Skip to main content

Advertisement

Log in

Drosophila as models to understand the adaptive process during invasion

Biological Invasions Aims and scope Submit manuscript

Abstract

The last few decades have seen a growing number of species invasions globally, including many insect species. In drosophilids, there are several examples of successful invasions, i.e. Zaprionus indianus and Drosophila subobscura some decades ago, but the most recent and prominent example is the invasion of Europe and North America by the pest species, Drosophila suzukii. During the invasive process, species often encounter diverse environmental conditions that they must respond to, either through rapid genetic adaptive shifts or phenotypic plasticity, or by some combination of both. Consequently, invasive species constitute powerful models for investigating various questions related to the adaptive processes that underpin successful invasions. In this paper, we highlight how Drosophila have been and remain a valuable model group for understanding these underlying adaptive processes, and how they enable insight into key questions in invasion biology, including how quickly adaptive responses can occur when species are faced with new environmental conditions.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adrion JR, Kousathanas A, Pascual M, Burrack HJ, Haddad NM, Bergland AO, Machado H, Sackton TB, Schlenke TA, Watada M, Wegmann D, Singh ND (2014) Drosophila suzukii: the genetic footprint of a recent, world-wide invasion. Mol Biol Evol 31:3148–3163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ananina G, Rohde C, David JR, Valente VL, Klaczko LB (2007) Inversion polymorphism and a new polytene chromosome map of Zaprionus indianus Gupta (1970) (Diptera, Drosophilidae). Genetica 131:117–125

    Article  PubMed  Google Scholar 

  • Arthur AL, Weeks AR, Sgrò CM (2008) Investigating latitudinal clines for life history and stress resistance traits in Drosophila simulans from eastern Australia. J Evol Biol 21:1470–1479

    Article  CAS  PubMed  Google Scholar 

  • Asplen MK, Anfora G, Biondi A, Choi D-S, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchnison WD, Isaacs R, Jiang Z-L, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton VM, Yu Y, Zappalà L, Desneux N (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

    Article  Google Scholar 

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

    Article  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 Drosophila subobscura: an evolutionary time series. Evolution 57:1837–1845

    Article  PubMed  Google Scholar 

  • Balanyà J, Oller JM, Huey RB, Gilchrist GW, Serra L (2006) Global genetic change tracks global climate warming in Drosophila subobscura. Science 313:1773–1775

    Article  PubMed  CAS  Google Scholar 

  • Balanyà J, Huey RB, Gilchrist GW, Serra L (2009) The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change. Heredity 103:364–367

    Article  PubMed  Google Scholar 

  • Bastide H, Yassin A, Johanning EJ, Pool JE (2014) Pigmentation in Drosophila melanogaster reaches its maximum in Ethiopia and correlates most strongly with ultra-violet radiation in sub-Saharan Africa. BMC Evol Biol 14:179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bauerfeind SS, Kellermann V, Moghadam NN, Loeshcke V, Fischer K (2014) Temperature and photoperiod affect stress resistance traits in Drosophila melanogaster. Physiol Entomol 39:237–246

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Blackburn S, van Heerwaarden B, Kellermann V, Sgrò CM (2014) Evolutionary capacity of upper thermal limits: beyond single trait assessments. J Exp Biol 217:1918–1924

    Article  PubMed  Google Scholar 

  • Bouiges A, Yassin A, Ikogou M, Lelarge C, Sikoa A-R, Mona S, Veuille M (2013) Detecting recent changes in the demographic parameters of drosophilid populations from Western and Central Africa. Comptes Rendus Geosci 345:297–305

    Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Article  Google Scholar 

  • Brncic D, Budnik M (1980) Colonization of Drosophila subobscura Collin in Chile. Drosoph Inf Serv 55:20

    Google Scholar 

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

    Article  Google Scholar 

  • Calabria G, Máca J, Bächli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Capy P, Pla E, David JR (1993) Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D. simulans. I. Geographic variations. Genet Sel Evol 25:517–536

