Biological Invasions

, Volume 18, Issue 4, pp 1089–1103 | Cite as

Drosophila as models to understand the adaptive process during invasion

  • Patricia Gibert
  • Matthew Hill
  • Marta Pascual
  • Christophe Plantamp
  • John S. Terblanche
  • Amir Yassin
  • Carla M. Sgrò
Insect Invasions

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.

Keywords

Local adaptation Phenotypic plasticity Drosophila subobscura Drosophila suzukii Zaprionus indianus 

References

  1. 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 31:3148–3163PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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 131:117–125PubMedCrossRefGoogle Scholar
  3. 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 21:1470–1479PubMedCrossRefGoogle Scholar
  4. 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 88:469–494CrossRefGoogle Scholar
  5. Ayala FJ, Serra L, Prevosti A (1989) A grand experiment in evolution: Drosophila subobscura colonization of the Americas. Genome 31:246–255CrossRefGoogle Scholar
  6. 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 57:1837–1845PubMedCrossRefGoogle Scholar
  7. Balanyà J, Oller JM, Huey RB, Gilchrist GW, Serra L (2006) Global genetic change tracks global climate warming in Drosophila subobscura. Science 313:1773–1775PubMedCrossRefGoogle Scholar
  8. Balanyà J, Huey RB, Gilchrist GW, Serra L (2009) The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change. Heredity 103:364–367PubMedCrossRefGoogle Scholar
  9. 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 14:179PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bauerfeind SS, Kellermann V, Moghadam NN, Loeshcke V, Fischer K (2014) Temperature and photoperiod affect stress resistance traits in Drosophila melanogaster. Physiol Entomol 39:237–246CrossRefGoogle Scholar
  11. Beckenbach AT, Prevosti A (1986) Colonization of North America by the European species, Drosophila subobscura and D. ambigua. Am Midl Nat 115:10CrossRefGoogle Scholar
  12. Blackburn S, van Heerwaarden B, Kellermann V, Sgrò CM (2014) Evolutionary capacity of upper thermal limits: beyond single trait assessments. J Exp Biol 217:1918–1924PubMedCrossRefGoogle Scholar
  13. 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 345:297–305CrossRefGoogle Scholar
  14. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155CrossRefGoogle Scholar
  15. Brncic D, Budnik M (1980) Colonization of Drosophila subobscura Collin in Chile. Drosoph Inf Serv 55:20Google Scholar
  16. Brncic D, Prevosti A, Budnik M, Monclus M, Ocana J (1981) Colonization of Drosophila subobscura in Chile. I. First population and cytogenetics studies. Genetica 56:3–9CrossRefGoogle Scholar
  17. 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 136:139–147CrossRefGoogle Scholar
  18. Capy P, Gibert P (2004) Drosophila melanogaster, Drosophila simulans: so similar yet so different. Genetica 120:5–16PubMedCrossRefGoogle Scholar
  19. 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 25:517–536PubMedCentralCrossRefGoogle Scholar
  20. Carles-Tolrá M (2009) Zaprionus indianus Gupta: new genus and species for the Iberian Peninsula (Diptera: Drosophilidae). Bol SEA 45:316Google Scholar
  21. 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 182:249–259PubMedCrossRefGoogle Scholar
  22. 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 90:34–36Google Scholar
  23. Chassagnard MT, Kraaijeveld AR (1991) The occurrence of Zaprionus sensu stricto in the Palearctic region (Diptera: Drosophilidae). Ann Soc Entomol Fr 27:495–496Google Scholar
  24. 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 6:171–193CrossRefGoogle Scholar
  25. 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 274:2531–2537CrossRefGoogle Scholar
  26. Chown SL, Hodgins KA, Griffin PC, Oakeshott JG, Byrne M, Hoffmann AA (2015) Biological invasions, climate change and genomics. Evol Appl 8:23–46PubMedPubMedCentralCrossRefGoogle Scholar
  27. 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 65:149–160Google Scholar
  28. 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 17:3614–3627PubMedCrossRefGoogle Scholar
  29. 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 450:203–218PubMedCrossRefGoogle Scholar
  30. 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 35:395–406PubMedPubMedCentralCrossRefGoogle Scholar
  31. Coyne JA, Beecham E (1987) Heritability of two morpho- logical characters within and among natural populations of Drosophila melanogaster. Genetics 117:727–737PubMedPubMedCentralGoogle Scholar
