Genetic Variability and Robustness of Host Odor Preference in Drosophila melanogaster

Please cite this article in press as: Ruebenbauer et al., Genetic Variability and Robustness of Host Odor Preference in Drosophilamelanogaster, Current Biology (2008), doi:10.1016/j.cub.2008.08.062

Genetic Variability and Robu

Current Biology 18, 1–6, September 23, 2008 ª2008 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2008.08.062

Reportstness

of Host Odor Preferencein Drosophila melanogaster

Agnieszka Ruebenbauer,1 Fredrik Schlyter,2

Bill S. Hansson,2,3 Christer Lofstedt,1

and Mattias C. Larsson2,*1Department of EcologyLund UniversitySolvegatan 37SE-223 62 LundSweden2Department of Plant Protection BiologyDivision of Chemical EcologySwedish University of Agricultural SciencesBox 102SE-230 53 AlnarpSweden3Department of Evolutionary NeuroethologyMax Planck Institute for Chemical EcologyHans-Knoll-Straße 8D-07745 JenaGermany

Summary

Chemosensory stimuli play a crucial role for host selectionin insects, including the fruit fly Drosophila melanogaster

[1]. Drosophila has been instrumental in unraveling the neu-rological basis of olfactory processing in insects [2]. Basic

knowledge regarding chemical ecology and thorough stud-

ies of olfactory preferences are still lacking to a great extentin D. melanogaster, however. We have characterized repeat-

able variation in olfactory preference between five classicalD. melanogaster wild-type strains toward a large array of nat-

ural host odors and synthetic compounds. By recording therate of attraction over up to 24 hr, we could compare stimuli

varying in attractiveness and characterize phenotypic pa-rameters on the basis of individual stimuli and the whole

stimulus array. Behavioral differences between strainswere predominantly due to variation in a single phenotypic

parameter: their overall responsiveness toward optimaland suboptimal olfactory stimuli. These differences were

not explained by variation in olfactory sensitivity, locomo-tory activity, or general vigor monitored by survival.

Comparisons with three recently established wild-typestrains indicated that a high behavioral threshold against

accepting suboptimal olfactory stimuli is the characteristicphenotype of wild D. melanogaster.

Results and Discussion

Responses of Strains to Natural and Synthetic Odors

Initially, we studied behavioral responses of five classical wild-type strains, Canton-S, Oregon R-C, Oregon R-S, Berlin-K, andwild-type Berlin (Table S1 available online), to a large set ofnatural and synthetic odors (Figure 1). Monitoring of attractionover an extended time period demonstrated extensive

*Correspondence: [email protected]

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temporal variation in olfactory-guided behavior between Dro-sophila wild-type strains. Much of these dynamics wouldprobably be overlooked unless monitored over time scalesthat encompass the full range of responses. Most stimuli eli-cited a positive attraction index within 24 hr. From the tempo-ral response patterns it is apparent, however, that the odorsdiffer greatly in their ability to induce attraction.

Natural stimuli were very attractive to the flies, but elicitedsignificantly different responses from various strains overshorter time intervals (Figure 1A). Only banana and mango eli-cited more or less uniform responses from all strains; other-wise the Berlin-K (BK) and wild-type Berlin (WTB) strainsconsistently displayed slower responses (Figure 1A andFigure S1). Responses to synthetic attractants were overallmuch slower than to natural stimuli, and differences betweenstrains were often more pronounced (Figure 1B). However,some compounds elicited slow but consistent attractionfrom all strains; (E)-2-hexenal was more or less neutral,whereas the two phenols, 3-octanol, and benzaldehyde werealways avoided (Figure S2). WTB and BK were much more se-lective than the other strains in their responses to syntheticstimuli, sometimes showing only barely significant attractioneven after 24 hr (Figure 1B). Lowering the concentration of re-pulsive odors one to two decadic steps generally changedtheir effect to neutral (data not shown). This dichotomy be-tween different types of attractive and repulsive stimuli agreesrelatively well with results obtained from other choice assays[3–7] but not from a recent arena assay [8].