    Article  PubMed Central  Google Scholar 

  • Carles-Tolrá M (2009) Zaprionus indianus Gupta: new genus and species for the Iberian Peninsula (Diptera: Drosophilidae). Bol SEA 45:316

    Google Scholar 

  • Castañeda LE, Balanya J, Rezende EL, Santos M (2013) Vanishing chromosomal inversion clines in Drosophila subobscura from Chile: is behavioral thermoregulation to blame? Am Nat 182:249–259

    Article  PubMed  Google Scholar 

  • Castrezena S (2007) New records of Zaprionus indianus Gupta, 1970 (Diptera, Drosophilidae) in North America and a key to identify some Zaprionus species deposited in the Drosophila Tucson Stock Center. Drosoph Inf Serv 90:34–36

    Google Scholar 

  • Chassagnard MT, Kraaijeveld AR (1991) The occurrence of Zaprionus sensu stricto in the Palearctic region (Diptera: Drosophilidae). Ann Soc Entomol Fr 27:495–496

    Google Scholar 

  • Chippindale AK, Leroi AM, Kim SB, Rose MR (1993) Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction. J Evol Biol 6:171–193

    Article  Google Scholar 

  • Chown SL, Slabber S, McGeoch M, Janion C, Leinaas HP (2007) Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc R Soc B: Biol Sci 274:2531–2537

    Article  Google Scholar 

  • Chown SL, Hodgins KA, Griffin PC, Oakeshott JG, Byrne M, Hoffmann AA (2015) Biological invasions, climate change and genomics. Evol Appl 8:23–46

    Article  PubMed  PubMed Central  Google Scholar 

  • Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insect 65:149–160

    Google Scholar 

  • Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627

    Article  CAS  PubMed  Google Scholar 

  • Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN et al (2007) Drosophila 12 Genomes Consortium. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218

    Article  PubMed  CAS  Google Scholar 

  • Commar LS, Galego LGC, Ceron CR, Carareto CMA (2012) Taxonomic and evolutionary analysis of Zaprionus indianus and its colonization of Palearctic and Neotropical regions. Genet Mol Biol 35:395–406

    Article  PubMed  PubMed Central  Google Scholar 

  • Coyne JA, Beecham E (1987) Heritability of two morpho- logical characters within and among natural populations of Drosophila melanogaster. Genetics 117:727–737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Da Mata RA, Tidon R, Côrtes LG, De Marco P, Diniz-Filho JAF (2010) Invasive and flexible: niche shift in the Drosophilid Zaprionus Indianus (Insecta, Diptera). Biol Invasions 12:1231–1241

    Article  Google Scholar 

  • Daehler CC (2003) Performance comparisons of co-occurring native and alien invsive plantes: Implications for Conservation and Restoration. Ann Rev Ecol Evol Syst 34:183–211

    Article  Google Scholar 

  • David JR, Bocquet C (1975) Similarities and differences in the latitudinal adaptation of two Drosophila sibling species. Nature 257:588–590

    Article  CAS  PubMed  Google Scholar 

  • David JR, Capy P (1988) Genetic variation of Drosophila melanogaster natural populations. Trends Genet 4:106–111

    Article  CAS  PubMed  Google Scholar 

  • David JR, Tsacas L (1981) Cosmopolitan, subcosmopolitan and widespread species: different strategies within the drosophilid family. CR Soc Biogeogr 57:11–26

    Google Scholar 

  • David JR, Capy P, Payant V, Tsakas S (1985) Thoracic trident pigmentation in Drosophila melanogaster: differentiation of geographical populations. Genet Sel Evol 17:211–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David J, Gibert P, Gravot E, Pétavy G, Morin J, Karan D, Moreteau B (1997) Phenotypic plasticity and developmental temperature in Drosophila: analysis and significance of reaction norms of morphometrical traits. J Therm Biol 22:441–451

    Article  Google Scholar 

  • David JR, Gibert P, Moreteau B (2004) Evolution of reaction norms. In: De Witt JJ, Scheiner SM (eds) Phenotypic plasticity. Functional and conceptual approaches. Oxford University Press, New York, pp 50–63

