Skip to main content
SpringerLink
Log in

Within- and among-population variation in oviposition preference for urea-supplemented food inDrosophila melanogaster

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Oviposition preference for ureasupplemented food was assayed by simultaneous choice trials on five pairs of closely related laboratory populations of Drosophila melanogaster.Each pair of populations had been derived from a separate ancestral population about 85 generations prior to this study. One population in each pair had been subjected to selection for larval tolerance to the toxic effects of urea; the other population served as a control. Considerable variation in oviposition preference was seen both within and among populations, with four of the ten populations showing a significant mean preference for ureasupplemented food. The degree of specificity shown by individual females was surprisingly high, leading to a bimodal distribution of oviposition preference in some populations. Overall, selection for larval tolerance to urea did not significantly affect oviposition preference. However, the data indicated that pairwise comparisons between randomly selected populations from the two larval selection regimes would lead to a range of possible outcomes, suggesting, in several cases, that selection for larval urea tolerance had led to significant differentiation of adult oviposition preference for urea in one or the other direction. The results, therefore, highlight the importance of population level replication and caution against the practice, common in ecological studies, of assaying oviposition preference in two populations that utilize different hosts in nature, and then drawing broad evolutionary inferences from the results.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barker J S F 1992 Genetic variation in cactophilicDrosophila for oviposition on natural yeast substrates;Evolution 46 1070–1083

    Article  CAS  Google Scholar 

  • Baur R, Feeny P and Stadler E1993 Oviposition stimulants for the black swallowtail butterfly: identification of electrophysiologically active compounds in carrot volatiles;J. Chem. Ecol. 19 919–937

    Article  CAS  Google Scholar 

  • Brodie E D III and Brodie E D Jr 1991 Evolutionary response of predators to dangerous prey: reduction of toxicity of newts and resistance of garter snakes in island populations;Evolution 45 221–224

    PubMed  Google Scholar 

  • Burdon J J and Thompson J N 1995 Changed patterns of resistance in a populationof Linum marginale attacked by the rust pathogenMelampsora link, J. Ecol 83 199–206

    Google Scholar 

  • Courtney S P 1981 Coevolution of Pierid butterflies and their cruciferous food plants;Oecologia 51 91–96

    Article  Google Scholar 

  • Courtney S P and Kibota T T 1990 Mother doesn’t know best: selection of hosts by ovipositing insects; inInsect-plant interactions (ed.) E A Bernays (Boca Raton: CRC Press) vol II, pp 161–188

    Google Scholar 

  • Craig T P, Itami J K, Abrahamson W G and Horner J D 1993 Behavioral evidence for host-race formation inEurosta solidaginis;Evolution 47 1696–1710

    Article  Google Scholar 

  • Feeny P 1991 Chemical constraints on the evolution of swallowtail butterflies; inPlant-animal interactions: evolutionary ecology in tropical and temperate regions (eds) P W Price, T M Lewinsohn, G W Fernandes and W W Benson (New York: Wiley) pp 315–340

    Google Scholar 

  • Fox G W 1993 A quantitative genetic analysis of oviposition preference and larval performance on two hosts in the Bruchid beetle,Callosobruchus maculatus;Evolution 47 166–175

    Article  Google Scholar 

  • Fox C/W, Waddell K J and Mousseau T A1994 Host-associated fitness variation in a seed beetle (Coleoptera: Bruchidae): evidence for local adaptation to a poor quality host;Oecologia 99 329–336

    Article  Google Scholar 

  • Fox L R and Eisenbach J 1992 Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivatedvs. wild crucifers;Oecologia 89 574–579

    Article  CAS  Google Scholar 

  • Freeman M F and Tukey J W 1950 Transformations related to the angular and the square root;Ann. Math. Stat. 21 607–611.

    Article  Google Scholar 

  • Futuyma D J and Peterson S C1985 Genetic variation in the use of resources by insects;Annu. Rev. Entomol. 30 217–238

    Article  Google Scholar 

  • Futuyma D J 1991 Evolution of host specificity in herbivorous insects; inPlant-animal interactions: evolutionary ecology in tropical and temperate regions (eds.) P W Price, T M Lewinsohn, G W Fernandes and W W Benson (New York: Wiley) pp 431–454

    Google Scholar 

  • Gould F 1988 Genetics of pairwise and multispecies plant-herbivore coevolution; inChemical mediation of coevolution (ed.) K C Spencer (San Diego: Academic Press) pp 13–55