Comparisons between starved and nonstarved animalsstressed the importance of the physiological state of the fliesfor their willingness to respond and accentuated differencesbetween natural odor blends and synthetic compounds as ol-factory stimuli (Figure S3). In the assays, we could not quantifyany aspect of fly behavior apart from trapping events. Obser-vations of the test chambers during hourly checks indicatedvery few general differences in fly behavior regardless of strainand treatment, and we rarely observed apparent directed-search behavior to any stimulus.

Control Experiments: EAG, Locomotion, and Survival

Electroantennographic (EAG) responses to four different syn-thetic stimuli (acetoin, ethyl hexanoate, ethyl acetate, andmethyl salicylate) and vinegar were not different among thestrains, indicating that all strains had the same ability to detectolfactory stimuli (Figure 2A). Electroantennographic record-ings cannot exclude minor differences that could be revealed,e.g., by single sensillum recordings but do indicate that overallsensitivity remains the same.

We also performed a series of control experiments to ex-clude unspecified factors that could explain differences in be-havioral responses. Differences in locomotory activity couldpotentially affect trap catch, but a simple line-crossing assayrevealed no differences in spontaneous locomotory activity(number of line crosses) between strains (means 6 SD: Can-ton-S 19.9 6 3.3; Oregon R-C 20.4 6 2.6; Oregon R-S 20.1 63.1; BK 20.3 6 2.9, WTB 20.0 6 3.2; ANOVA F = 0.2, 4 d.f.,p > 0.95). Survival experiments under conditions of unlimitedaccess to food and under starvation conditions revealed no

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Figure 1. Response of Five Classical Wild-Type Strains to Selected Natural and Synthetic Stimuli

Variation in attraction of five D. melanogaster classical wild-type strains over time (0–8 hr and 24 hr) to a panel of selected olfactory stimuli. (A) shows re-

sponses to selected natural stimuli, including several fruits, yeast, and balsamic vinegar. (B) shows responses to selected synthetic single compounds.

Graphs show mean attraction index 6 SD. n = 5. Triangles show the time points selected in a stepwise discriminant analysis to find the greatest overall

differences between strains. Responses to the full range of natural and synthetic stimuli are found in Figures S1 and S2.

Current Biology Vol 18 No 182


apparent differences, in general vigor between strains, thatcould explain differences in behavioral responses (Figure 2B).

What Is the Natural Behavioral Phenotype of Drosophila?

Finally, we repeated behavioral experiments with the five clas-sical strains in parallel with three newly established strains,Dalby-HL (D-HL), Helsingborg-E (HB-E), and Helsingborg-F(HB-F), to four diagnostic stimuli in order to determine whichof the classical wild-type strains (if any) displayed the most‘‘natural’’ behavioral phenotype. The newly established strainswere consistently the most conservative in their choices, withbehavioral responses as low as or lower than the most selec-tive classical wild-type strains (WTB and BK) (Figure 3). Behav-ioral responses from the five classical wild-type strains weresimilar to those previously obtained from these strains (Fig-ure 1, Table 1). Repeatability estimates (r) [9] for three of thestimuli (lemon, ethyl acetate, and acetic acid) retested withthe same five strains were very high (0.98–0.99) [10]. The ex-ception was rotten banana, which was attractive to all strains,resulting in lower between-strain variation.

Behavioral differences between the classical wild-typestrains probably reflect genetically determined preferencesrather than differences in olfactory sensitivity, locomotion, orgeneral vigor. Nevertheless, the most extreme differencesfound between wild-type strains in our study appear to becomparable in magnitude to effects caused by severe ablation

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of receptor neurons [11] or to some of the variations foundbetween different Drosophila species [12]. The picture emerg-ing from our results is that the natural phenotype of D. mela-nogaster is very selective in its attraction to host odors, justlike most other insects, by virtually ignoring single compo-nents of host odor blends in comparison with the complex odorblends. The relatively low selectivity displayed by the twoOregon strains and Canton-S, whose responses to somesynthetic stimuli approached the levels exhibited to naturalfruit odors, stands in stark contrast to the more conservativenatural phenotype.