    Google Scholar 

  • David JR, Gibert P, Legout H, Pétavy G, Capy P, Moreteau B (2005) Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 94:3–12

    Article  CAS  PubMed  Google Scholar 

  • David JR, Araripe LO, Bitner-Mathé BC, Capy P, Goñi B, Klacz-ko LB, Legout H, Martins MB, Vouidibio J, Yassin A, Moreteau B (2006) Quantitative trait analyses and geographic variability of natural populations of Zaprionus indianus, a recent invader in Brazil. Heredity 96:53–62

    CAS  PubMed  Google Scholar 

  • Delpuech JM, Moreteau B, Chiche J, Pla E, Vouidibio J, David JR (1995) Phenotypic plasticity and reaction norms in temperate and tropical populations of Drosophila melanogaster: ovarian size and developmental temperature. Evolution 49:670–675

    Article  Google Scholar 

  • DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity. Functional and conceptual approaches. Oxford University Press, New York

    Google Scholar 

  • Facon B, Hufbauer RA, Tayeh A, Loiseau A, Lombaert E, Vitalis R, Guillemaud T, Lundgren JG, Estoup A (2011) Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr Biol 21:424–427

    Article  CAS  PubMed  Google Scholar 

  • Falconer DS (1989) Introduction to quantitative genetics. Longman, New York

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Fragata I, BalanyÀ J, Rego C, Matos M, Rezende EL, Santos M (2010) Contrasting patterns of phenotypic variation linked to chromosomal inversions in native and colonizing populations of Drosophila subobscura. J Evol Biol 23:112–123

    Article  CAS  PubMed  Google Scholar 

  • Gibert P, Moreteau B, David JR (2000) Developmental constraints on adaptive plasticity: reaction norms of pigmentation in adult segments of Drosophila melanogaster. Evol Dev 2:249–260

    Article  CAS  PubMed  Google Scholar 

  • Gibert P, Moreteau B, Pétavy G, Karan D, David JR (2001) Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution 55:1063–1068

    Article  CAS  PubMed  Google Scholar 

  • Gibert P, Moreteau B, David JR (2004) Phenotypic plasticity of body pigmentation in Drosophila melanogaster: genetic repeatability of quantitative parameters in two successive generations. Heredity 92:499–507

    Article  CAS  PubMed  Google Scholar 

  • Gibert P, Allemand R, Henri H, Huey RB (2010) Local adaptation and evolution of parasitoid interactions in an invasive species, Drosophila subobscura. Evol Ecol Res 12:873–883

    Google Scholar 

  • Gilchrist GW, Huey RB, Balanyà J, Pascual M, Serra L (2004) A time series of evolution in action: a latitudinal cline in wing size in South American Drosophila subobscura. Evolution 58:768–780

    Article  PubMed  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 

  • Gordon (1936) The frequency of heterozygosis in free-living populations of Drosophila melanogaster and Drosophila subobscura. J Genet 33:25–60

    Article  Google Scholar 

  • Gupta JP (1970) Description of a new species of Phorticella zaprionus (Drosophilidae) from India. Proc Ind Natl Sci Acad 36:62

    Google Scholar 

  • Haerty W, Gibert P, Capy P, Moreteau B, David JR (2003) Microspatial structure of Drosophila melanogaster populations in Brazzaville: evidence of natural selection acting on morphometrical traits. Heredity 91:440–447

    Article  CAS  PubMed  Google Scholar 

  • Harry M, Rashkovetsky E, Pavlicek T, Baker S, Derzhavets EM, Capy T, Cariou M-L, Lachaise D, Asada N, Nevo E (1999) Fine-scale biodiversity of Drosophilidae in “Evolution Canyon” at the Lower Nahal Oren microsite, Israel. Biologia 54:685–705

    Google Scholar 

  • Hendry AP, Kinnison MT (1999) The pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637–1653

    Article  Google Scholar 

  • Hill MP, Chown SL, Hoffmann AA (2013) A predicted niche shift corresponds with increased thermal resistance in an invasive mite, Halotydeus destructor. Global Ecol Biogeogr 22:942–951