  32. 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 12:1231–1241CrossRefGoogle Scholar
  33. Daehler CC (2003) Performance comparisons of co-occurring native and alien invsive plantes: Implications for Conservation and Restoration. Ann Rev Ecol Evol Syst 34:183–211CrossRefGoogle Scholar
  34. David JR, Bocquet C (1975) Similarities and differences in the latitudinal adaptation of two Drosophila sibling species. Nature 257:588–590PubMedCrossRefGoogle Scholar
  35. David JR, Capy P (1988) Genetic variation of Drosophila melanogaster natural populations. Trends Genet 4:106–111PubMedCrossRefGoogle Scholar
  36. David JR, Tsacas L (1981) Cosmopolitan, subcosmopolitan and widespread species: different strategies within the drosophilid family. CR Soc Biogeogr 57:11–26Google Scholar
  37. David JR, Capy P, Payant V, Tsakas S (1985) Thoracic trident pigmentation in Drosophila melanogaster: differentiation of geographical populations. Genet Sel Evol 17:211–224PubMedPubMedCentralCrossRefGoogle Scholar
  38. 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 22:441–451CrossRefGoogle Scholar
  39. 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 50–63Google Scholar
  40. 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 94:3–12PubMedCrossRefGoogle Scholar
  41. 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 96:53–62PubMedGoogle Scholar
  42. 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 49:670–675CrossRefGoogle Scholar
  43. DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity. Functional and conceptual approaches. Oxford University Press, New YorkGoogle Scholar
  44. 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 21:424–427PubMedCrossRefGoogle Scholar
  45. Falconer DS (1989) Introduction to quantitative genetics. Longman, New YorkGoogle Scholar
  46. 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 22:650–658PubMedCrossRefGoogle Scholar
  47. 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 23:112–123PubMedCrossRefGoogle Scholar
  48. Gibert P, Moreteau B, David JR (2000) Developmental constraints on adaptive plasticity: reaction norms of pigmentation in adult segments of Drosophila melanogaster. Evol Dev 2:249–260PubMedCrossRefGoogle Scholar
  49. Gibert P, Moreteau B, Pétavy G, Karan D, David JR (2001) Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution 55:1063–1068PubMedCrossRefGoogle Scholar
  50. 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 92:499–507PubMedCrossRefGoogle Scholar
  51. 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 12:873–883Google Scholar
  52. 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 58:768–780PubMedCrossRefGoogle Scholar
  53. Gómez-Baldó L, Latorre A, Serra L, Mestres F (2008) Molecular variation in the Odh gene in Chilean natural populations of D. subobscura. Hereditas 145:154–162CrossRefGoogle Scholar
  54. Gordon (1936) The frequency of heterozygosis in free-living populations of Drosophila melanogaster and Drosophila subobscura. J Genet 33:25–60CrossRefGoogle Scholar
  55. Gupta JP (1970) Description of a new species of Phorticella zaprionus (Drosophilidae) from India. Proc Ind Natl Sci Acad 36:62Google Scholar
  56. 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 91:440–447PubMedCrossRefGoogle Scholar
  57. 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 54:685–705Google Scholar
  58. Hendry AP, Kinnison MT (1999) The pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637–1653CrossRefGoogle Scholar
  59. 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 22:942–951CrossRefGoogle Scholar
  60. Hoffmann AA, Parsons PA (1988) The analysis of quantitative variation in natural populations with isofemale strains. Genet Sel Evol 20:87–98PubMedPubMedCentralCrossRefGoogle Scholar
  61. 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 129:133–147PubMedCrossRefGoogle Scholar
  62. 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 55:1621–1630PubMedCrossRefGoogle Scholar
  63. Hoffmann AA, Hallas RJ, Dean JA, Schiffer M (2003) Low potential for climatic stress adaptation in a rainforest Drosophila species. Science 301:100–102PubMedCrossRefGoogle Scholar
  64. Huey RB, Pascual M (2009) Partial thermoregulatory compensation by a rapidly evolving invasive species along a latitudinal cline. Ecology 90:1715–1720PubMedCrossRefGoogle Scholar
  65. Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309PubMedCrossRefGoogle Scholar
  66. Imasheva AG, Bubli OA, Lazebny OE (1994) Variation in wing length in Eurasian populations of Drosophila melanogaster. Heredity 72:508–514PubMedCrossRefGoogle Scholar