Behavioral Variation and Host ChoiceHost and mate choice in insects are governed by highly spe-cific chemosensory cues [13–15], with minor changes to thesignal often greatly affecting behavior [16–18, 14]. Host choiceis a complex event involving attraction to blends of com-pounds characteristic of individual or alternate hosts, in paral-lel with avoidance of compounds characteristic of nonhosts orunsuitable hosts [19, 20]. Chemosensory preferences in com-bination with physiological adaptations determine the hostrange [21]. Local adaptations in host preference can occureven on a microhabitat scale, causing a degree of habitat fidel-ity and transient, partial reproductive isolation [22]. A host-choice event could be regarded as the product of at least twocombined processes, however: evaluation of stimuli according

Figure 2. Control Experiments: Electroantennographic Responses and Survival in Five Strains

(A) Comparisons of electroantennographic (EAG) responses from five D. melanogaster classical wild-type strains. The left shows responses to acetoin, ethyl

hexanoate, ethyl acetate, methyl salicylate, and vinegar (mean net amplitude 6 SD. n = 10, pooled response from five males and five females). There were no

significant differences between strains or sexes in their EAG responses to any stimulus. The right shows examples of responses to selected stimuli: water

(control), acetoin, and balsamic vinegar.

(B) Survival curves for five D. melanogaster classical wild-type strains (CS, OR-C, OR-S, WTB, and BK) over time (means 6 SD; n = 12; pooled response from

six vials with males and six with females; each vial started with ten flies). The left panel shows survival under conditions of unlimited food supply. The right

panel shows survival under starvation conditions, in which flies were provided with water only.

Genetic Variability in Host Odor Preference3


to a preference hierarchy, followed by a choice to accept or re-ject an individual host according to the degree of selectivity orchoosiness [23]. This study represents the first large-scale at-tempt to characterize behavioral variation in this adaptive con-text and is thus fundamentally different from olfactory behaviorin D. melanogaster on the basis of simple operational parame-ters such as avoidance of a single olfactory stimulus [24–26].

We have shown that strains differed primarily in their overallresponsiveness toward different olfactory stimuli (Figure S4).The fruits used here all constitute acceptable oviposition sitesfor D. melanogaster, eliciting a high degree of attraction.Whereas banana and mango were highly attractive to allstrains, other fruits were accepted to a lesser degree primarilyby the Berlin strains and the newly established strains. Thegreatest differences between wild-type strains were found intheir responses to some of the single synthetic compounds.

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Responses to single compounds rarely approached those tocomplex blends from natural odor sources. The natural envi-ronment for the fruit fly consists of fermenting plant materialrich in ethanol and other alcohols, acids, acetone, fruit esters,and highly volatile esters such as ethyl acetate. Acetoin isa metabolic product of bacteria involved in fermentation pro-cess in the presence of glucose or other fermentable sourceof carbon [27]. The synthetic stimuli thus constitute potentiallyrelevant stimuli for the flies, but each represents a degradedand suboptimal signal, containing only part of the informationpresent in the complete volatile profile of the natural stimuli(see also [28]).

Preference Hierarchies and Host Shifts

Factorial ANOVA with a selected time point for each stimulusalways revealed strong effects of both stimulus and strain,

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Figure 3. Response of Five Classical and Three New

Strains to Four Diagnostic Stimuli

Attraction of eight D. melanogaster wild-type strains

(CS, OR-C, OR-S, WTB, BK, and the newly estab-

lished D-HL, HB-E, and HB-F) over time (0–8 hr and

24 hr) to a diagnostic set of two natural and two syn-

thetic stimuli. Graphs show mean attraction index 6

SD. n = 5. Triangles show the time points selected in

a stepwise discriminant analysis to find the greatest

overall differences between strains.