    Article  Google Scholar 

  • Hoffmann AA, Parsons PA (1988) The analysis of quantitative variation in natural populations with isofemale strains. Genet Sel Evol 20:87–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann AA, Weeks AR (2007) Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129:133–147

    Article  PubMed  Google Scholar 

  • Hoffmann AA, Hallas R, Sinclair B, Mitrovski P (2001) Levels of variation in stress resistance in Drosophila among strains, local populations, and geographic region: patterns for desiccation, starvation, cold resistance and associated traits. Evolution 55:1621–1630

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann AA, Hallas RJ, Dean JA, Schiffer M (2003) Low potential for climatic stress adaptation in a rainforest Drosophila species. Science 301:100–102

    Article  CAS  PubMed  Google Scholar 

  • Huey RB, Pascual M (2009) Partial thermoregulatory compensation by a rapidly evolving invasive species along a latitudinal cline. Ecology 90:1715–1720

    Article  PubMed  Google Scholar 

  • Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309

    Article  CAS  PubMed  Google Scholar 

  • Imasheva AG, Bubli OA, Lazebny OE (1994) Variation in wing length in Eurasian populations of Drosophila melanogaster. Heredity 72:508–514

    Article  PubMed  Google Scholar 

  • James AC, Azevedo RBR, Partridge L (1995) Cellular basis and developmental time in a size cline of Drosophila melanogaster. Genetics 140:659–666

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi NK, Biddinger DJ, Demchak K, Deppen A (2014) First report of Zaprionus indianus (Diptera: Drosophilidae) in commercial fruits and vegetables in Pennsylvania. J Insect Sci 14:259

    Article  PubMed  Google Scholar 

  • Karan D, Dahiya N, Munjal AK, Gibert P, Moreteau B, Parkash R, David JR (1998) Desiccation and starvation tolerance of adult Drosophila: opposite latitudinal clines in natural populations of three different species. Evolution 52:825–831

    Article  Google Scholar 

  • Karan D, Dubey S, Moreteau B, Parkash R, David JR (2000) Geographical clines for quantitative traits in natural populations of a tropical drosophilid: Zaprionus indianus. Genetica 108:91–100

    Article  CAS  PubMed  Google Scholar 

  • Karsten M, Jansen van Vuuren B, Addison P, Terblanche JS (2015) Deconstructing intercontinental invasion pathway hypotheses of the Mediterranean fruit fly (Ceratitis capitata) using a Bayesian inference approach: are port interceptions and quarantine protocols successfully preventing new invasions? Div Dist 21:813–825

    Article  Google Scholar 

  • Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112–113:145–164

    Article  PubMed  Google Scholar 

  • Klepsatel P, Gáliková M, De Maio N, Huber CD, Schlötterer C, Flatt T (2013) Variation in thermal performance and reaction norms among populations of Drosophila melanogaster. Evolution 67:3573–3587

    Article  PubMed  Google Scholar 

  • Kristensen TN, Overgaard J, Lassen J, Hoffmann AA, Sgrò C (2015) Low evolutionary potential for egg-to-adult viability in Drosophila melanogaster at high temperatures. Evolution 69:803–814

    Article  PubMed  Google Scholar 

  • Kyriacou CP, Peixoto AA, Sandrelli F, Costa R, Tauber E (2008) Clines in clock genes: fine-tuning circadian rhythms to the environment. Trends Genet 24:24–132

    Article  CAS  Google Scholar 

  • Lachaise D, Silvain JF (2004) How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120:17–39

    Article  PubMed  Google Scholar 

  • Lande R (2015) Evolution of phenotypic plasticity in colonizing species. Mol Ecol 24:2038–2045

    Article  PubMed  Google Scholar 

  • Laurent SJ, Werzner A, Excoffier L, Stephan W (2011) Approximate Bayesian analysis of Drosophila melanogaster polymorphism data reveals a recent colonization of Southeast Asia. Mol Biol Evol 28:2041–2051

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Li H, Stephan W (2006) Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet 2:e166