    Chapter  Google Scholar 

  • Hamilton J G and Zalucki M P 1993 Interactions between a specialist herbivore,Crocidosema plebejana, and its host plantsMalva parviflora and cotton,Gossypium hirsutum: oviposition preference;Entomol Exp. Appl 66 207–212

    Article  Google Scholar 

  • Hanks L M, Paine T D and Millar J G 1993 Host species preference and larval performance in the wood-boring beetlePhoracantha semipunctata F;Oecologia 95 22–29

    Article  Google Scholar 

  • Higa I and Fuyama Y 1993 Genetics of food preference inDrosophila sechellia;Genetica 88 129–136

    Article  CAS  Google Scholar 

  • Honda. K 1986 Flavanone glycosides as oviposition stimulants in a papilionid butterfly,Papilio protenor;J. Chem. Ecol. 12 1999–2010

    Article  CAS  Google Scholar 

  • Huang X and Renwick J A A 1993 Differential selection of host plants by twoPieris species: the role of oviposition stimulants and deterrents;Entomol. Exp. Appl. 68 59–69

    Article  Google Scholar 

  • Jaenike J 1982 Environmental modification of oyiposition behaviour inDrosophila;Am. Nat. 119 784–802

    Article  Google Scholar 

  • Jaenike J 1987 Genetics of oviposition-site preference inDrosophila tripunctata;Heredity 59 363–369

    Article  Google Scholar 

  • Jaenike J 1989 Genetic population structureof Drosophila tripunctata: patterns of variation and covariation of traits affecting resource use;Evolution 43 1467–1482

    PubMed  Google Scholar 

  • Jaenike J 1990 Host specialization in phytophagous insects;Annu. Rev. Ecol. syst. 21 243–272

    Article  Google Scholar 

  • Janz N, Nylin S and Wedell N 1994 Host plant utilization in the comma butterfly: sources of variation and evolutionary implications;Oecologia 99 132–140

    Article  Google Scholar 

  • Jarosz A M and Burdon J J 1991 Host-pathogen interactions in natural populations ofLinum marginale andMelampsora lint II. Local and regional variation in patterns of resistance and racial structure;Evolution 45 1618–1627

    CAS  PubMed  Google Scholar 

  • Joshi A and Thompson J N 1995a Alternative routes to the evolution of competitive ability in two competing species ofDrosophila;Evolution 49 616–625

    Article  Google Scholar 

  • Joshi A and Thompson J N 1995b Trade-offs and the evolution of host specialization;Evol. Ecol. 9 82–92

    Article  Google Scholar 

  • Joshi A and Thompson J N 1996 Evolution of broad and specific competitive ability in novel versus familiar environments inDrosophila species,Evolution 50 188–194

    Article  Google Scholar 

  • Joshi A, Knight C D and Mueller L D 1996 Genetics of larval urea tolerance inDrosophila melanogaster;Heredity 77 33–39

    Article  Google Scholar 

  • Krebs R A, Barker J S F and Armstrong T P 1992 Coexistence of ecologically similar colonising species III.Drosophila aldrichi andD. buzzatii: larval performance on, and adult preference for, threeOpuntia cactus species;Oecologia 92 363–372

    Article  Google Scholar 

  • Leddy P M, Paine T D and Bellows T S Jr 1993 Oppositional preferences ofSiphoninus phillyreae and its fitness on seven host plant species;Entomol. Exp. Appl. 68 43–50

    Article  Google Scholar 

  • Lederhouse R C, Ayres M P, Nitao J K and Scriber J M 1992 Differential use of lauraceous hosts by swallowtail butterflies,Papilio troilus andP. palamedes (Papilionidae);Oikos 63 244–252

    Article  Google Scholar 

  • Lu W H and Logan P 1994 Genetic variation in oviposition between and within populations ofLeptinotarsa decemlineata (Coleoptera: Chrysomelidae);Ann. Entomol. Soc. Am. 87 634–640

    Article  Google Scholar 

  • McCauley DE 1991 The effect of host plant patch size variation on the population structure of a specialist herbivore insect,Tetraopes tetraopthalmus;Evolution 45 1675–1684

    Article  Google Scholar 

  • Moreteau B, R’Kha S and David J R 1994 Genetics of a nonoptimal behaviour: oviposition preference ofDrosophila mauritiana for a toxic resource;Behav. Genet. 24 433–441