as well as interactions between these two factors, within allthree data sets (Tables S3 and S4). Interactions suggest thatstrains exhibit differences in their relative attraction to olfac-tory stimuli. Overall preference hierarchies nevertheless ap-pear rather robust between strains (Figure 1). Although thereis obviously great variation between strains in their respon-siveness to suboptimal olfactory attractants, they also seemto have retained most of their basic wild-type preferences.Other examples from mate- and host-choice systems also in-dicate that overall preference hierarchies and selectivity maybe independently selected. Males of the cabbage loopermoth Trichoplusia ni, selected to respond to a new mutantpheromone blend, responded to both the new and the oldblend [29]. Host preference hierarchies of the swallowtail but-terfly Papilio zelicaon remained the same in populations thatused different host plants [30]. Insects in laboratory culturescan quite easily be selected to oviposit on artificial diets, oreven completely artificial substrates such as paper, over justa few generations but nevertheless prefer the ancestral host([31] and unpublished data). These examples suggest a widen-ing of the response window rather than a change of prefer-ences. In contrast, different host races of the apple maggotfly Rhagoletis pomonella represent a true reversal in prefer-ence, in which each host race avoids the host of the otherrace [32]. The combined evidence suggests that indiscriminateindividuals may be favored during the initial phases of behav-ioral shifts, whereas a reversal in preference may require a con-siderably longer selection process.

Genetics and Behavioral ConsistencyA strong genetic component determining olfactory prefer-ences should yield strong associations between genetic simi-larity and behavioral responses, and perhaps also consistencyof responses over different types of stimuli. Principal compo-nent analysis suggested rather high overall consistency in

Table 1. Repeatability of Responses of Five Classical Strains to Four Diagnostic Stimuli

Stimuli n0 Among MSA Within MSW s2A

Acetic acid 1% 2 0.501 0.0044 0.248

Ethyl acetate 1% 2 1.471 0.0021 0.734

Lemon 2 0.604 0.0017 0.301

Banana, rotten 2 0.021 0.0056 0.008

a r = s2A/(s2 + s2

A), calculation according to Lessells and Boag [9]. Comparison of within-strain and be

group size, n0) with the same stimulus, at the time point selected as most different in our stepwise disc

MSW and s2, mean squares within groups, and s2A, among-groups variance component.

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clustering between different strains on thebasis of their responses to different odorarrays at selected individual time points(Figure 4). Genetic differences betweenthe strains used in this study could be

caused by geographical variation [33], sampled substrate[22], random founder effects, genetic drift, and selection incaptivity. Presumably, a lower degree of selectivity is causedby factors associated with captivity. The conservative behav-ioral phenotypes of our recently established wild-type strains(D-HL, HB-E, and HB-F) would then represent a universal be-havior characteristic of wild D. melanogaster, resembledmost closely by the WTB and BK strains among the classicalwild-type strains. The domestication process itself does notnecessarily cause low selectivity, however, given that theBerlin strains still retain a wild-type-like phenotype aftermany decades in captivity.

ConclusionsBy monitoring adaptive responses over time, we have de-tected differences in olfactory preference among wild-typestrains, which to a great extent could be attributed to varia-tions in a single phenotypic parameter: their overall respon-siveness toward optimal and suboptimal olfactory stimuli.We have demonstrated that low attraction scores to individualsynthetic test stimuli in our trap assays is not a symptom ofolfactory defects but rather an adaptive selectivity typicalfor wild D. melanogaster. Similar differences are likely to beimportant in any comparison between genotypes in an uncon-trolled genetic background and should not be underestimated.

Experimental Procedures

Experimental Animals

We used five different previously cultured wild-type strains (here referred to

as classical wild-type strains), Canton S, Berlin-K, Oregon R-C, Oregon R-S,

and wild-type Berlin (Table 1) and three recently established wild-type

strains, Dalby-HL, Helsingborg-E, and Helsingborg-F.