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Loh R, Bitner-Mathé BC (2005) Variability of wing size and shape in three populations of a recent Brazilian invader, Zaprionus indianus (Diptera: Drosophilidae), from different habitats. Genetica 125:271–281

    Article  PubMed  Google Scholar 

  • Loh R, David JR, Debat V, Bitner-Mathá BC (2008) Adaptation to different climates results in divergent phenotypic plasticity of wing size and shape in an invasive drosophilid. J Genet 87:209–217

    Article  PubMed  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet JM, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5:e9743

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • López MM (1985) Drosophila subobscura has been found in the Atlantic Coast of Argentina. Drosoph Inf Serv 61:113

    Google Scholar 

  • Markow TA, Hanna G, Riesgo-Escovar JR, Tellez-Garcia AA, Richmond MP, Nazario-Yepiz NO, Laclette MRL, Carpinteyro-Ponce J, Pfeiler E (2014) Population genetics and recent colonization history of the invasive drosophilid Zaprionus indianus in Mexico and Central America. Biol Inv 16:2427–2434

    Article  Google Scholar 

  • Mattos Machado T, Solé-Cava A, David JR, Bitner-Mathé BC (2005) Allozyme variability in an invasive drosophilid, Zaprionus indianus (Diptera: Drosophilidae): comparison of a recently introduced Brazilian population with Old World populations. Ann Soc Entomol Fr 41:7–13

    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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morin JP, Moreteau B, Pétavy G, David JR (1999) Divergence of reaction norms of size characters between tropical and temperate populations of Drosophila melanogaster and D. simulans. J Evol Biol 12:329–339

    Article  Google Scholar 

  • Munjal AK, Karan D, Gibert P, Moreteau B, Parkash R, David JR (1997) Thoracic trident pigmentation in Drosophila melanogaster: latitudinal and altitudinal clines in Indian populations. Genet Sel Evol 29:601–610

    Article  PubMed Central  Google Scholar 

  • Murren CJ, Maclean HJ, Diamond SE, Steiner UK, Heskel MA, Handelsman CA, Ghalambor CK, Auld JR, Callahan HS, Pfennig DW, Relyea RA, Schlichting CD, Kingsolver J (2014) Evolutionary change in continuous reaction norms. Am Nat 183:453–467

    Article  PubMed  Google Scholar 

  • Nardon C, Deceliere G, Lœvenbruck 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  CAS  PubMed  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Noor MAF (1998) Diurnal activity patterns of Drosophila subobscura and D. pseudoobscura in sympatric populations. Am Midl Nat 140:34–41

    Article  Google Scholar 

  • Noor MAF, Pascual M, Smith KR (2000) Genetic variation in the spread of Drosophila subobscura from a nonequilibrium population. Evolution 54:696–703

    Article  CAS  PubMed  Google Scholar 

  • Nyamukondiwa C, Kleynhans E, Terblanche JS (2010) Phenotypic plasticity of thermal tolerance contributes to the invasion potential of Mediterranean fruit flies (Ceratitis capitata). Ecol Entomol 35:565–575

    Article  Google Scholar 

  • Okada T, Carson HL (1983) The genera Phorticella Duda and Zaprionus Coquillett (Diptera, Drosophilidae) of the Oriental region and New Guina. Kontyu 51:539–553

    Google Scholar 

  • Parsons PA (1983) The evolutionary biology of colonizing species. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Pascual M, Ayala FJ, Prevosti A, Serra L (1993) Colonization of North America by Drosophila subobscura: Ecological analysis of three communities of drosophilids in California. J Zool Syst Evol Res 31:216–226

    Article  Google Scholar 

  • Pascual M, Chapuis MP, Mestres F, Balanyà J, Huey RB, Gilchrist GW, Serra L, Estoup A (2007) Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods. Mol Ecol 15:3069–3083

    Article  CAS  Google Scholar 

  • Pegueroles G, Papaceit M, Quintana A, Guillén A, Prevosti A, Serra L (1995) An experimental study of evolution in progress: clines for quantitative traits in colonizing and Paleartic populations of Drosophila. Evol Ecol 9:453–465