  67. James AC, Azevedo RBR, Partridge L (1995) Cellular basis and developmental time in a size cline of Drosophila melanogaster. Genetics 140:659–666PubMedPubMedCentralGoogle Scholar
  68. 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 14:259PubMedCrossRefGoogle Scholar
  69. 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 52:825–831CrossRefGoogle Scholar
  70. 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 108:91–100PubMedCrossRefGoogle Scholar
  71. 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 21:813–825CrossRefGoogle Scholar
  72. Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112–113:145–164PubMedCrossRefGoogle Scholar
  73. 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 67:3573–3587PubMedCrossRefGoogle Scholar
  74. 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 69:803–814PubMedCrossRefGoogle Scholar
  75. Kyriacou CP, Peixoto AA, Sandrelli F, Costa R, Tauber E (2008) Clines in clock genes: fine-tuning circadian rhythms to the environment. Trends Genet 24:24–132CrossRefGoogle Scholar
  76. Lachaise D, Silvain JF (2004) How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120:17–39PubMedCrossRefGoogle Scholar
  77. Lande R (2015) Evolution of phenotypic plasticity in colonizing species. Mol Ecol 24:2038–2045PubMedCrossRefGoogle Scholar
  78. 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 28:2041–2051PubMedCrossRefGoogle Scholar
  79. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  80. Li H, Stephan W (2006) Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet 2:e166PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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 125:271–281PubMedCrossRefGoogle Scholar
  82. 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 87:209–217PubMedCrossRefGoogle Scholar
  83. 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:e9743PubMedPubMedCentralCrossRefGoogle Scholar
  84. López MM (1985) Drosophila subobscura has been found in the Atlantic Coast of Argentina. Drosoph Inf Serv 61:113Google Scholar
  85. 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 16:2427–2434CrossRefGoogle Scholar
  86. 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 41:7–13Google Scholar
  87. Mestres F, Serra L, Ayala FJ (1995) Colonization of the Americas by D. subobscura: lethal-gene allelism and association with chromosomal arrangements. Genetics 140:1297–1305PubMedPubMedCentralGoogle Scholar
  88. 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 98:9167–9170PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 12:329–339CrossRefGoogle Scholar
  90. 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 29:601–610PubMedCentralCrossRefGoogle Scholar
  91. 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 183:453–467PubMedCrossRefGoogle Scholar
  92. 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 14:869–878PubMedCrossRefGoogle Scholar
  93. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  94. Noor MAF (1998) Diurnal activity patterns of Drosophila subobscura and D. pseudoobscura in sympatric populations. Am Midl Nat 140:34–41CrossRefGoogle Scholar
  95. Noor MAF, Pascual M, Smith KR (2000) Genetic variation in the spread of Drosophila subobscura from a nonequilibrium population. Evolution 54:696–703PubMedCrossRefGoogle Scholar
  96. 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 35:565–575CrossRefGoogle Scholar
  97. Okada T, Carson HL (1983) The genera Phorticella Duda and Zaprionus Coquillett (Diptera, Drosophilidae) of the Oriental region and New Guina. Kontyu 51:539–553Google Scholar
  98. Parsons PA (1983) The evolutionary biology of colonizing species. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  99. 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 31:216–226CrossRefGoogle Scholar
  100. 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 15:3069–3083CrossRefGoogle Scholar
  101. 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 9:453–465CrossRefGoogle Scholar
  102. Pegueroles C, Ordonez V, Mestres F, Pascual M (2010) Recombination and selection in the maintenance of the adaptive value of inversions. J Evol Biol 23:2709–2717PubMedCrossRefGoogle Scholar
  103. Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. John Hopkins University Press, BaltimoreGoogle Scholar
  104. Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486PubMedCrossRefGoogle Scholar
  105. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367PubMedCrossRefGoogle Scholar
  106. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294PubMedCrossRefGoogle Scholar