Trap Assays

The trap assay is a variation on choice assays that have been used to deter-

mine differences in odor-guided behavior between different genotypes or

F Sign. ra

114.6 *** 0.983

692.0 *** 0.997

355.1 *** 0.994

3.8 * 0.582

tween-strain variation over two separate trials (mean

riminant analysis. MSA, mean squares among groups,

Figure 4. Overall Similarity in Preference in Five and Eight Strains on the

Basis of Multivariate Analysis

Principle component analysis to separate different strains on the basis of

their similarity of responses to three different sets of stimuli at selected

time points. In each case, separation is based on two aggregated compo-

nents, which together explained >90% of the total variation. (A) shows

a comparison between five strains (CS, OR-C, OR-S, WTB, and BK) on the

basis of responses to all natural stimuli. The axes have been inverted (mul-

tiplied by 21) for better spatial alignment of the results to the other two data

sets. (B) shows a comparison between five strains (CS, OR-C, OR-S, WTB,

and BK) on the basis of responses to synthetic stimuli. (C) shows compari-

son between all eight strains (CS, OR-C, OR-S, WTB, BK, and the newly

established D-HL, HB-E, and HB-F) to a set of four diagnostic stimuli (two

fruits and two synthetic compounds).

Genetic Variability in Host Odor Preference5


species of Drosophila [34, 12]. Test chambers (high, plastic Petri dishes,

with a ventilation hole in the lid, covered with a thin mesh) contained a treat-

ment and control trap made from small glass vials with a cut micropipette tip

inserted into the opening. The number of flies in the transparent test cham-

ber and in either of the traps was counted at every hour during the first 8 hr

and after 24 hr. Attraction to olfactory stimuli was calculated on the basis of

the following attraction index, AI:

AI = ðT 2 CÞ=ðT + C + OÞ

where T = number of flies in the treatment trap, C = number of flies in the

control trap, and O = number of flies outside the traps in the test chamber.

Results of the trap assays were presented as mean attraction index of five

independent repetitions 6 SD.

For natural stimuli, we used yeast solution, dilute balsamic vinegar, and

six different fruits: apple, banana, mango, orange, lemon, and strawberries,

in both fully ripe and rotten forms. For synthetic stimuli, we selected 17

odorants (Table S2) tested at 0.1% and 1% dilutions. The odorants were

chosen to represent a broad sample of ecologically relevant odors such

as fruit and fermentation volatiles and odors that are known effective ligands

for olfactory receptor neurons in D. melanogaster [35, 36].

Statistical Treatment of Behavioral Data

For statistical analysis to draw general conclusions from the whole material,

we collapsed original data sets (12,240 cases) into a series of data points

consisting of a single selected time point for each stimulus, in which the

strains showed the greatest difference in response. This was determined

by a stepwise discriminant analysis (STEPDISC in SAS, DISCRIMINANT in

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SPSS), in which a one-way ANOVA was used to quantify differences be-

tween the strains at each individual time point.

Supplemental Data

Supplemental Data include Supplemental Experimental Procedures, four

figures, and four tables and can be found with this article online at http://

www.current-biology.com/cgi/content/full/18/18/---/DC1/.

Acknowledgments

We are indebted to Jan-Eric Englund for invaluable contributions to the sta-

tistical analysis. Newly established fly lines were obtained from Lena Ever-

tsson, Lie Fredholm, Roger Hardling, and Asa Lankinen. Fly stocks were ob-

tained from the Bloomington Stock Center and from Bjorn Brembs (WTB).

Funding was provided by the Crafoord Foundation (to M.C.L.), the Trygger

Foundation (to M.C.L.), Vetenskapsradet (The Swedish Science Council) (to

C.L. and B.S.H.), and the Linnaeus Initiative ‘‘Insect Chemical Ecology,

Ethology, and Evolution’’ (ICE3).

Received: June 13, 2008

Revised: August 4, 2008

Accepted: August 15, 2008

Published online: August 18, 2008

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Genetic Variability and Robustness of Host Odor Preference in Drosophila melanogaster

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