    Article  Google Scholar 

  • Pegueroles C, Ordonez V, Mestres F, Pascual M (2010) Recombination and selection in the maintenance of the adaptive value of inversions. J Evol Biol 23:2709–2717

    Article  CAS  PubMed  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. John Hopkins University Press, Baltimore

    Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486

    Article  PubMed  Google Scholar 

  • Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367

    Article  PubMed  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Rego C, Blanya J, Fragata I, Matos M, Rezende EL, Santos M (2010) Clinal pattern of chromosomal inversion polymorphisms in Drosophila subobscura are partly associated with thermal preferences and heat stress resistance. Evolution 64:385–397

    Article  PubMed  Google Scholar 

  • Renkema JM, Miller M, Fraser H, Legare JP, Hallett RH (2013) First records of Zaprionus indianus Gupta (Diptera: Drosophilidae) from commercial fruit fields in Ontario and Quebec, Canada. J Entomol Soc Ont 144:125–130

    Google Scholar 

  • Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993

    Article  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, Mccauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Santos J, Pascual M, Simões P, Fragata I, Lima M, Kellen B, Santos M, Marques A, Rose MR, Matos M (2012) From nature to the laboratory: the impact of founder effects on adaptation. J Evol Biol 25:2607–2622

    Article  CAS  PubMed  Google Scholar 

  • Sawyer LA (1997) Natural variation in a Drosophila clock gene and temperature compensation. Science 278:2117–2120

    Article  CAS  PubMed  Google Scholar 

  • Sexton JP, McKay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climates in North America. Ecol Appl 12:1652–1660

    Article  Google Scholar 

  • Sgrò CM, Overgaard J, Kristensen TN, Mitchell KA, Cockerell FE, Hoffmann AA (2010) A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from eastern Australia. J Evol Biol 23:2484–2493

    Article  PubMed  Google Scholar 

  • Simberloff D, Rejmánek M (2011) Encyclopedia of biological invasions. University of California Press, Berkeley and Los Angeles

    Google Scholar 

  • Simões P, Pascual M, Santos J, Rose MR, Matos M (2008) Evolutionary dynamics of molecular markers during local adaptation: a case study in Drosophila subobscura. BMC Evol Biol 8:66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simões P, Calabria G, Picão-Osório J, Balanyà J, Pascual M (2012) The Genetic content of chromosomal inversions across a wide latitudinal gradient. PLoS ONE 7:e51625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swindell WR, Bouzat JL (2006) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: Evidence for purging. J Evol Biol 19:1257–1264

    Article  CAS  PubMed  Google Scholar 

  • Telonis-Scott M, Hoffmann AA, Sgrò CM (2011) The molecular genetics of clinal variation: A case study of ebony and thoracic trident pigmentation in Drosophila melanogaster from eastern Australia. Mol Ecol 20:2100–2110

    Article  PubMed  Google Scholar 

  • Terblanche JS, Hoffmann AA, Mitchell KA, Rako L, le Roux PC, Chown SL (2011) Ecologically relevant measures of tolerance to potentially lethal temperatures. J Exp Biol 214:3713–3725

    Article  PubMed  Google Scholar 

  • Trussell GC, Smith LD (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Natl Acad Sci USA 97:2123–2127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsacas L (1985) Zaprionus indianus Gupta, 1970, nouveau nom pour le plus commun des Zaprionus africains (Diptera, Drosophilidae). Ann Soc Ent Fr (NS) 21:343–344

    Google Scholar 

  • Urbanski J, Mogi M, O’Donnell D, DeCotiis M, Toma T, Armbruster P (2012) Rapid Adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am Nat 179:490–500

    Article  PubMed  Google Scholar 

  • Van der Linde K, Steck GJ, Hibbard K, Birdsley JS, Alonso LM, Houle D (2006) First records of Zaprionus indianus (Diptera: Drosophilidae), a pest species on commercial fruits from Panama and the United States of America. Fla Entomol 89:402–404