    Article  CAS  Google Scholar 

  • Mueller L D 1995 Adaptation and density-dependent natural selection; inGenetics of natural populations: the continuing importance of Theodosius Dobzhansky (ed.) L Levine (New York: Columbia University Press) pp 101–124

    Google Scholar 

  • Ng D 1988 A novel level of interactions in plant insect systems;Nature (London) 334 611–612

    Article  Google Scholar 

  • Nishida R, Ohsugi T, Kokubo S and Fukami H 1987 Oviposition stimulants of a Citrus-feeding swallowtail butterfly,Papilio xuthus L;Experientia 43 342–344

    Article  CAS  Google Scholar 

  • Nylin S 1988 Host plant specialisation and seasonality in a polyphagous butterfly,Polygonia c-album (Nymphalidae);Oikos 53 381–386

    Article  Google Scholar 

  • Nylin S and Janz N 1993 Oviposition preference and larval performance inPolygonia c-album (Lepidoptera: Nymphalidae): the choice between bad and worse;Ecol. Entomol. 18 394–398

    Article  Google Scholar 

  • Penz C M and Araujo A M 1991 Interaction betweenPapilio hectorides (Papilionidae) and four host plants (Piperaceae, Rutaceae) in a southern Brazilian population;J. Res. Lepidoptera. 29 161–171

    Google Scholar 

  • Rank N E 1992 Host plant preference based on salicylate chemistry in a willow leaf beetle(Chrysomela aeneicollis);Oecologia 90 95–101

    Article  Google Scholar 

  • Renwick J A A and Chew F S 1994 Oviposition behaviour in Lepidoptera;Annu. Rev. Entomol 39 377–400

    Article  Google Scholar 

  • Roininen H and Tahvanainen J 1989 Host selection and larval performance of two willow-feeding sawflies;Ecology 70 129–136

    Article  Google Scholar 

  • Roininen H, Vuorinen J, Tahvanainen J and Julkunen-Tiitto R 1993 Host preference and allozyme differentiation in shoot galling sawfly,Euura atra;Evolution 47 300–308

    Article  Google Scholar 

  • Rose M R 1984 Laboratory evolution of postponed senescence inDrosophila melanogaster;Evolution 38 1004–1010

    Article  Google Scholar 

  • Rose M R and Service P M 1985 Evolution of aging;Rev. Biol. Res. Aging 2 85–98

    Google Scholar 

  • Singer M C 1982 Quantification of host specificity by manipulation of oviposition behaviour in the butterflyEuphydryas editha;Oecologia 52 224–229

    Article  Google Scholar 

  • Singer M C 1983 Determinants of multiple host use by a phytophagous insect population;Evolution 37 389–403

    Article  Google Scholar 

  • Singer M C 1986 The definition and measurement of oviposition preference; inPlant-insect interactions (eds) J Miller and T A Miller (New York: Springer Verlag) pp 65–94

    Chapter  Google Scholar 

  • Singer M C, Ng D and Thomas C D 1988 Heritability of oviposition preference and its relationship to offspring performance within a single insect population;Evolution 42 977–985

    Article  CAS  Google Scholar 

  • Singer M C, Thomas C D, Billington H L and Parmesan C 1989 Variation among conspecific insect populations in the mechanistic basis of diet breadth;Anim. Behav. 37 751–759

    Article  Google Scholar 

  • Singer M C, Ng D and Moore R A 1991 Genetic variation in oviposition preference between butterfly populations;J. Insect. Behav. 4 531–535

    Article  Google Scholar 

  • Singer M C, Ng D, Vasco D and Thomas C D 1992 Rapidly evolving associations among oviposition preferences fail to constrain evolution of insect diet;Am. Nat. 139 9–20

    Article  Google Scholar 

  • Sokal R R and Rohlf F J 1981Biometry 2nd edition (New York: Freeman)

    Google Scholar 

  • Szentesi A and Jermy T 1990 The role of experience in host plant choice by phytophagous insects; inInsect-plant interactions (ed.) E A Bernays (Boca Raton: CRC Press) vol II, pp 39–74

    Google Scholar 

  • Tabashnik B E 1983 Host range evolution: the shift from native legume hosts to alfalfa by the butterflyColias philodice eryphile;Evolution 37 150–162

    Article  Google Scholar 

  • Tabashnik B E, Wheelock H, Rainbolt J D and Watt W B 1981 Individual variation in oviposition preference in the butterfly,Colias eurytheme;Oecologia 50 225–230