  107. 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 85:5597–5600PubMedPubMedCentralCrossRefGoogle Scholar
  108. 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 44:218–221CrossRefGoogle Scholar
  109. 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 64:385–397PubMedCrossRefGoogle Scholar
  110. 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 144:125–130Google Scholar
  111. 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 9:981–993PubMedCrossRefGoogle Scholar
  112. 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 32:305–332CrossRefGoogle Scholar
  113. 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 25:2607–2622PubMedCrossRefGoogle Scholar
  114. Sawyer LA (1997) Natural variation in a Drosophila clock gene and temperature compensation. Science 278:2117–2120PubMedCrossRefGoogle Scholar
  115. Sexton JP, McKay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climates in North America. Ecol Appl 12:1652–1660CrossRefGoogle Scholar
  116. 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 23:2484–2493PubMedCrossRefGoogle Scholar
  117. Simberloff D, Rejmánek M (2011) Encyclopedia of biological invasions. University of California Press, Berkeley and Los AngelesGoogle Scholar
  118. 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 8:66PubMedPubMedCentralCrossRefGoogle Scholar
  119. 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:e51625PubMedPubMedCentralCrossRefGoogle Scholar
  120. Swindell WR, Bouzat JL (2006) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: Evidence for purging. J Evol Biol 19:1257–1264PubMedCrossRefGoogle Scholar
  121. 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 20:2100–2110PubMedCrossRefGoogle Scholar
  122. 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 214:3713–3725PubMedCrossRefGoogle Scholar
  123. 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 97:2123–2127PubMedPubMedCentralCrossRefGoogle Scholar
  124. Tsacas L (1985) Zaprionus indianus Gupta, 1970, nouveau nom pour le plus commun des Zaprionus africains (Diptera, Drosophilidae). Ann Soc Ent Fr (NS) 21:343–344Google Scholar
  125. 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 179:490–500PubMedCrossRefGoogle Scholar
  126. 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 89:402–404CrossRefGoogle Scholar
  127. Van Heerwaarden B, Sgrò CM (2013) Multivariate analysis of adaptive capacity for upper thermal limits in Drosophila simulans. J Evol Biol 26:800–809PubMedCrossRefGoogle Scholar
  128. Van Timmeren S, Isaacs R (2014) Drosophila suzukii in Michigan vineyards, and the first report of Zaprionus indianus from this region. J Appl Entomol 138:519–527CrossRefGoogle Scholar
  129. 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 76:156Google Scholar
  130. Vilela CR (1999) Is Zaprionus indianus Gupta, 1970 (Diptera, Drosophilidae) currently colonizing the Neotropical region? Drosoph Inf Serv 82:37–39Google Scholar
  131. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  132. Yassin A (2013) Phylogenetic classification of the family Drosophilidae Rondani (Diptera): the role of morphology in the post-genomic era. Syst Entomol 38:349–364CrossRefGoogle Scholar
  133. 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 87:67–68Google Scholar
  134. 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 8:491–501PubMedCrossRefGoogle Scholar
  135. 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 20:34–40PubMedCrossRefGoogle Scholar
  136. 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 332:898–908CrossRefGoogle Scholar
  137. 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 55:335–339PubMedCrossRefGoogle Scholar
  138. Ziska LH, Blumenthal DM, Runion GB, Hunt ER, Diaz-Soltero H (2010) Invasive species and climate change: an agronomic perspective. Clim Change 105:13–42CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Patricia Gibert
    • 1
  • Matthew Hill
    • 2
  • Marta Pascual
    • 3
  • Christophe Plantamp
    • 1
  • John S. Terblanche
    • 2
  • Amir Yassin
    • 4
  • Carla M. Sgrò
    • 5
  1. 1.CNRS, UMR 5558, Laboratoire de Biométrie et Biologie EvolutiveUniversité Lyon 1VilleurbanneFrance
  2. 2.Centre for Invasion Biology, Department of Conservation Ecology and Entomology, Faculty of AgriSciencesStellenbosch UniversityMatielandSouth Africa
  3. 3.Departament de Genètica – IRBio, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  4. 4.Laboratory of GeneticsUniversity of WisconsinMadisonUSA
  5. 5.School of Biological SciencesMonash UniversityMelbourneAustralia

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