    Article  Google Scholar 

  • Van Heerwaarden B, Sgrò CM (2013) Multivariate analysis of adaptive capacity for upper thermal limits in Drosophila simulans. J Evol Biol 26:800–809

    Article  PubMed  Google Scholar 

  • Van Timmeren S, Isaacs R (2014) Drosophila suzukii in Michigan vineyards, and the first report of Zaprionus indianus from this region. J Appl Entomol 138:519–527

    Article  Google Scholar 

  • Van’t Land J, van Putten P, Villarroel H, Kamping A, van Delden W (1995) Latitudinal variation in wing length and allele frequencies for Adh and alpha-Gpdh in populations of Drosophila melanogaster from Ecuador and Chile. Drosoph Inf Serv 76:156

    Google Scholar 

  • Vilela CR (1999) Is Zaprionus indianus Gupta, 1970 (Diptera, Drosophilidae) currently colonizing the Neotropical region? Drosoph Inf Serv 82:37–39

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Yassin A (2013) Phylogenetic classification of the family Drosophilidae Rondani (Diptera): the role of morphology in the post-genomic era. Syst Entomol 38:349–364

    Article  Google Scholar 

  • Yassin AE, Abou-Youssef A (2004) A new front for a global invasive drosophilid: the colonization of the Northern-Western desert of Egypt by Zaprionus indianus Gupta, 1970. Drosoph Inf Serv 87:67–68

    Google Scholar 

  • Yassin A, Capy P, Madi-Ravazzi L, Ogereau D, David JR (2008) DNAbarcode discovers two cryptic species and two geographical radiations in the invasive drosophilid Zaprionus indianus. Mol Ecol Resour 8:491–501

    Article  CAS  PubMed  Google Scholar 

  • Yassin A, Borai F, Capy P, David JR, Elias E, Riad SA, Shalaby HG, Serour S, Abou-Youssef A (2009a) Mitochondrial DNA and chromosomal variation of the invasive drosophilid Zaprionus indianus in Egypt. Mitochondrial DNA 20:34–40

    Article  CAS  PubMed  Google Scholar 

  • Yassin A, David JR, Bitner-Mathé BC (2009b) Phenotypic variability of natural populations of an invasive drosophilid, Zaprionus indianus, on different continents: Comparison of wild-living and laboratory-grown flies. Comptes Rendus Biol 332:898–908

    Article  Google Scholar 

  • Yassin A, Da Lage JL, David JR, Kondo M, Madi-Ravazzi L, Prigent S, Toda MJ (2010) Polyphyly of the Zaprionus genus group (Diptera: Drosophilidae). Mol Phylogenet Evol 55:335–339

    Article  PubMed  Google Scholar 

  • Ziska LH, Blumenthal DM, Runion GB, Hunt ER, Diaz-Soltero H (2010) Invasive species and climate change: an agronomic perspective. Clim Change 105:13–42

    Article  Google Scholar 

Download references

Acknowledgments

This paper had its origin at a workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” hosted by the DST-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, in November 2014. We thank Jean David for collecting and providing us with D. suzukii isofemale lines from Paris. CMS was supported by funding from the Science and Industry Endowment Fund and the Australian Research Council. MP is a member of the research group 2014SGR-336 of the Generalitat de Catalunya and supported by project CTM2013-48163. CP was funded by Bayer CropScience France. Additional financial support was provided by HortGro, the National Research Foundation of South Africa, Stellenbosch University, and SubTrop. The November 2014 workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” was hosted and co-funded by the DST-NRF Centre of Excellence for Invasion Biology at Stellenbosch University, South Africa.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia Gibert.

Additional information

Guest editors: Matthew P. Hill, Susana Clusella-Trullas, John S. Terblanche & David M. Richardson / Insect Invasions

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gibert, P., Hill, M., Pascual, M. et al. Drosophila as models to understand the adaptive process during invasion. Biol Invasions 18, 1089–1103 (2016). https://doi.org/10.1007/s10530-016-1087-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1087-4

Keywords

Navigation