    Article  Google Scholar 

  • Thomas C D, Ng D, Singer M C, Mallet J L B, Parmesan C and Billington H L 1987 Incorporation of a European weed into the diet of a North American herbivore;Evolution 41 892–901

    Article  CAS  Google Scholar 

  • Thompson J N 1988a Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects;Entomol. Exp. Appl. 47 3–14

    Article  Google Scholar 

  • Thompson J N 1988b Variation in preference and specificity in monophagous and oligophagous swallowtail butterflies;Evolution 42 118–128

    Article  Google Scholar 

  • Thompson J N 1988c Evolutionary genetics of oviposition preference in swallowtail butterflies;Evolution 42 1223–1234

    Article  Google Scholar 

  • Thompson J N 1990 Coevolution and the evolutionary genetics of interactions among plants and insects and pathogens; inPests, pathogens, and plant communities (eds) J J Burdon and S R Leather (Oxford: Blackwell Scientific) pp 249–271

    Google Scholar 

  • Thompson J N 1993 Preference hierarchies and the origin of geographic specialization in host use in swallowtail butterflies;Evolution 47 1585–1594

    Article  Google Scholar 

  • Thompson J N 1994a The geographic mosaic of evolving interactions; inIndividuals, populations and patterns in ecology (eds) S R Leather, A D Watt, N J Mills and K F A Walters (Andover: Intercept Press) pp 419–432

    Google Scholar 

  • Thompson J N 1994bThe revolutionary process (Chicago: The University of Chicago Press)

    Book  Google Scholar 

  • Thompson J N and Pellmyr O 1991 Evolution of oviposition behaviour and host preference in Lepidoptera;Annu, Rev. Entomol. 36 65–89

    Article  Google Scholar 

  • Thompson J N, Wehling W F and Podolsky R 1990 Evolutionary genetics of host use in swallowtail butterflies;Nature (London) 344 148–150

    Article  Google Scholar 

  • Travisano M, Mongold J A, Bennett A F and Lenski R E 1995 Experimental tests of the roles of adaptation, chance and history in evolution;Science 267 87–90

    Article  CAS  Google Scholar 

  • Valladares G and Lawton J H 1991 Host-plant selection in the holly leaf-miner: does mother know best?;J. Anim. Ecol. 60 227–240

    Article  Google Scholar 

  • Via S 1986 Genetic covariance between oviposition preference and larval performance in an insect herbivore;Evolution 40 778–785

    Article  Google Scholar 

  • Via S 1990 Ecological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems;Annu. Rev. Entomol. 35 421–446

    Article  CAS  Google Scholar 

  • Wasserman S S 1986 Genetic variation in adaptation to food plants among populations of the southern cowpea weevil,Callosobruchus maculatus: evolution of oviposition preference;Entomol. Exp. Appl. 42 201–212

    Article  Google Scholar 

  • Wasserman S S and Futuyma D J 1981 Evolution of host plant utilization in laboratory populations of the southern cowpea weevil,Callosobruchus maculatus F. (Coleoptera: Bruchidae);Evolution 35 605–617

    Article  Google Scholar 

  • Wiklund C 1975 The evolutionary relationship between adult oviposition preferences and larval host plant range inPapilio machaon L;Oecologia 18 185–197

    Article  CAS  Google Scholar 

  • Wiklund C 1981 Generalist vs. specialist oviposition behaviour inPapilio machaon (Lepidoptera) and functional, aspects on the hierarchy of oviposition preferences;Oikos 36 163–170

    Article  Google Scholar 

  • Williams K S 1983 The coevolution ofEuphydryas chacedona and their larval host plants. III. Oviposition behaviour and host plant quality;Oecologia 56 336–340

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Amitabh Joshi

    Present address: Evolution and Behaviour Laboratory, Animal Behaviour Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Jakkur PO, 560 064, Bangalore, India

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, 92717, Irvine, CA, USA

    Amitabh Joshi, Wendy A. Oshiro, Jason Shiotsugu & Laurence D. Mueller

Authors
  1. Amitabh Joshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wendy A. Oshiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jason Shiotsugu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laurence D. Mueller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amitabh Joshi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Joshi, A., Oshiro, W.A., Shiotsugu, J. et al. Within- and among-population variation in oviposition preference for urea-supplemented food inDrosophila melanogaster . J. Biosci. 22, 325–338 (1997). https://doi.org/10.1007/BF02703235

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02703235

Keywords

Search

Navigation