J, Latorre A, Serra L (1997) Analysis of the variability of D. azteca and D. athabasca populations revealed by randomly amplified polymorphic DNA. J Zool Syst Evol Res 35:159–164

    Article  Google Scholar 

  • Pascual M, Aquadro CF, Soto V, Serra L (2001) Microsatellite variation in colonizing and Palearctic populations of D. subobscura. Mol Biol Evol 18:731–740

    Article  PubMed  CAS  Google Scholar 

  • Pascual M, Chapuis MP, Mestres F, Balanyà J, Huey RB, Gilchrist GW, Serra L, Estoup A (2007) Introduction history of D. subobscura in the New World: a microsatellite-based survey using ABC methods. Mol Ecol 16:3069–3083

    Article  PubMed  CAS  Google Scholar 

  • Pinsker W, Sperlich D (1981) Geographic pattern of allozyme and inversion polymorphism in chromosome O of D. subobscura. Genetica 57:51–64

    Article  Google Scholar 

  • Prevosti A, de Frutos R, Alonso G, Latorre A, Monclús M, Martínez MJ (1984) Genetic differentiation between natural populations of D. subobscura in the Western Mediterranean area with respect to chromosomal variation. Génét Sél Evol 16:143–156

    Article  Google Scholar 

  • Prevosti A, Serra L, Ribó G, Aguadé M, Sagarra E, Monclús M, García MP (1985) The colonization of D. subobscura in Chile. II. Clines in the chromosomal arrangements. Evolution 39:838–844

    Article  Google Scholar 

  • Prevosti A, Ribó G, Serra L, Aguadé M, Balanyà J, Monclús M, Mestres F (1988) Colonization of America by D. subobscura: experiment in natural populations that supports the adaptive role of chromosomal–inversion polymorphism. Proc Natl Acad Sci USA 85:5597–5600

    Article  PubMed  CAS  Google Scholar 

  • Prevosti A, Serra L, Aguadé M, Ribó G, Mestres F, Balañá J, Monclús M (1989) Colonization and establishment of the palearctic species D. subobscura in North and South America. In: Fontdevila A (ed) Evolutionary biology of transient unstable populations. Springer, Berlin, pp 114–129

  • Prevosti A, Serra L, Segarra C, Aguadé A, Ribó G, Monclús M (1990) Clines of chromosomal arrangements of D. subobscura in South America evolve closer to Old World patterns. Evolution 44:218–221

    Article  Google Scholar 

  • Reiland J, Hodge S, Noor MAF (2002) Strong founder effect in Drosophila pseudoobscura colonizing New Zealand from North America. J Hered 93:415–420

    Article  PubMed  CAS  Google Scholar 

  • Rius M, Pascual P, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14:818–828

    Article  Google Scholar 

  • Rozas J, Aguadé M (1990) Evidence of extensive genetic exchange in the rp49 region among polymorphic chromosome inversions in D. subobscura. Genetics 126:417–426

    PubMed  CAS  Google Scholar 

  • Rozas J, Aguadé M (1991) Using restriction-map analysis to characterize the colonization process of D. subobscura on the American continent. I. rp49 region. Mol Biol Evol 8:447–457

    CAS  Google Scholar 

  • Rozas J, Hernández M, Cabrera CV, Prevosti A (1990) Colonization of America by D. subobscura: Effect of the founder event on the mitochondrial DNA polymorphism. Mol Biol Evol 7:103–109

    PubMed  CAS  Google Scholar 

  • Rozas J, Segarra C, Zapata C, Alvarez G, Aguadé M (1995) Nucleotide polymorphism at the rp49 region of D. subobscura: lack of geographic subdivision within chromosomal arrangements in Europe. J Evol Biol 8:355–367

    Article  CAS  Google Scholar 

  • Rozas J, Segarra C, Ribó G, Aguadé M (1999) Molecular population genetics of the rp49 gene region in different chromosomal inversions of D. subobscura. Genetics 151:189–202

    PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Martín H (2006) Estudi de les associacions entre al.lels de loci microsatel.lits i inversions cromosòmiques en poblacions europees i colonitzadores de D. subobscura. Diploma d’Estudis Avançats. Dept. Genètica, Universitat de Barcelona, Spain

  • Solé E, Balanyà J, Sperlich D, Serra L (2002) Long-term changes in the chromosomal inversion polymorphism of D. subobscura. I. Mediterranean populations from Southwestern Euope. Evolution 56:830–835

    PubMed  Google Scholar 

  • Sperlich D (1964) Chromosomale Strukturanalyse und Fretilitätsprünfung an einer Marginalpopulation von D. subobscura. Z Vererbungsl 95:73–81

    Article  PubMed  CAS  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tollenaere C, Brouart C, Duplantier J-M, Rahalison L, Rahelinirina S, Pascal M, Moné H, Mouahid G, Leirs H, Cosson J-F (2010) Phylogeography of the introduced species Rattus rattus in the western Indian Ocean, with special emphasis on the colonization history of Madagascar. J Biogeogr 37:398–410

    Article  Google Scholar 

  • Wright S, Dobzhansky Th, Hovanitz W (1942) Genetics of natural populations. VII. The allelism of lethals in the third chromosome of D. pseudoobscura. Genetics 27:363–394

    PubMed  CAS  Google Scholar 

  • Zivanovic G, Mestres F (2000) Lethal genes in O5 chromosomes of D. subobscura from Europe and America. J Zool Syst Evol Res 38:123–126

    Article  Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2007) The genetic structure of Balkan populations of D. subobscura. Hereditas 144:120–128

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Mr. R. Rycroft and Mr. M. Bunn (S.A.L. Universitat de Barcelona) for corrections to the English text. This study was supported by the following grants: CGL2006-13423-C02-02 from the Ministerio de Ciencia y Tecnología (MCYT, Spain), BFU2009-07564 and BFU2009-12895-CO2-01 from the Ministerio de Ciencia e Innovación (Spain) and 2009 SGR 636 from the Generalitat de Catalunya (Spain). FM is member of IRBio (Institut de Recerca de la Biodiversitat).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francesc Mestres.

Additional information

Pedro A. Araúz and Francesc Peris-Bondia contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10709_2012_9647_MOESM1_ESM.tif

Gene tree obtained using the Odh nucleotide sequences from Barcelona. Only bootstrap values over 70 are presented. Abbreviations are as follows: BC and FBC stand for chromosomal lines obtained from a wild male and from an individual son of a wild female offspring from Barcelona, respectively. The arrangement of each chromosomal line sequenced is also presented after its abbreviation (TIFF 2309 kb)

10709_2012_9647_MOESM2_ESM.tif

Gene tree obtained using the Odh nucleotide sequences from Mt. Parnes. Only bootstrap values over 70 are presented. Abbreviations are as follows: MP stands for chromosomal lines obtained from a wild male from Mt. Parnes. The arrangement of each chromosomal line sequenced is also presented after its abbreviation (TIFF 2308 kb)

Supplementary material 3 (DOC 190 kb)

Supplementary material 4 (DOC 56 kb)

Supplementary material 5 (DOC 38 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Araúz, P.A., Peris-Bondia, F., Latorre, A. et al. Molecular evidence to suggest the origin of a colonization: Drosophila subobscura in America. Genetica 139, 1477–1486 (2011). https://doi.org/10.1007/s10709-012-9647-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-012-9647-8

Keywords

Navigation